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Behavioral Ecology Symposium '94: Frank & McCoy Intro. 1
INTRODUCTION TO
INSECT BEHAVIORAL ECOLOGY : THE GOOD, THE BAD, AND
THE BEAUTIFUL: NON-INDIGENOUS SPECIES IN FLORIDA
INVASIVE ADVENTIVE INSECTS AND OTHER ORGANISMS IN
FLORIDA.
J. H. FRANK' AND E. D. MCCOY2
'Entomology & Nematology Department, University of Florida,
Gainesville, FL 32611-0620
2Biology Department and Center for Urban Ecology, University of South Florida,
Tampa, FL 33620-5150
ABSTRACT
An excessive proportion of adventive (= "non-indigenous") species in a community
has been called "biological pollution." Proportions of adventive species of fishes, am
phibia, reptiles, birds and mammals in southern Florida range from 16% to more than
42%. In Florida as a whole, the proportion of adventive plants is about 26%, but of in
sects is only about 8%. Almost all of the vertebrates were introduced as captive pets,
but escaped or were released into the wild, and established breeding populations; few
arrived as immigrants (= "of their own volition"). Almost all of the plants also were in
produced, a few arrived as immigrants (as contaminants of shipments of seeds or
other cargoes). In contrast, only 42 insect species (0.3%) were introduced (all for bio
logical control of pests, including weeds). The remainder (about 946 species, or 7.6%)
arrived as undocumented immigrants, some of them as fly-ins, but many as contami
nants of cargoes. Most of the major insect pests of agriculture, horticulture, human
made structures, and the environment, arrived as hitchhikers (contaminants of, and
stowaways in, cargoes, especially cargoes of plants). No adventive insect species caus
ing problems in Florida was introduced (deliberately) as far as is known.
The cause of most of the so-called biological pollution is the public's demand for
pet" animals and "ornamental" plants of foreign origin, the public's environmental ir
responsibility in handling these organisms, the dealers' willingness to supply these
organisms for cash, and governments' unwillingness to stem the flow of a lucrative
commerce. The cause of almost all of the remaining part is flight, walking, swimming,
and rafting from adjoining states and from nearby countries in the Caribbean, Mexico
and Central America. The introduction of specialized insect biological control agents,
although it contributes to biological pollution, appears to be an environmentally
sound solution to the much greater biological pollution caused by immigrant insects
and introduced plants in Florida. Greater concern for insects as living things, or as in
tegral parts of nature, coupled with increased understanding of how problem insects
get into Florida, may foster a more even-handed approach to the reduction of biologi
cal pollution.
Key Words: Adventive species, biological pollution, immigrant species, insects and
commerce, introduced species.
RESUME
Una proporci6n excesiva de species foraneas (=no indigenas) en una comunidad
ha sido denominada "poluci6n biol6gica". Las proporciones de species foraneas de pe
ces, anfibios, reptiles, aves, y mamiferos en el sur de la Florida varian del 16 al 42%.
En la Florida en su totalidad, la proporci6n de plants foraneas es de alrededor del
This article is from Florida Entomologist Online, Vol. 78, No. 1 (1995).
FEO is available from the Florida Center for Library Automation gopher (sally.fcla.ufl.edu)
and is identical to Florida Entomologist (An International Journal for the Americas).
FEO is prepared by E. O. Painter Printing Co., P.O. Box 877, DeLeon Springs, FL. 32130.
Florida Entomologist 78(1)
26%, mientras que la de insects es de solo el 8%. Casi todos los vertebrados han sido
introducidos como animals de compania, los cuales escaparon o fueron soltados en
espacios naturales y se establecieron como poblaciones reproductivamente viables.
Muy pocas species llegaron como inmigrantes (= "por su propia voluntad"). Casi to
das las plants han sido introducidas, pero llegaron como inmigrantes o como conta
minantes en importaciones de semillas. Sin embargo, solo 42 species de insects
(0.3%) han sido introducidos y todos como control biol6gico de plagas, incluyendo ma
las hierbas. El resto (aproximadamente 946 species, 6 7.6%) lleg6 como inmigrantes
desconocidos, algunos de ellos volando y muchos como contaminants en cargamen
tos. La mayoria de los insects perjudiciales para la agriculture, horticulture, cons
trucciones humans y el medio ambiente llegaron como "polizones" contaminantss
de, almacenados en, cargamentos, especialmente cargamentos de plantss. Parece ser
que ningfn insecto foraneo que cause problems en la Florida fue introducido (delibe
radamente).
La causa mayor de la llamada poluci6n biol6gica es la demand del pfblico de ani
males de compania y plants ornamentales de origen extranjero, la irresponsabilidad
del pfblico manejando estos organismos, la avidez de los comerciantes en proporcio
nar dichos organismos a cambio de dinero y la reticencia de los gobiernos en cortar la
avalanche de negocios lucrativos. Las causes del resto de la poluci6n biol6gica estan
fundamentadas casi en su totalidad en el desplazamiento en vuelo, por via terrestre,
a nado y en estructuras a la deriva desde los paises vecinos caribenos, Mexico, y Cen
tro America. La introducci6n de insects especializados en el control de plagas, aun
que contribuya a la poluci6n biol6gica, parece ser una soluci6n medioambiental de
peso al problema mas grave de la poluci6n biol6gica producida por los insects y plan
tas llegados a la Florida como inmigrantes. Una preocupaci6n mayor por los insects,
como entidades vivas, o como parties integrales de la naturaleza, emparejada con un
incremento en el conocimiento sobre c6mo los insects problematicos entran a la Flo
rida, puede favorecer una estrategia mas equilibrada para la reducci6n de la poluci6n
biol6gica.
Florida's flora and fauna are threatened by a burgeoning human population, ap
preaching 14 million, with a growth rate triple that of the USA during the last decade.
By the year 2020, this population could grow to 23 million. The Everglades are said
to be dying due to water shortage and pollution. Florida Bay, at the tip of the penin
sula, is threatened by enormous algal blooms said to be due to pollution from agricul
tural lands, and more than 40,000 ha of seagrasses and sponges are dead. Coral reefs
are said to be dying from pollution and disturbance. Of 25 shrimp boats operating
from Marathon in the early 1970s, there now are none. In the Tampa Bay area, well
fields have been over-pumped, drying up thousands of hectares of wetlands. In central
Florida, lakes are said to be polluted with pesticides, causing, for example, a dramatic
drop in the largemouth bass population and a 90% decline in the alligator population
of Lake Apopka. On the east coast, from Fernandina Beach in the north to Miami
Beach in the south, coastal erosion is said to be fueled by overpopulation: about $450
million have been spent pumping sand onto beaches since 1965 to replace the tons
eroded by storms. Pollution in the Gulf of Mexico has made bacterial infection from
eating raw oysters a frequent health risk. The conch population in the Caribbean has
declined by 90% in the past 20 years, and edible marine fish populations on the east
coast mirror this decline.
Millions of hectares of Florida no longer even remotely resemble a pristine state.
They are now urban landscapes with buildings and roads and ornamental plants, or
March, 1995
Behavioral Ecology Symposium '94: Frank & McCoy Intro. 3
agricultural landscapes modified to support the human population, or salt marshes
modified to suppress their natural mosquito populations so that humans will not be
bitten. All of these changes have supplanted the natural plant and animal popular
tions. All major agricultural crops, farm animals, and popular pet animals in Florida,
from citrus to corn to cattle to cats, are introduced. Of all plants of foreign origin that
are imported into the USA, 85% arrive through Miami International Airport. Miami
also is the busiest US port for fish and wildlife. The root cause of what has been
termed the "biological pollution" (McKnight 1993) of Florida is the public's desire for
animals and plants of foreign origin, the public's environmental ii. I 1il..11 deal
ers' ability to earn money by satisfying this desire, and governments' unwillingness to
intervene substantially in this profitable commercial activity (Belleville 1994).
In southern Florida, especially, untrammeled whims of humans have introduced
so many species of non-farm animals (mainly as "pets") that the native fauna is
greatly diluted. Running wild in Dade and Broward Counties have been piranhas,
walking catfish, blue tilapia ("introduced from Africa in 1961 by officials of the Game
and Freshwater Fish Commission"), electric eels, little barbed Amazonian catfish that
swim up [human] urinary tracts, and other fish ("23 exotic fish now breeding in the
wild"), Cuban anoles, iguanas, Asian water monitors, caimans, boa constrictors, py
thons, mambas ("people want the newest animals as pets"), red-whiskered bulbuls,
monk parakeets, howler monkeys, gibbons, green African savannah monkeys, crab
eating macaques, and a herd of 300 buffalo (Belleville 1994). Nine years ago, the
fauna of southern Florida included the following percentages of species introduced al
most entirely by the pet trade: fishes (16%), amphibians (22%), reptiles (42%), mam-
mals (23%) (Ewel 1986). The percentage of birds is obscured under a category called
"free-flying exotics" but, with 16-17 species of parrots and many other species estab
lished, it may exceed the percentage of any of the other classes. Recent estimates com-
piled for all of Florida (US Congress 1993) suggest the percentages of established
adventive vertebrate species exceed 20% for most groups. Many such "pet" animals
escaped from their owners, or were released I. I1... I ii. I, into the wild. Animals
shipped from Florida also have caused problems. For example, red-eared turtles are
shipped to France, Belgium, the Netherlands and Germany; over 500,000 individuals
are shipped to France alone per year. Some inevitably escaped into the wild where
they displaced native turtles (Simons 1994).
Importers of non-crop plants (mainly as "ornamentals") likewise have contributed
to dilution of the native flora. Among the worst weeds (Exotic Pest Plant Council
1993) are punk trees, introduced to Florida "to drain wetlands"; water hyacinth, "im
ported for its pretty, orchidlike blossom"; hydrilla, "a frilly little plant in aquariums";
and Australian pine, "introduced as an ornamental" (Belleville 1994); others include
Brazilian pepper, kudzu vine, and cogon grass, all introduced (deliberately). The
USDA and Fairchild Botanical Gardens had active programs to introduce tens of
thousands of plants of foreign origin for no reason essential to human existence. At
present, about 27% of the total established flora of Florida is comprised of adventive
species (Table 1). Waiting in the wings, some 25,000 introduced plant species are
grown in cultivation, but are not yet established in nature (Table 1). Florida is not
only a beneficiary of plants of foreign origin, but a donor, and it also donates pest in
sects infesting ornamental plants (Miller 1994).
The purpose of this introduction is to show what problems adventive species of in
sects cause in Florida (also see US Congress 1993). These species are placed into a
framework that categorizes them to show which ones were introduced, and estimate
how many arrived without invitation, i.e., were immigrants. We also pose some
philosophical questions about introductions of insects and other organisms to Florida.
Florida Entomologist 78(1)
TABLE 1. A COMPARISON OF THE FLORIDA FLORA AND FAUNA
Type Plants Insects
Indigenous species 2,525" 11,512'
Adventive species
Species immigrant to Florida and established in nature 0' 946'
Species introduced to Florida and established in nature 925`' 42d
Species now cultivated, but not established in nature 25,000b 5e
"after Ward (1989), after comments by David Hall and Thomas Sheehan, estimates explained in Frank & Mc
Coy (1995), biological control agents, after Frank & McCoy (1993), house crickets and mealworms as fishbait,
honey bees, silkworms, and a mantis, 'some of the plants reported by Ward (1989) as "introduced" may, in fact,
be immigrants, because it is scarcely conceivable that some of the weeds among them were introduced deliber
ately, and their seeds may have arrived on the wind, in sea-drift, or as contaminants of shipments of other seeds
or materials.
THE CURRENT STATUS OF ADVENTIVE INSECT SPECIES IN FLORIDA
Nomenclature
A distinction is made in this paper between immigration and introduction, fol
lowing Frank & McCoy (1990). Immigrants arrive of their own volition, even if as
stowaways in cargoes, and have no permit for their entry into Florida. The word in-
troduced is restricted to purposely-introduced species, following Zimmerman (1948).
A Florida permit (DPI-FDACS) is now required for introduction of any insect spe
cies into Florida, and in many examples a federal permit (USDA-APHIS-PPQ or
USDA-APHIS-VS or USPHS-CDC) also is required. Adventive species (elsewhere
called non-indigenous species) are those that immigrated together with those that
were introduced.
Recognition of Adventive Species
Assessment of adventive insect species in Florida is complicated by a very imper
fect knowledge of indigenous species (see Frank & McCoy 1995). There is no baseline
information on insects from the time of the rediscovery of the Americas by Columbus,
nor from the time of the American revolution. Only for a few (mainly pests) is there
information from even 100 years ago, and some are not yet recorded at all. There are
now manuals on the Florida species of a few insect families. An enormous amount of
taxonomic research still is required, especially on species that are not pests. This re
search is progressing at a snail's pace because it has little popular appeal, and public
funds to support it are virtually unavailable.
The extreme south of Florida presents a special problem as to which species are
adventive. Many West Indian insects inhabit the Florida Keys and adjacent main
land. The major part of the range of these species is in Cuba or other islands, and they
also inhabit a small part of Florida. Lack of baseline data for some species from 20
years ago, much less 200 years ago, makes it impossible to state how long they have
been in Florida. Some species undoubtedly become extinct in Florida from time to
time, and then recolonize by flight and winds from the south. Six of them are butter
flies: Chlorostrymon maesites Herrich-Schaeffer, Eunica tatila Herrich-Schaeffer,
Strymon acis Drury, Eumaeus atala Poey, Heraclides aristodemus (Esper), and Anaea
March, 1995
Behavioral Ecology Symposium '94: Frank & McCoy Intro. 5
troglodyta F. Other insect species are so poorly studied that when they are reported
for the first time from Monroe County or Dade County, they are recorded as immi
grants simply because there is no earlier information. However, the six butterfly spe
cies are listed among Florida's rare and endangered invertebrate animals. There is
unequal treatment under the law because butterflies have popular appeal, so there is
more information about them. Inadequate knowledge of the insect fauna of Cuba and
the Bahamas compounds the problem. Florida-based entomologists were discouraged
for years from working in Cuba for political reasons.
Records of Adventive Species
Systematic knowledge about Florida's insect fauna is woefully inadequate (see Ha
beck 1987), because the almost exclusive demand from the public has been on meth
ods for controlling pest species. No agency of the Florida government has a program
providing grants for taxonomic research on non-pest species of insects. Although
these insects are considered to be wildlife by the US Fish and Wildlife Service (US
FWS), they are not considered to be wildlife by the Florida Game and Fresh Water
Fish Commission (FGFWFC). Consequently, the Non Game Wildlife Program of FG
FWFC rarely makes funds available for research on them. Professional entomologists
were hired in Florida almost entirely to solve problems caused by pest insects. The
Florida Department of Agriculture and Consumer Services (FDACS) responded to the
need for knowledge on insect fauna in general by housing the Florida State Collection
of Arthropods in Gainesville, by paying publication costs for taxonomic work on non
pest species (should someone be willing to write them), and by encouraging donation
of specimens to the collection. The Institute of Food and Agricultural Sciences of the
University of Florida pays publication costs for work by students and employees on
non-pest species, but does not encourage such research.
As a consequence of the emphasis on pest insects, families containing pests [e.g.,
Culicidae (mosquitoes) and Diaspididae (armored scale insects)] are well known, but
families containing mostly innocuous insects are not. The sole exception is the group
of families (Nymphalidae, Papilionidae, Pieridae, etc.) called butterflies. Therefore,
there is no thorough catalog of the insect fauna of Florida. Although many hundreds
of immigrant species now exist in Florida, they are yet a fairly small percentage (un
der 9%) of the total number of species (Table 1). For example, only four of the 78 mos
quito species are immigrants (Frank & McCoy 1995). The proportion is likely to be
higher among plant-feeding insects than among non-plant-feeding insects, because
many pests of plants have immigrated with imported shipments of plants. The pro
portion of introduced species is less than half of 1% (Table 1).
Extremely few populations of insect species are monitored routinely in several
Florida localities: almost the sole exceptions are some mosquitoes. Most populations
are noticed only when their numbers are very high, and cause damage to ornamental
plants, crop plants, structures, livestock, and other human possessions. The task of
annual monitoring of more than 12,500 insect species (Frank & McCoy 1995) is vastly
beyond current capabilities, so there is virtually no information on most adventive in
sects in Florida.
Recognition that many of the major pests of North American crops were adventive,
and probably had immigrated with infested shipments of plants, led to the Federal
Plant Quarantine Act of 1912 (Sailer 1978). The act was designed to bar the importa
tion of cargoes infested with plant-feeding insects, through inspection at ports. Much
harm had already been caused to agriculture by such immigrant pests. Implementa
tion of the law, however, merely slowed the establishment of immigrant insect species,
Florida Entomologist 78(1)
and did not prevent it (Sailer 1978). USDA-APHIS inspectors at US ports and air
ports in fiscal year 1980 intercepted over 18,000 infested shipments (Frank & McCoy
1992).
Unlike the northern parts of the USA, Florida contends not only with infested
shipments, but also with flight of insects from the West Indies. Assessment of the lit
erature showed 271 immigrant insect species reported for Florida for the first time be
tween 1971 and 1991 (Frank & McCoy 1992). These were living in Florida when
found, and the information gives a rough measure of the current rate of establishment
of immigrant species. Relatively few insect species are introduced under permit
(Frank & McCoy 1993, 1994).
Major Pathways of Arrival of Adventive Species
Immigrant species: fly-ins. Florida's northern and western borders are permeable
to flying and walking insects. Many of Florida's insect species (including pests) are
shared with neighboring states for this reason. A familiar example is the love bug
(Plecia nearctica Hardy). This is a Mexican and Central American species which ex
tended its range to include the Gulf Coast of the USA. Moving into Florida from Ala
bama in 1949, its population spread to southern Florida in 1975 (Buschman 1976). A
large proportion of the insect species of southern Florida arrived by flight, perhaps as
sisted by winds, from the West Indies, the Bahamas, and the Yucatan peninsula of
Mexico. Even wingless species may have arrived by rafting on floating driftwood. Ar
rival of additional species by flight will continue indefinitely. An aphid which may ar
rive soon from Cuba (it colonized Cuba from Central America), is Toxoptera citricida
(Kirkaldy), a vector of tristeza disease of citrus. There is no way of preventing such
immigration, although some immigrants from the south, if detected soon after they
arrive, may be eradicated by use of chemicals.
Immigrant species: stowaways. More than 25,000 adventive species of plants now
grow in Florida (Table 1). Every imported shipment of plants offers opportunity to
plant-feeding insects to immigrate as stowaways. Despite the efforts of shippers and
inspectors, such plant-feeding insects continue to immigrate. These insects tend to be
the most important pests of the introduced plants, but some of them turn their atten
tion to related, indigenous plants. Thousands of shipments are discovered every year
to contain insect stowaways, but only a tiny percentage of shipments is inspected at
ports and airports. Furthermore, Miami International Airport receives 85% of all
shipments of plants to the USA. These, along with shipments of other kinds of cargoes
that arrive by air, sea, and land, have been, and continue to be, the main method of
immigration of Florida's most important adventive pest insects (Frank & McCoy
1992).
Introduced species: commerce in insects. There has been enormous commerce in in
produced plants, and some of these plants have become weeds. In contrast, there has
been very little commerce in insects introduced for purposes other than biological con
trol, except for European honey bees (Apis mellifera L.) and, to a trivial extent, orien
tal silkworms (Bombyx mori L.). Much more recently, other insects, including a
Chinese mantis (Tenodera aridifolia Stoll), a Madagascan cockroach (Grom-
phadorhina sp.), a European cricket (Acheta domesticus (L.)), and a giant mealworm
of unknown origin (Zophobas sp.), have been imported and sold to the public as pets,
or for educational purposes, or as fishing bait; their owners sometimes release them
into the wild, or they escape (Frank & McCoy 1994). Some adventive butterflies are
imported for living displays by commercial butterfly zoos, but are not intended for re
lease into the wild (Frank & McCoy 1994). There is no evidence that any of these spe
March, 1995
Behavioral Ecology Symposium '94: Frank & McCoy Intro. 7
cies have established populations in nature in Florida or have caused environmental
harm. To reduce future risk from this avenue, such importations are now allowed only
after review and under permit from the Division of Plant Industry, FDACS (Florida
Administrative Code 1993).
Twenty-one insect species adventive to Florida have been imported commercially
as biological control agents since 1980. At least four of these already have established
populations in Florida, and some others are indigenous to other parts of the USA
(Frank & McCoy 1993, 1994). None of these species has been reported to cause envi
ronmental damage. Importations of biological control agents from abroad are allowed
only after Federal review and under Federal permit. Florida, virtually alone among
the States, now requires its own review and additional permit from the Division of
Plant Industry, FDACS (Florida Administrative Code 1993); furthermore, Florida re
quires this permit even for importations from other parts of the USA. It is to the ad
vantage of the companies selling biological control agents that these species do not
establish populations in Florida, or at least are not able to sustain large populations,
because such populations could eliminate or reduce repeated sales.
Introduced species: importations by government and universities for biological con
trol ofpests. These are non-commercial introductions of species which initially are im
ported under permit into secure quarantine laboratories. If, after testing, they prove
to be specific natural enemies of targeted pest species, then a second round of permits
is required before their progeny may be released into nature. Targets are pest insects
and weeds, and most of these are immigrants (Frank & McCoy 1993). This is the most
tightly regulated of all forms of introductions of animals: insects imported into Flor
ida from abroad require Federal (USDA) and State (DPI) permits for importation to
quarantine, and Federal and State permits for release into the wild. They may also
need documentation of importation as wildlife from the USFWS, and may need vari
ous export permits from their countries of origin (depending upon the laws of the
country in question).
Despite all the testing and paperwork, most introduced biological control agents
do not establish populations. Records show that 151 insect species have been released
in Florida as biological control agents, 139 of them against pest insects and 12 against
weeds (Frank & McCoy 1993). Among those that became established (34 against in
sects, 8 against weeds), some proved highly beneficial. Examples are the minute
wasps Amitus hesperidum Silvestri and Encarsia opulenta (Silvestri) that now con
trol citrus blackfly, and the flea beetle Agasicles .* .' ,'. Selman & Vogt that now
controls alligatorweed. Although regulations governing introduction of insect biologi
cal control agents were less stringent 50 years ago, none of the 42 introduced species
has been shown to have detrimental effects on the environment.
Problems Caused by Adventive Species
Immigrant insect species annually cause hundreds of millions of dollars in damage
to agriculture (including livestock and forestry), horticulture, and structures in Flor
ida. Research into these problems is supported by public and private funds, but the
system is being swamped by the high arrival rate of immigrant pests. The following
problems, especially notable because of their occurrences on public lands, are the
principal ones that we can identify. The only realistic hope for a long-term solution to
any of these problems is through introduction of biological control agents (Tschinkel
1993, Frank & Thomas 1994).
Tillandsia bromeliads. Metamasius callizona (Chevrolat) is a weevil native to
Mexico and Central America. In 1989 it was discovered on introduced bromeliads in
Florida Entomologist 78(1)
a nursery in Broward County. Surveys were made, and weevils were found on public
lands throughout Broward County and in Dade and Palm Beach Counties, and on pri
vate lands in Lee County. Populations of the indigenous bromeliad Tillandsia utricu
lata, which is protected under State law, have been decimated in Broward County
parks. The weevil also kills the indigenous Tillandsia paucifolia and Tillandsia fas
ciculata, and is too widespread to eradicate by the use of chemicals. It seems inevita
ble that populations of these protected plants will decline drastically throughout their
range in Florida (Frank & Thomas 1994), and they are candidates for listing as en
dangered.
Introduced Ficus spp. Over 60 exotic Ficus (fig) species have been introduced into
southern Florida as ornamentals. It was thought that none of these species would set
viable seed because each is pollinated only by its own species of agaonid wasp, and the
wasps were not introduced. But, Ficus altissima Blume, F benghalensis L., and F mi
crocarpa L., are now weeds because they are pollinated routinely by immigrant aga
onid wasps. Fertile seeds of these enormous trees now germinate in Dade and Monroe
counties. Seedlings sprout in public and private lands and on structures, such as high
way bridges, where they pose a maintenance problem, because they can destroy the
structures as they grow. They are invasive on public lands. There is evidence that the
pollinating wasps of Ficus microcarpa arrived in seeds brought from Hawaii, and
there is concern that fruits (and thus seeds) of the other two fig species are being
spread by introduced parrots (Nadel et al. 1992).
Endangered cacti. Cactoblastis cactorum Bergroth is a moth, native to South
America, whose larvae feed on Opuntia cacti. Introduced into Australia in 1925, it
saved 12 million acres of pasture land that had been rendered useless by infestation
with two species of Opuntia unwisely imported from the Gulf of Mexico coast. Be
tween 1957 and 1970, it was introduced into Nevis, Montserrat, Antigua, and Grand
Cayman, where Opuntia spp. were weeds. From those islands it spread to Puerto
Rico, Haiti, the Dominican Republic, and the Bahamas, and in 1989, was found in the
Florida Keys (Habeck & Bennett 1990). Unfortunately, in the Florida Keys, it places
the rare cacti Opuntia spinosissima Martyn (Mill.) and Opuntia triacantha (Willde
now) at risk. Cactoblastis probably arrived in Florida as a contaminant of Opuntia im
ported as ornamental plants. Inter-island flight or stowing away aboard boats are less
likely means of arrival. Deliberate importation as a biological control agent for Opun
tia cacti, by some member of the public, is still less likely.
Endangered morning glories. Florida's endangered species of morning glories are
Ipomoea microdactyla (Grisebach) and Ipomoea tenuissima Choisy Sweetpotato (Ip
omoea batatas Lamarck) is a relative. These plants face a new threat: the tortoise bee
tle Chelymorpha cribraria (F.) This leaf feeding beetle was discovered in Broward
County in 1993, and its range had spread to Dade County's Matheson Hammock Park
by March 1994 (Thomas 1994). The beetle is native to South America and the West In
dies. Importation of infested sweetpotato is a likely means of arrival.
Fire ants. Solenopsis invicta Buren, inaptly termed "the red imported fire ant," ar
rived in the southern USA about 1940 as an immigrant from South America. Gradu
ally it spread throughout the south, in part by flight, and in part as a contaminant of
cargoes. In agricultural ecosystems it inflicts important mortality on such pests as
sugarcane borer, boll weevil, and horn fly, but also destroys indigenous natural ene
mies of these and other pests. It has displaced populations of native ants in disturbed
habitats and it kills nestling birds, but its effect on undisturbed public lands may be
much less than on disturbed lands (Tschinkel 1993).
March, 1995
Behavioral Ecology Symposium '94: Frank & McCoy Intro. 9
Conflicts Caused by Adventive Species
The means of arrival of immigrant species often is obscure. By definition they were
not introduced under permit, so there are no records of introduction. An example is
Cactoblastis cactorum. This moth was introduced to Australia I. I.1.. I ii. I, to combat
Opuntia cacti. These plants had been introduced to Australia deliberately for horti
cultural reasons, but became invasive and caused great losses to agricultural inter
ests. Agriculture was in conflict with horticulture, but public interests were on the
side of agriculture. Introduction of the moth to Australia, and its successful control of
Opuntia, were viewed as highly beneficial.
Cactoblastis was introduced into Nevis, Montserrat, Antigua, and Grand Cayman
to suppress Opuntia on agricultural lands, and the introductions were requested by
the governments of those islands. Cactoblastis was not introduced into Puerto Rico,
Haiti, the Dominican Republic, or the Bahamas by their governments. Either the
moth was smuggled to these islands by private agricultural interests to combat Opun
tia species that were viewed as weeds, or it flew there from the other islands or hitch
hiked on boats.
The situation is more complex in Florida. Horticultural interests have imported
Opuntia cacti into Florida as ornamental plants, and some of these imported plants
are known to have been infested with Cactoblastis; this is by far the most likely means
of arrival. There are private agricultural interests that would view introduction of
Cactoblastis as beneficial to suppress Opuntia on rangelands, though its discovery in
the Florida Keys, which are not noted for agriculture, suggests that this was not the
means of arrival. But, in Florida, there are endangered Opuntia species. The interests
of agriculture, horticulture, and conservation are here in conflict. Boat traffic between
the Florida Keys and other islands gives adult moths a good possibility of hitchhiking.
There is a minor possibility that adult moths flew directly from Cuba, perhaps aided
by winds.
SOME PHILOSOPHICAL CONCERNS ABOUT INSECTS AND INSECT INTRODUCTION
IN FLORIDA
Although species of exotic vertebrates and plants have, for the most part, been in-
troduced to Florida I. 1.1.. I ii. I, adventive species of insects are predominantly im-
migrants (i.e., not deliberately introduced; see Frank & McCoy 1990 for a discussion
of these terms; also see Frank & McCoy 1992, 1993, 1994). The introduced vertebrates
and plants were brought to Florida because they were thought to possess desirable
properties, and only later did they prove to be invasive and potentially detrimental to
the native flora and fauna. The introduced insects also were brought to Florida be
cause they were thought to possess desirable properties, principally in controlling
pests. It is not clear that any of the insect species introduced to Florida for pest control
have been detrimental to the native biota, although the potential for harm clearly is
present (see Simberloff 1992, Simberloff & Stiling 1993). The potential for harm to
rare insects outside the crop environment is an especially important, although under
appreciated, consideration of classical biological control programs (Samways 1988,
1994).
The need to integrate conservation and pest control concerns raises some interest
ing philosophical-as well as practical-questions. The first has to do with insect con
servation: Is too little attention paid to insect conservation (see New 1984, Samways
Florida Entomologist 78(1)
1994)? In Florida, the official lists of endangered and potentially endangered animal
and plant (Wood 1993) taxa include 17 of fish (includes species, subspecies, and pop
ulations), 6 of amphibians, 27 of reptiles, 45 of birds, 43 of mammals, and 566 of
plants. The lists also contain 85 invertebrate taxa, of which 47 are insects. Seven or
ders are represented among the listed insect taxa: Ephemeroptera (2 taxa), Odonata
(4), Orthoptera (4), Coleoptera (19), Trichoptera (6), Lepidoptera (8), and Diptera (4).
Within the two best-represented orders, 6 of the 8 lepidopteran taxa are butterflies,
and 15 of the 19 coleopteran taxa are scarabs. One butterfly, Schaus' swallowtail, is
listed as endangered by both the USFWS and the FGFWFC; the other 46 insect taxa
are listed as C2 by USFWS, but are not listed at all by FGFWFC. The C2 listing offers
no federal protection, and means only that USFWS encourages consideration of such
taxa in environmental planning. Furthermore, the document created to allow govern
mental agencies in Florida to set conservation priorities in a reasonable way (Millsap
et al. 1990) keys only on "fish and wildlife," and, thus, does not deal with invertebrates
or plants. By implication, the omission of invertebrates, coupled with their relatively
poor representation in the official lists, suggests that persons who might be interested
in studying rare invertebrates probably are not likely to obtain funding from the
agencies who employ this document. Although the USFWS insists that insects are
"wildlife," the FGFWFC apparently has not subscribed to this inclusive definition in
the granting of funds through its Non Game Wildlife Program (with the exception of
Schaus' swallowtail). The advice to persons interested in insect conservation often is
to apply to an agricultural agency for funding, even if the kinds of insects those per
sons wish to study have nothing to do with agriculture. Finally, the attempt to set con
servation priorities in a reasonable, comparative way (Millsap et al. 1990), and
thereby to avoid use of perception, politics, and other such criteria which typically af
fect governmental lists of taxa at risk (see McCoy & Mushinsky 1992), succeeds, as
much as it does, only for vertebrates. Among insects, the few conservation efforts that
are mounted are likely to be directed at the showy, popular taxa, such as butterflies
and beetles (see Pyle et al. 1981, Samways 1994), rather than at the bland ("ugly" in
some minds), obscure taxa, despite the fact that such taxa may be equally, or even
more, threatened (see Samways 1994).
So, a case can be made that indeed too little attention is paid to insect conserve
tion. We suggest that it is important at least to recognize the possibility that a very
large and diverse group of organisms is being neglected. Insects currently suffer from
a poor public image, although they have not always done so (Frank & McCoy 1991,
Samways 1994). Unfortunately, some popular philosophical theories about nature re
inforce this poor image. For instance, individualistic theories embraced by many an
imal-rights activists (e.g., Regan 1983, Singer 1985), apart from their failure to attach
increased moral status to endangered taxa, paternalistically focus attention on crea
tures which are most like humans (see des Jardins 1993). So-called holistic philosophy
ical theories about nature offer an alternative to individualistic theories-and to
biocentric theories (e.g., Taylor 1986), as well (see des Jardins 1993). The commonly
employed philosophical and ecological bases for these holistic theories seem to be
weak, however (Peters 1991, Shrader-Frechette & McCoy 1993). Because of their
numbers and diversity-and even their utilitarian values-insects are likely to fare
well under a more holistic perspective of nature. And if so, then it follows that to em
ploy this more holistic perspective, we must better understand the ecological roles in
sects play. A first step toward increased understanding in Florida is characterization
of the habitats of very many more of the taxa indigenous to the state, especially those
that are precinctive (Frank & McCoy 1995), a process that is well under way in other
places, such as the Amazonian rain forest (T. Erwin pers. comm.).
March, 1995
Behavioral Ecology Symposium '94: Frank & McCoy Intro. 11
A second philosophical and practical question involves movements of organisms.
The question is: Are the risks of introductions of certain kinds of organisms, namely
classical biological control agents, scrutinized too closely, relative to those of other
kinds of organisms? To address the question, we must provide a little history.
Importers of insects have for years had to follow federal regulations required by
USDA-APHIS-PPQ, USDA-APHIS-VS, and USPHS-CDC. These regulations were de
signed to ensure that insects imported into the USA should not become pests; that is,
they were not likely to be phytophagous on commercially-important plants ("plant
pests"), or parasites and/or vectors of diseases of farm animals ("animal pests"), or
parasites and/or vectors of diseases of humans ("vectors"). By extension, the regular
tions were applied to phytophagous insects that were actual or potential biological
control agents of weeds, so that such insects could be imported only to approved quar
antine facilities, until further approval for release were issued. By further extension,
under nebulous authority, the regulations also were applied to entomophagous in
sects imported for biological control purposes. We shall place the insects discussed in
this paragraph in "category A."
The federal regulations applied to insects in category A never applied to many
other insects that at least had the potential to become pests. Among these other in
sects are termites, cockroaches, pests of stored products (e.g., mealworms and crickets
imported as fish bait), honey bees, silkworms, insects imported for "educational pur
poses" (e.g., certain mantids), and insects and other arthropods imported as "pets"
(e.g., certain scorpions and tarantulas). Insects, such as exotic butterflies imported by
hobbyists or insect zoos, might or might not have been considered "plant pests," but
were not required to be held in quarantine facilities regardless. While agricultural in
spectors at land-, sea, and airports examined cargoes for "plant pests" and "animal
pests," they more or less left other living arthropods alone. Further, agricultural in
spectors had no jurisdiction over the business of USPHS-CDC-which did not have its
own inspectors-so they were not required to report discovery of "vectors," such as
mosquito larvae, among shipments of plants. Still further, although agricultural in
spectors could deny entry to declared biological control agents without permit, they
did not have jurisdiction over entomophagous insects, and were not required to report
these either, so entomophagous insects could be imported by the public. In brief, there
was little or nothing to prevent members of the public from importing all kinds of en
tomophagous and other insects-so long as they were not obvious "plant pests" or "an
imal pests" and nothing to prevent these insects from being released into the
environment. Put simply, a wide variety of living insects could be imported legally and
released into the environment. Agriculture and horticulture were protected, which
was the stated purpose of the law, but the natural environment was largely unpro
tected. We shall place the insects discussed in this paragraph in "category B."
Later, EPA was empowered to regulate entry of biological control agents. By fed
eral inter-agency agreement, it was decided that USDA-APHIS was doing a good job
of regulating entry of insect biological control agents, and the EPA had no need to du
plicate the effort. But, the emphasis still was on regulation of insects in category A.
The insects in category B, that had been ignored by USDA-APHIS, were now being ig
nored by EPA.
The Florida legislature, in 1993, finally saw that all sorts of insects and other ter
restrial arthropods were entering Florida under various guises, not only from abroad,
but also from other states of the USA. It decided that all living insects and other ter
restrial arthropods that anyone wanted to import should be subject to evaluation and
permitting by DPI-FDACS. The law that it enacted was, arguably, the first sensible
attempt at regulating importation of living organisms in the country. In fact, it makes
Florida Entomologist 78(1)
the federal laws unnecessary and redundant, as far as importations into Florida are
concerned. The Florida law should serve as a model for a revised federal law. Only if
the federal law becomes as stringent as the Florida law, and covers inter-state ship
ment, should the Florida law be repealed.
Later still, USFWS, which has no inter-agency agreement with USDA-APHIS, de
cided that insects are wildlife and importers/exporters of insects must follow its wild
life regulations and the wildlife regulations that it attributes to countries of origin.
Thus, for example, anyone collecting insects in Mexico has to buy a Mexican hunting
permit (for $750) and hire a Mexican hunting guide, according to USFWS regulations.
Such permits are difficult-nearly impossible-to obtain, and so all insects exported
from Mexico, dead or alive, are currently illegal in the eyes of USFWS. Tens of mil
lions of insect specimens in national, state, and private collections technically are il
legal contraband, because they are not accompanied by wildlife permits. USFWS does
not recognize Mexican collecting/export permits for insects issued by Mexican agricul
tural/scientific authorities, which are much easier to obtain. Although USFWS is
rightly attempting to restrict trade in insect specimens belonging to endangered spe
cies (mainly butterflies), it is inadvertently causing a severe hindrance to biological
control. This problem could be solved by federal inter-agency agreement.
Based on our historical account, we conclude that the risks of introduction of bio
logical control agents are scrutinized much more closely than those of other kinds of
insects. We would not suggest that as a consequence of this uneven treatment, moni
touring of importation of biological control agents should be slackened. Indeed, there is
need for classical biological control to become more predictive (see Samways 1994).
Rather, we would suggest that monitoring of the importation of other kinds of insects
needs to be tightened, if the realized and potential threat of "biological pollution" by
insects is to be lessened. To lessen the threat, we submit the following four proposals.
First, legal (under permit) and illegal (without permit) importation of "pet" insects
and other terrestrial arthropods should cease. Penalties for attempted illegal impor
station will have to be made more obvious and more severe. Second, insects imported
for educational and research purposes (by universities, schools, zoos, and other orga
nizations) should be held under conditions as secure as those now required for initial
importation of biological control agents. Third, importation of "ornamental" plants
should cease, unless importations are limited to seed-to restrict hitchhiking insect
pests-or unless all incoming shipments are fumigated with chemicals shown to have
ovicidal activity or dipped in chemicals with ovicidal activity. Fourth, all incoming
shipments containing wood or other vegetable matter, even if only as packing crates,
should be fumigated with chemicals shown to have ovicidal activity. Importers of in
sects or vegetable matter will have to pay the costs of any necessary secure facilities
or required chemical treatment. All ships and boats arriving at Florida docks will
have to be fumigated at owners' expense. All road vehicles will have to be stopped at
Florida's borders and the drivers cautioned about potential searches, and fumigation
of plant materials. If these restrictions cannot be implemented, because of political
and economic pressure, then importers should pay into a fund which would provide
research costs for the biological control of organisms that become established in na
ture.
CONCLUSIONS
Many biologists still fail to comprehend the means of arrival of adventive (= "non
indigenous") organisms in Florida, and in the USA in general. It may be that almost
all adventive vertebrates and plants are introduced. But, by following an assumption
March, 1995
Behavioral Ecology Symposium '94: Frank & McCoy Intro. 13
that adventive insects likewise are introduced, they confuse purposeful introduction
with all other means of arrival. We distinguish these other means of arrival as immi-
gration, which we consider to include all the undocumented modes of arrival, include
ing flight, walking, swimming, rafting, and hitchhiking in cargoes. It is immigrant
species which form 95.7% of the adventive insects in Florida (Frank & McCoy 1995)
and some of them are important pests. The introduced species in Florida, in con
trast, were imported and released under permit because they are potentially benefit
cial-all of them are biological control agents of pests. None of them has been
implicated in any kind of environmental damage. We are concerned that well-mean
ing but uninformed biologists should not label "introduced" (= all non-indigenous;
their definition) insects as necessarily a bad thing for the environment-when, in fact
insects introduced (our definition) by humans may be the least risky way to save the
environment from damage caused by other organisms, purposefully or inadvertently,
brought to Florida by humans.
THIS SYMPOSIUM
We have suggested that, in order to deal with biological pollution in a more even
handed way, greater attention needs to be paid to documentation of Florida's insect
fauna and to philosophical and practical questions involved with insect introduction.
The contributions to this symposium address these two subjects. J. H. Frank & E. D.
McCoy (1995) offer, for the first time, estimates of the current size of the Florida insect
fauna, the proportion of indigenous and adventive species and, within these catego
ries, the proportion of precinctive, indigenous but not precinctive, and immigrant spe
cies. They use information from various experts coupled with knowledge from an
earlier paper on number of introduced species, to derive these estimates. They then
compare their estimates with similar ones derived for the insect fauna of Hawaii. Al
though Hawaii's immigrant insect problem is much worse than Florida's, Frank &
McCoy (1995) find no reason to be complacent, because Florida's immigrant insect
problem may be much worse than those of most of the other contiguous states.
Plants introduced for ornamentation and insects introduced for purposes other
than biological control raise important questions about the efficacy of biological intro
ductions in general. For these kinds of organisms, especially, the risks to the public
could be great enough to outweigh any benefits of introduction that might accrue.
Substantial attention should be paid to the potential risks of such introductions. D.
Cathcart discusses the potential benefits of importing bromeliads: aesthetics; re
search on systematics, physiology, and culture methods; preservation of gene pools;
and, perhaps, production of bromeliads to restock areas in their native lands where
they have become extirpated or endangered. He also discusses the precautions taken
by his firm to ensure that insects do not hitchhike into Florida on bromeliads. R.
Boender discusses the potential benefits of importing butterflies, and derives a list
very similar to Cathcart's: entertainment, education, research on production meth
ods, production of living specimens for use by researchers, preservation of gene pools
and, perhaps, production of butterflies to restock areas in their native lands where
they have become extirpated or endangered. He also discusses the precautions taken
by his butterfly farm and exhibition to ensure that butterflies do not escape and be
come established "plant pests."
Insects introduced as biological control agents have contributed some conspicuous
successes in the struggle to reduce the effect of invasive adventive species in Florida.
T D. Center and co-workers illustrate the use of biological control to solve problems
caused on public lands-including waterways-by introduced and immigrant species.
Florida Entomologist 78(1)
Problem species on public lands mainly are plants, but to a lesser extent, also include
insects. Center and co-workers reiterate the important point that even though some
members of the public may see classical biological control as contributing yet more ad
ventive species to already burdensome numbers, classical biological control is an en
vironmentally sound solution to the problem caused by some introduced and
immigrant species.
Insect introduction for the purpose of biological control has a long history of gov
ernment regulation in Florida. M. C. Thomas reflects the concerns of FDACS-DPI
about immigrant and introduced insects. He points out that state laws now require
importation permits for all arthropods and molluscs (no longer just for "plant pests"
and biological control agents) from anywhere outside Florida. He warns of the signif
icant potential danger to the environment from the kinds of arthropods and molluscs
that the pet trade has been importing.
ACKNOWLEDGMENTS
We are indebted to David Hall and Thomas Sheehan (both formerly of the Univer
sity of Florida) for helping us to obtain an estimate of the number of cultivated but not
yet naturalized plant species in Florida. We thank John L. Capinera and J. Patrick
Parkman for reviewing a draft of this manuscript. Pablo Delis provided the Spanish
abstract. This is Florida Agricultural Experiment Station journal series R-04282.
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Florida Entomologist 78(1)
THE IMPORTANCE OF MAINTAINING BROMELIAD IMPORTS
D.J.CATHCART
Tropiflora, 3530 Tallevast Road, Sarasota, FL 34243, USA
ABSTRACT
Exotic bromeliads are important to horticulture in Florida. Several hundred bro
meliad species from eight common and over 40 obscure genera have been imported
into Florida to fuel an industry of horticulture and scientific enquiry. Recent moves
aimed at restricting the importation of exotic fauna and flora, including bromeliads,
could be detrimental to an important industry. This information is presented to argue
for the economic importance of bromeliads, their low incidence of pest infestation and
lack of any threat to native species through intentional or unintentional release of im
ported species to the wild. Additional benefits are gained from the cultivation and ul
timate preservation of endangered taxa.
Key Words: Bromeliaceae, insects, introductions, exotic species, Florida
RESUME
Las bromelias ex6ticas son parte important de la horticulture en la Florida. Va
rios cientos de species de bromelias correspondientes a 8 g6neros comunes y mas de
40 no comunes han sido importadas a la Florida con el prop6sito de incrementar la in
dustria de la horticulture y de satisfacer las necesidades de la investigaci6n cientifica.
Las recientes medidas de restricci6n a la importaci6n de flora y fauna ex6ticas, inclu
yendo bromelias, podrian actuar en detrimento de tal actividad. La present informa
ci6n sustenta el interns econ6mico de las bromelias, su baja incidencia de infestaci6n,
y la ausencia de peligro alguno para las species nativas, motivado por la liberaci6n
intencional o accidental de species importadas. Beneficios adicionales podrian obte
nerse mediante el cultivo y la preservaci6n de los grupos en peligro de extinci6n.
The first exotic bromeliads to be introduced to horticulture in Florida were im
ported from Europe at the beginning of the last century. Although the USA became
the leader in bromeliad sciences, Europe never relinquished its hold on the U.S. mar
ket. Today, millions of seedlings and tens of thousands of finished plants are imported
annually into the USA from Belgium and Holland alone. In Florida, over a dozen large
nurseries and many smaller ones devote themselves to bromeliad production. Orna
mental bromeliads have become a commercial crop worth an estimated $20 million
per year to Florida horticulture. Several meristem laboratories in Florida have begun
production of patented and non-patented bromeliad varieties, but most bromeliad
nurseries in Florida and, indeed, the entire USA depend partly or wholly on imported
meristems, seedlings or cuttings for their growing-on stock.
BROMELIADS AND THEIR CULTIVATION
Bromeliaceae are tropical and subtropical herbs, native, with a single exception, to
the New World. Over 2,000 species belong to three subfamilies (Pitcairnioideae,
Tillandsioideae and Bromelioideae) with approximately 50 genera. In general, brome
This article is from Florida Entomologist Online, Vol. 78, No. 1 (1995).
FEO is available from the Florida Center for Library Automation gopher (sally.fcla.ufl.edu)
and is identical to Florida Entomologist (An International Journal for the Americas).
FEO is prepared by E. O. Painter Printing Co., P.O. Box 877, DeLeon Springs, FL. 32130.
March, 1995
Behavioral Ecology Symposium '94: Cathcart
liads form rosette-shaped whorls of parallel-veined leaves and produce perfect, 3-pet
aled flowers. Leaves are covered with trichomes or peltate scales which enable these
plants to adapt to various harsh growing condition. Bromeliads may be terrestrials,
facultative epiphytes, or obligate epiphytes, and exhibit great diversity among family
members: compare Ananas comosus (L.) (pineapple) with Tillandsia usneoides (L.)
(Spanish moss).
A Brief History
Exotic bromeliads have been a factor in the horticultural world since the 1500s. On
his second voyage in 1493, Columbus was introduced to Ananas comosus by the Carib
Indians on Guadeloupe. This plant had been a part of pre-Columbian culture for un
told years. By the end of the 1700s, the subfamilies of bromeliads had been described.
Early plant explorers prized bromeliads for their unusual form and beauty. By the
late 1700s and early 1800s, the search was on in earnest for new species, introducing
hundreds of species to cultivation in Europe by the turn of the twentieth century.
Although Florida has 17 native species of bromeliads, representing three genera in
the subfamily Tillandsioideae, these were never horticulturally important. The first
exotic bromeliads to be introduced to Florida horticulture were imported from Europe
at the beginning of the last century. Florida's pineapple industry, begun in the 19th
century, peaked in the 1930s, and it is now very small. Changing weather conditions
eventually made it unprofitable.
Importance to Agriculture and Horticulture
Historically, bromeliads have had limited agricultural use. Several bromeliad spe
cies produce commercially important fibers. Bromelain, an enzyme produced by
Ananas comosus fruits in defense against insect larvae (Benzing 1980), is becoming
important in the chemical and pharmaceutical industries. A second enzyme, hemi
sphericin, produced by Bromelia, may become important (Gutierrez et al. 1993). As a
food source, bromeliads provide a few species with edible stems, flowers, roots and
fruits, the most notable of which is Ananas comosus. Now, more than ever before, bro
meliads hold the promise of a bright future in the horticultural industry.
Florida's Commercial Production of Ornamental Bromeliads
Commercial bromeliad production in Florida is now centered on the production of
ornamental varieties. Large and modern facilities produce millions of finished brome
liads from domestic and imported seed, meristems, cuttings and pre-finished mate
rial. Most revenues are generated in the market for bromeliad hybrids for
interiorscape and flowering potted-plants, with only 8 genera and a few dozen species
dominating production.
A much smaller but still important part of the bromeliad market lies in the pro
duction of bromeliads for use as novelties. This includes various species grown espe
cially for use in dish gardens, for mounting on decorative wood and as 'tourist
novelties', such as small Tillandsia plants on magnets and sea shells.
A growing sector of the industry is producing bromeliads as landscape plants.
South and central Florida, and the warmer parts of the sun belt are well suited to ex
ploit this potential in bromeliads. Several Florida nurseries now specialize in land
scape bromeliad production.
Florida Entomologist 78(1)
Many people across the country and the world have collections of bromeliads. To
satisfy their needs, several smaller Florida nurseries specialize in the production of a
wide array of species, hybrids and cultivars.
INTERNATIONAL TRADE IN BROMELIADS
Although the production of bromeliads in the USA (with the exception of pineap
ples) is centered in Florida, our state by no means has a lock on the industry. Califor
nia is second to Florida in bromeliad production, and Hawaii is now entering the
market place.
Just as Florida's pineapple production was nearly eliminated by cold tempera
tures, so is Hawaii's moving east due to increasing production costs. Pineapple pro
duction for the U.S. market is now much greater in Central America than it ever was
in Hawaii. Despite the fact that Hawaii is still a major pineapple producer, many Ha
waiian nurserymen are now entering the exotic bromeliad market, with some major
facilities producing foliage and decorative flowering species of bromeliads.
Which Bromeliads Are Imported?
Of 50 genera and over 2,000 species of bromeliads, only a relative few are com
only imported. Of these, much the majority are from cultivated stock. Plants of wild
origin are imported to a much more limited degree. These few are used primarily as
propagation stock, hybrid parent stock, limited sales to collectors, and as herbarium
material. Many, if not most of the bromeliads imported, are artificially propagated hy
brids, patented varieties not otherwise available in this country.
Economics
Bromeliad cuttings can be grown faster and cheaper in nurseries abroad than in
the USA. Many such facilities exist in Puerto Rico, Guatemala, Costa Rica, Colombia
and, to a lesser extent, in several other Latin American countries. The largest brome
liad nursery in the world is in Holland, and it funnels millions of seedlings and fin
ished plants annually into the U.S. market. Plants of the genus Tillandsia are grown
in large overseas operations where a combination of selected climatic conditions and
lower production costs make production there more lucrative. These plants, often in
corporate into novelty uses, cannot be sent to the USA as finished products for direct
sale. Nurseries here must, at the very least, house them for a time, pending sales.
However, these plants are usually brought in as cuttings or pre-finished, and grown
out for an extended period to produce a superior, unblemished, finished product.
THE NEED TO IMPORT BROMELIADS
Commercial Competition
The bromeliad market is extremely competitive and the biggest companies vie for
market share with a steady stream of beautiful new patented varieties. Hybridizers
are working constantly to produce ever more spectacular and hardy varieties for the
marketplace. This work is fueled by one thing: new stock. The competition for finding
and being the first to use new superior clones and new species of bromeliads, espe
cially in the genera Guzmania, Vriesia, and Aechmea, is stiff. At stake may be the very
March, 1995
Behavioral Ecology Symposium '94: Cathcart
survival of the U.S. bromeliad industry. Many superior hybrids have been produced in
the USA and are now grown under licensing agreements here and abroad. A single
patented variety could be worth millions to the patent holder.
Research
Florida is the center of bromeliad research. The Marie Selby Botanical Garden and
the Mulford B. Foster Bromeliad Identification Center employ full-time research staff
investigating the taxonomy and physiology of bromeliads. Researchers and scientists
from all over the world come to Florida to involve themselves with these studies. Im
portation of fresh research material is essential to the survival of these institutions.
In no less a manner, the results of their research are essential to the survival of the
bromeliad industry.
Conservation
Great concern has been expressed in recent years about the possible imminent de
mise of many tropical organisms, including bromeliads. Recently, seven species of bro
meliads were added to the CITES list of endangered species. Rampant habitat
destruction is the major cause of their decline in nature and can be attributed to many
factors. Land-clearing for cattle production and other agricultural use leads the list of
habitat-destroying activities. New, full-sun varieties of coffee and cacao are causing
great tracts of montane forest to be cleared where once some canopy, often bearing ep
iphytic bromeliads, was left for shading the crops. Traditional crops such as bananas
and now pineapples have caused the decimation of much lowland forest for their pro
duction. Logging, mining and human encroachment have eliminated much critical
habitat.
Importing bromeliads for the purpose of saving rarer species and conserving the
biological diversity of others is now a reality. Already some species exist in cultivation
that are known or thought to be extinct in their natural habitats. These and other spe
cies of bromeliads, still found in their natural habitats, but declining from various fac
tors, are being cultivated with an eye toward reintroduction. All this is made possible
by bromeliad importation.
THE ARGUMENT AGAINST IMPORTING BROMELIADS
Human Health Risks
Misinformation has been responsible for some minor hysteria about the "problem"
of mosquitoes in bromeliads. Both of the two species of mosquito known to develop ha
bitually as larvae in bromeliad tanks in Florida, are native to Florida, and neither is
known to be a vector of diseases of humans. It appears that they are no more than a
nuisance (Frank 1994). Even though some neotropical mosquitoes have larvae spe
cialized to existence in bromeliad tanks and have adults that vector diseases to hu
mans, none of these has become established in Florida. Larvae of a few other mosquito
species sometimes inhabit water in bromeliad tanks in Florida, but bromeliad tanks
are just a small part of their habitat, and they would occur whether or not bromeliad
tanks were available to them. It is fairly easy to control bromeliad-inhabiting mosqui
toes, of native or foreign origin, in nurseries and well-maintained landscapes. Much
Florida Entomologist 78(1)
of the misinformation is spread by the pest-control industry which profits from the
public's fear of disease.
A similar misinformation campaign has been mounted against a native bromeliad,
Tillandsia usneoides (Spanish moss). Much profit has been made by pest-control com
panies by spraying copper to eliminate the 'moss' after convincing people that it kills
their trees, a premise long ago proved false.
Risks to Agriculture and Horticulture
Bromeliads have been imported into the USA for more than a hundred years. So
far, no pest of foreign origin, whose presence in Florida is attributed to bromeliad im
ports, has been shown to affect plants other than bromeliads.
Bromeliads collected in the field in the tropics may house all sorts of insects and
other invertebrate animals, which are often difficult to detect because of the plants'
structure. USDA inspectors at airports annually discover large numbers of insects,
molluscs, and plant pathogens in imported bromeliads, as a result of carelessness on
the part of the shippers. If plants have to be collected in the field, they should be
cleaned carefully and then dipped in a suitable chemical pesticide.
Bromeliads shipped from nurseries abroad are likely to be much cleaner of insects
in general than are plants collected in the field. However, those pests that do hitch
hike in such plants are more likely to be specific pests of bromeliads. Most such pests
have so far been species of scale insects specific to bromeliads. Again, the best solution
is to dip all plants in a suitable chemical pesticide. The onus is on the importer to
make sure that only pest-free plants are imported, because USDA inspectors are too
short-staffed to inspect more than a small fraction of plants. A pest of concern which
has become established in southern Florida due to its hitchhiking in imported brome
liads is Metamasius callizona (Chevrolat) (Frank & Thomas 1994). Other pests as im
portant as M. callizona could arrive in imported bromeliads if importers are not
extremely careful. Vigilance is now required to detect and control this weevil pest in
nurseries and collections in Florida.
Risks to the Native Flora
No exotic species of bromeliad has become established in nature in Florida, even
on a limited scale, even though some species could certainly survive. In biological
terms, bromeliads of foreign origin do not seem to be "invasive" in Florida even when
they originate from places of similar climate. Reasons for their lack of invasiveness
have not been investigated.
Presence of Metamasius callizona in nature in four counties in Florida is of more
concern. Its continued spread is believed to be in part due to transport of infested
plants and in part to flight by adults. What effect this weevil will ultimately have on
the bromeliad flora of southern Florida is unknown. A hope is that insect biological
control agents will be discovered in its native range, will be introduced successfully
into Florida, and will succeed in controlling this pest in nature.
CONCLUSION
Bromeliad importation appears to be fairly benign. Lacking strong evidence to the
contrary, bromeliads should continue to be imported as an important part of Florida's
horticultural industry and as fuel for its research facilities. Hundreds of jobs directly
related to the bromeliad industry, and thousands indirectly related, may be at stake.
March, 1995
Behavioral Ecology Symposium '94: Cathcart
The bromeliad industry helps make Florida the top state in the nation in horticultural
production. Our subtropical climate lends itself well to landscaping with bromeliads,
and bromeliads now add beauty to countless homes, business, parks, public works,
tourist attractions and public buildings. This same climate allows the cultivation of a
wide and ever-increasing variety of threatened and endangered bromeliad species.
Coupling this with a fairly low incidence of pest infestation leaves little grounds for
the restriction of bromeliad imports.
ACKNOWLEDGMENTS
Isabel Bohorquez kindly translated the abstract into Spanish.
REFERENCES CITED
BENZING, D. H. 1980. The Biology of the Bromeliads. Mad River Press; Eureka, Cali
fornia.
FRANK, J. H. 1994. Mosquito Production from Bromeliads in Florida. University of
Florida, Institute of Food and Agricultural Sciences, SP 166.
FRANK, J. H., AND M. C. THOMAS. 1994. Metamasius callizona (Chevrolat) (Co
leoptera: Curculionidae), an immigrant pest, destroys bromeliads in Florida.
Canadian Entomol. 126: 673-682.
GUTIERREZ 0., M., M. CAMINO L., F. CASTREJON A., AND A. JIMENEZ P. 1993. Arthro
pods associated with Bromelia hemisphaerica (Bromeliales: Bromeliaceae) in
Morelos, Mexico. Florida Entomol. 76: 616-621.
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Behavioral Ecology Symposium '94: Frank & McCoy
PRECINCTIVE INSECT SPECIES IN FLORIDA
J. H. FRANK' AND E. D. MCCOY2
'Entomology & Nematology Department, University of Florida,
Gainesville, FL 32611-0620, USA
Biology Department, University of South Florida,
Tampa, FL 33620-5150, USA
ABSTRACT
The number of insect species now occurring in Florida is estimated at about
12,500. Statements from specialists in 28 insect taxa (at the level of family or higher),
representing some 40% of the fauna, suggest that about 12% of the total fauna (13%
of the indigenous fauna, with range 0-43% among taxa) is precinctive. Immigrants
form less than 8% of the total fauna. Only 42 (0.3%) species are known to have been
introduced I. .. I i. I, for purposes of biological control. The proportions of immi
grants and of precinctive species are far lower than in the Hawaiian insect fauna, but
the proportion of immigrants exceeds that of the fauna of the contiguous United
States as a whole.
Key Words: Adventive species, indigenous species, precinctive species, immigrant
species, diversity.
This article is from Florida Entomologist Online, Vol. 78, No. 1 (1995).
FEO is available from the Florida Center for Library Automation gopher (sally.fcla.ufl.edu)
and is identical to Florida Entomologist (An International Journal for the Americas).
FEO is prepared by E. O. Painter Printing Co., P.O. Box 877, DeLeon Springs, FL. 32130.
Florida Entomologist 78(1)
RESUME
Se estima que el numero de species de insects existentes en la Florida es cercano
a 12500. Opiniones de especialistas en 28 grupos de insects (a nivel de familiar o su
perior) que representan un 40% de la fauna, sugieren que cerca de 12% de la fauna to
tal (13% de la fauna indigena, con intervalo 0-43% entire grupos) es precinctiva. Los
inmigrantes constituyen menos del 8% de la fauna total. Solo 42 (0.3%) species han
sido introducidas intencionalmente, con fines de control biol6gico. Las proporciones de
species inmigrantes y precinctivas son much menores que en la fauna de insects de
Hawaii, pero la proporci6n de inmigrantes excede la de la fauna de los Estados Unidos
contiguos como un total.
Many generalizations about the diversity of insects have been drawn from the Eu
ropean fauna, especially the fauna of the British Isles. This has been possible because
of virtually complete checklists published, for example, by the Royal Entomological
Society. Checklists are available for other locations, as well, such as Hawaii. A second
(revised) edition of a computerized checklist of the arthropod fauna reported from Ha
waii in the literature has just been published (Nishida 1994). Even though it is stated
to be incomplete and may contain errors, it documents some striking facts. For exam
ple [using our terminology (Frank & McCoy 1990) rather than Nishida's (1994)
terms], it gives the number of indigenous insect species as 5,059 (4,980 precinctive
and 79 indigenous but not precinctive), and the number of adventive species as
2,549 (2,137 immigrant and 412 introduced). These proportions are so different
from our conception of the Florida insect fauna that we thought it useful to compare
the faunas of Florida and Hawaii.
Because we shall use precise terminology (Frank & McCoy 1990) to make compare
isons between faunas, it is important that we reiterate what the terms mean. The six
categories into which we shall place insects are indigenous, precinctive,1 indige-
nous but not precinctive, adventive, immigrant, and introduced. The six cate
gories are delimited as follows.
Indigenous: native
A. Precinctive: native to and restricted to the area specified (the usage
follows Sharp 1900)
B. Indigenous but not precinctive: native to the area specified and
elsewhere
Adventive (= non-indigenous): not native; arrived from elsewhere
C. Immigrant: not native to the area specified and arrived there by
means other than purposeful introduction, such as flight, walking,
swimming, rafting, phoresy, hitchhiking in cargoes, and as aerial
plankton (the usage follows Sailer 1978, although he neither provided
a definition nor used the term consistently)
D. Introduced: not native to the area specified and arrived there by
means of purposeful introduction (the usage follows Zimmerman
1948)
There is no checklist of the insect fauna of Florida, although works including all
known species of Ephemeroptera, Odonata, Blattodea, Isoptera, Orthoptera and Lep
'Later in this paper we use the noun precinction (the state of being restricted to a specified
area) which was used in English in 1730 (OED 1971). It bears the same relationship to precinctive
as endemism bears to the adjective endemic.
March, 1995
Behavioral Ecology Symposium '94: Frank & McCoy
idoptera, and partial checklists of one, or a few related families in other orders, have
been published. Therefore, we estimated the total number of insect species now occur
ring in Florida and, using this total number as a basis, we estimated the numbers of
immigrant species, precinctive species, and indigenous but not precinctive
species (number of introduced species was known). With these estimates in hand,
we could then compare the insect faunas of Florida and Hawaii.
THE TOTAL NUMBER OF INSECT SPECIES IN FLORIDA
Several ways exist to estimate the total number of insects in Florida. One could,
for example, use the combined knowledge of expert taxonomists (e.g., Gaston 1991),
or extrapolate from extensive field collections (e.g., Stork 1988, Hodkinson & Casson
1991), or extrapolate from ratios of numbers of insect species to numbers of plant spe
cies (e.g., Hodkinson & Casson 1991, Gaston 1992). We have chosen yet another way,
to extrapolate from a particularly well-known group, the beetles (see Erwin 1982,
1988; Stork 1988). Although there is no checklist of the insect fauna of Florida,
Michael C. Thomas is constructing a computerized catalog of Florida Coleoptera. This
catalog will include all species documented in the literature and all species repre
sented in the Florida State Collection of Arthropods, with entries corrected in consul
station with specialist taxonomists. Thomas informs us that the number of species
names listed is now over 4,000, and he expects the total to reach 5,000 when document
station is complete. Given that beetles comprise 40% of all insect species (Borror et al.
1976), and assuming that the composition (proportions among orders) of the insect
fauna of Florida is not especially divergent from other faunas, then the total number
of insect species now occurring in Florida should be about (5,000 x 100/40 =) 12,500.
THE NUMBERS OF IMMIGRANT AND INTRODUCED INSECT SPECIES IN FLORIDA
We documented 271 immigrant insect species as newly recorded in the literature
from 1971 to 1991 (Frank & McCoy 1992). We have not surveyed the older literature
to the same purpose, but will attempt to extrapolate. We adopted the anthropocentric
concept that species occurring in Florida before Columbus' first voyage are indige
nous. Immigrant species probably did arrive (as stowaways) with early Spanish colo
nists, but we believe that the number of species immigrating has increased very much
in recent decades (see Frank & McCoy 1993). We attribute this recent increase to the
arrival of insects (as stowaways) in the cargoes, especially cargoes of plants, that have
been shipped to Florida in ever-increasing numbers. Although dozens of immigrant
species were known as pests in the 19th century, the number is now in the hundreds.
Based on our documentation of recent immigrations, we would place the number of
immigrant species now present in Florida at about 1,000; the estimate derived from
statements of specialist taxonomists (see below) is about 950.
We also documented 42 introduced insect species as established in Florida
(Frank & McCoy 1993). Many more species have been brought to Florida deliberately
(Frank & McCoy 1993, 1994), and 151 of these have been released for biological con
trol purposes.
THE NUMBER OF PRECINCTIVE INSECT SPECIES IN FLORIDA
Determining which taxa are precinctive is an undertaking fraught with uncertain
ties, and it is worth spending some time to understand clearly what it means to be
precinctive. Precinctive taxa often are of great interest simply because they are
Florida Entomologist 78(1)
unique (Australian marsupials or the "Teesdale Rarities," for instance) or because
they may tell us something interesting about biogeographic processes or for numerous
other reasons. Perhaps the most interesting question to be asked about precinctive
taxa is: What creates them? We may proceed to answer this question by looking for ar
eas with large numbers of precinctive taxa and then inferring a cause based upon
which particular areas are singled out. Like all conclusions generated in this fashion,
the "cause" decided upon may not be totally convincing. A classic example may be
found in patterns of precinctive taxa on isolated oceanic islands (Briggs 1966, 1969;
McDowell 1968, 1970; McCoy & Heck 1987). It seems clear that precinctive taxa are
produced by precisely the same biotic and abiotic constraints that circumscribe
ranges in general. Indeed, it should be apparent that there is nothing unusual about
precinctive taxa per se; every taxon is precinctive to some geographical area. Precinc
tive taxa typically become useful and interesting when they are confined to relatively
small areas, especially if those areas harbor large numbers of them. In such cases, one
quite naturally assumes that restriction of many species to small areas is improbable
and, consequently, that very powerful biotic or abiotic range limitations have been at
work. Rotondo et al. (1981), for example, illustrate the role of island integration in
promoting high numbers of precinctive taxa on some Pacific islands, especially the
Hawaiian Islands. So, how does one determine when a certain level of precinction in
an area is improbable? For example, is the 10%-level of precinction thought to be
present among marine invertebrates in the northern Gulf of Mexico iHrdgplrh 1953,
McCoy & Bell 1985) truly unusual? We suppose that to find out, one could divide the
eastern coast of the Western Hemisphere into segments, each equal the length of the
northern Gulf of Mexico, assign species to them in a weighted random fashion, and
compute resulting levels of precinction. Such a procedure would be overkill, though,
for it is almost always relative levels of precinction that are deemed out of the ordi
nary In the Gulf of Mexico, it is true that levels of precinction are low in most places,
so an area with a level of 10% stands out. It would not stand out if, say, 8% precinction
were the rule everywhere else in the Gulf. One could probably argue, therefore, that
any changes in precinction, even small ones, deserve investigation. The roles of vari
ous limiting factors in circumscribing ranges may be understood further by such in
vestigations. One should keep in mind, however, that the identification of areas of
unusual levels of precinction is a subjective and relative process. The criterion em
played usually will be consensus. Failure to acknowledge these facts about how pre
cinction is recognized may lead to some unusual exercises in logic. Consider, for
example, a hypothetical case of three adjacent areas divided by arbitrary boundaries.
Suppose that researchers have identified areas "A" and "C" as possessing relatively
many precinctive species, and have produced some geological explanation for their
isolation. By consensus, then, "A" and "C" are touted as unusually rich areas of pre
cinction, and the other area, "B," is forgotten. This scenario might be appropriate if,
say, "A" and "C" each had 6 precinctive species and "B" only 2. It might not be appro
private, however, if "A" and "C" each had 10 precinctive species and "B" none. One
might feel compelled in the second case to single out "B" as an unusually poor area of
precinction, and try instead to explain this "phenomenon." Of course, the explanation
produced is likely to be the reciprocal of one that would be produced for relatively-high
levels of precinction in "A" and "C." Because of inherent subjectivity and relativity, the
entire process of identifying unusual levels of precinction is dangerously prone to cir
clarity (see, for example, Guillory 1979). Bearing these caveats in mind, we shall at
tempt to provide some estimates of the number of insect taxa precinctive to Florida.
We felt estimates of the numbers of precinctive species could be achieved best by
asking a large number of specialists with knowledge of the Florida fauna at the family
March, 1995
Behavioral Ecology Symposium '94: Frank & McCoy
level (or a higher level) to prepare a statement for publication (cf. Muller et al. 1989).
Each statement would be published under the name of the specialist who prepared it,
and would give the total number of indigenous species, subdivided into the two sub
categories (precinctive, and indigenous but not precinctive), as recorded in the
literature. Subspecies would not be considered. Species present at the time of Colum
bus would be considered indigenous. Indigenous species reported only from Florida
(not from neighboring states, nor from the West Indies, nor from other regions) would
be considered precinctive. Obviously, this determination requires substantial judg
ment by the specialists. Species believed to be indigenous to the Greater Antilles or to
the southeastern USA, that also occur in Florida, would be considered indigenous
but not precinctive. The specialists' statements would not only allow an overall es
timate of the proportion of precinctive species, but would allow examination of vari
ation from taxon to taxon. We contacted colleagues who study a broad cross-section of
the fauna, and it was their interests that selected the taxa included, so we felt that
there is no biological bias in selection of taxa. Their statements included about 40%
of the estimated 12,500 species of Florida insects, and allowed the compilation shown
in Table 1.
Mayflies (Ephemeroptera)
Manuel L. Pescador, Entomology-Water Studies, Florida A&M University,
Tallahassee, FL 32308-4100, USA
Florida has a mayfly fauna of relatively low diversity. Of the 71 species known in
the state, 23 are indigenous, 10 of which are precinctive and 13 are not precinctive.
The precinctive species include 3 of Baetidae [Baetis alachua (Berner), Callibaetis
floridanus Banks, and C. pretiosus Banks], 3 of Metretopodidae [Siphoplecton brun
neum Berner, S. fuscum Berner, and S. simile Berner], one of Heptageniidae [Stena
cron floridense (Lewis)], one of Ephemeridae [Hexagenia orlando Traver], and 2 of
Caenidae [Brachycercus maculatus Berner and B. nasutus Soldan]. There is no evi
dence to suggest any mayfly dispersal from the West Indies to Florida, and the mayfly
faunas of the two areas show no phyletic relationships.
Dragonflies and damselflies (Odonata)
Sidney W. Dunkle, Biology Department, Collin County Community College,
Plano, TX 75074, USA
An estimated 144 species of Odonata were indigenous to Florida at the time of Eu
ropean discovery. Of these, 104 are dragonflies (Anisoptera) and 40 are damselflies
(Zygoptera). Of the 144 indigenous Odonata, 5 (4 Anisoptera, 1 Zygoptera) are pre-
cinctive. There are now 12 established species of immigrant Odonata, one of them
[Crocothemis servilia (Drury)] from Asia, 3 [Celithemis elisa (Hagen), Enallagma
basidens Calvert and E. civil Hagen] from North America, and 8 from the neotropics.
No species of Odonata has been introduced (deliberately) to Florida. Additionally, 7
species have been found as vagrants, without breeding populations. More than a third
(163 species) of the North American odonate fauna has now been found in Florida.
This information was extracted from a publication by S. W. Dunkle (1992. Distribu
tion of dragonflies and damselflies in Florida. Bull. American Odonatology 1(2): 29
50).
Florida Entomologist 78(1)
March, 1995
TABLE 1. VARIATION AMONG TAXA IN PROPORTION OF PRECINCTIVE SPECIES AND NUM
BER OF IMMIGRANT SPECIES.
Taxon
EPHEMEROPTERA
ODONATA
BLATTODEA
ISOPTERA
ORTHOPTERA
HEMIPTERA
Lygaeidae
Miridae
HOMOPTERA
Fulgoroidea
Coccidae
NEUROPTERA
COLEOPTERA
Carabidae
Staphylinidae
Scarabaeidae
Lampyridae
Nitidulidae
flat bark beetles'
Bruchidae
Curculionidae2
LEPIDOPTERA
Tortricidae
Sesiidae
Geometridae
butterflies3
DIPTERA
Culicidae
Tabanidae
Tephritidae
HYMENOPTERA
Ichneumonidae
Aphelinidae
Indigenous Precinctive Immigrant
23 10 (43%) 48
144 5 (4%) 12
25 1 (4%) 15
14 3 (21%) 3
232 41 (18%) 10
10 (10%)
36 (21%)
34 (16%)
3 (21%)
1 (1%)
40 (11%)
74 (23%)
45 (16%)
20 (41%)
3 (6%)
0 (0%)
0 (0%)
115 (22%)
26 (11%)
2 (5%)
33 (14%)
0 (0%)
20 (6%)
3 (10%)
'Silvanidae+Passandridae+Laemophloeidae
excluding Brentidae+Anthribidae+Scolytidae+Platypodidae
'Papilionoidea+Hesperioidea
Behavioral Ecology Symposium '94: Frank & McCoy
TABLE 1. VARIATION AMONG TAXA IN PROPORTION OF PRECINCTIVE SPECIES AND NUM-
BER OF IMMIGRANT SPECIES.
Taxon Indigenous Precinctive Immigrant
Formicidae 149 14 (11%) 52
TOTAL (THIS SAMPLE) 4,160 547 (13%) 342
TOTAL (WHOLE FAUNA) 11,512 1,514 (13%) 946
Silvanidae+Passandridae+Laemophloeidae
excluding Brentidae+Anthribidae+Scolytidae+Platypodidae
'Papilionoidea+Hesperioidea
Cockroaches (Blattodea)
P G. Koehler and R. J. Brenner, Entomology & Nematology Department,
University of Florida, Gainesville, FL 32611 0630,
and Medical and Veterinary Entomology Research Laboratory, USDA-ARS,
1600 SW 23rd Drive, Gainesville, FL 32604, USA
The cockroach fauna of Florida has recently been cataloged and is taxonomically
diverse compared to that of other U.S. states. There are 25 indigenous species in 17
genera and 4 families. One species, Arenivaga floridensis Caudell, is precinctive. It
is the only species of this genus in the eastern USA, and is a remnant of a larger, xeric
adapted biota that was abundant during the last glacial period. There are 24 cock
roach species indigenous but not precinctive. The range of 8 extends to the West
Indies, whereas the range of 9 extends to the U.S. mainland outside Florida. An addi
tional 3 species range from Florida to the U.S. mainland and into Central America,
and 2 species range from the West Indies into Florida and to the U.S. mainland out
side Florida. The range of the final 2 species is from the West Indies into Florida and
into Central America. The Florida fauna also includes 15 immigrant species that ar
rived from the Old World. The major pest species of cockroaches are all immigrants.
Termites (Isoptera)
Rudolf H. Scheffrahn, FLREC -University of Florida, 3205 SW College Avenue,
Ft. Lauderdale, FL 33314-7799, USA
The termite fauna of Florida, although taxonomically diverse, is a well-studied
group. Fourteen indigenous species from 8 genera and 3 families are represented.
Three species, Calcaritermes nearcticus Snyder, Neotermes luykxi Nickle & Collins,
and Amitermes floridensis Scheffrahn et al. are precinctive. Of the remaining 11 in
digenous species, six are also recorded from the West Indies or Neotropical mainland,
three occur on the U.S. mainland outside Florida, and two occur both on the U.S.
mainland and offshore. Based on extensive recent collections in the West Indies, it is
unlikely that species now thought to be precinctive to Florida will be found elsewhere
in the future. The Florida fauna also includes 3 immigrant species.
Grasshoppers and crickets (Orthoptera)
Thomas J. Walker, Entomology & Nematology Department, University of Florida,
Gainesville, FL 32611-0620, USA
Except for an eneopterine cricket, probably from Taiwan, recently established in
south Florida, these figures are from S. B. Peck, T. J. Walker & J. L. Capinera (1992.
Distributional review of the Orthoptera of Florida. Florida Entomol. 75: 329-342).
There are 242 species of Orthoptera known to occur in Florida. Of these, 232 are in
digenous, 191 are indigenous but not precinctive, 41 are precinctive, and 10 are
Florida Entomologist 78(1)
post-Columbian immigrants. For the 87 species of Caelifera, the numbers are 87, 70,
17, and 0, and for the 155 Ensifera, they are 145, 121, 24, and 10.
Seed bugs (Hemiptera: Lygaeidae)
R. M. Baranowski, University of Florida Institute of Food & Agricultural Sciences,
Tropical Research and Education Center, Homestead, FL 33031, USA
There are 115 species of Lygaeidae known to occur in Florida. Ten species are
known only from Florida, and 95 more are likewise considered indigenous. Ten spe
cies are considered recent immigrants based on habitat distribution and the proba
ability of their being collected by general collectors. Thus, of the 115 known Florida
species, 105 are known from outside of Florida.
Plant bugs (Hemiptera: Miridae)
A. G. Wheeler, Jr. and T J. Henry, Bureau of Plant Industry,
Pennsylvania Department of Agriculture, Harrisburg, PA 17110,
and Systematic Entomology Laboratory, USDA-ARS,
c/o National Museum of Natural History, Washington, DC 20560, USA
The Floridian mirid fauna consists of 175 indigenous (= native) species, including
36 (21%) that are precinctive. These figures are based on the most recent catalog of
the group, by T J. Henry & A. G. Wheeler (1988. Family Miridae Hahn 1833 (
Capsidae Burmeister 1835), The plant bugs, p. 251-507 in T J. Henry and R. C. Froe
schner [eds.]. Catalog of the Heteroptera, or True Bugs, of Canada and the Continen
tal United States. E. J. Brill; Leiden). The total number of mirids recorded from
Florida increases to 185 with the addition of 10 species that we consider to be immi-
grant.
Planthoppers (Homoptera: Fulgoroidea)
Lois B. O'Brien, Entomology-Biological Control, Florida A&M University,
Tallahassee, FL 32307-4100, USA
In 7 of the 11 families of Fulgoroidea found in the U.S. (except Delphacidae, Der
bidae, Flatidae, and Tropiduchidae), most species occur in the western U.S. In one
family, Tropiduchidae, all 3 species known from the U.S. occur in Florida; one is pre-
cinctive, one indigenous with extensions to nearby states and Cuba, and one indige
nous to Florida, Cuba, and Hispaniola. However, many species in the Greater Antilles
were identified before genitalia were used for identification, and some records are sus
pect. Species from the Lesser Antilles are better known and, except for Delphacidae,
at least 90% are precinctive to one island. Species that were described from the
Greater Antilles have been discovered in Florida during the last 50 years, but their
date of arrival cannot be pinpointed. Thirty-four (16%) of 214 indigenous Florida spe
cies of Fulgoroidea are precinctive. There are 6 immigrants, including 3 pantropical
pests of corn and sugarcane which arrived in this century.
Soft scales (Homoptera: Coccidae)
Avas B. Hamon, Florida State Collection of Arthropods, P.O. Box 147100, Gainesville,
FL 32614-7100, USA
Fourteen species of the soft scale family Coccidae are indigenous to Florida. Of
these 14 species, only 3 are precinctive, and the other 11 are indigenous but not
precinctive. Thirty immigrant species of soft scales are reported from Florida.
March, 1995
Behavioral Ecology Symposium '94: Frank & McCoy
Lacewings, antlions, and relatives (Neuroptera)
Lionel A. Stange, Florida State Collection of Arthropods, P.O. Box 147100,
Gainesville, FL 32614-7100, USA
There are 85 species of Neuroptera (including Megaloptera) indigenous to Florida.
Only one species, Mantispa floridana Banks, is precinctive to Florida. There are no
adventive species. At least 4 species remain to be described.
Ground beetles (Coleoptera: Carabidae)
P. M. Choate, Entomology & Nematology Department, University of Florida,
Gainesville, FL 32611-0620, USA
Florida has 365 indigenous species of ground beetles. Of these, 40 are precinc-
tive, while 325 are indigenous but not precinctive. There are 3 immigrant spe
cies.
Rove beetles (Coleoptera: Staphylinidae, sensu strict)
J. H. Frank, Entomology & Nematology Department, University of Florida,
Gainesville, FL 32611-0620, USA
The traditional concept of Staphylinidae is used here, to include Micropeplinae (no
species yet reported from Florida), but exclude Scaphidiidae [-inae], Dasyceridae [
inae], and Pselaphidae [-inae]. There are 328 indigenous species of Staphylinidae in
Florida, including 74 precinctive species and 254 indigenous but not precinctive
species. In addition, 15 adventive species are established in Florida, all of which are
immigrants (none of them was introduced). At very least a quarter of the sta
phylinid fauna is yet unrecorded: its eventual recording will increase the totals in the
various categories. The proportion of precinctive species may be reduced by modern
reports of the staphylinid fauna of Alabama, Georgia, and the Greater Antilles.
Scarab beetles (Coleoptera: Scarabaeidae)
Robert E. Woodruff, Emeritus Entomologist, Florida State Collection of Arthropods,
P.O. Box 147100, Gainesville, FL 32614-7100, USA
Two volumes (of 3) in the series "The Scarab Beetles of Florida" have been pub
lished by R. E. Woodruff (1973. Part I. Arthropods of Florida and Neighboring Land
Areas, Vol. 8) and by R. E. Woodruff & B. M. Beck (1989. Part II. Arthropods of Florida
and Neighboring Land Areas, Vol. 13), and the family is better known than most.
There are 292 species recorded from Florida of which 17 are immigrant, thus 275 are
indigenous and of these 45 are precinctive!
Fireflies (Coleoptera: Lampyridae)
James E. Lloyd, Entomology & Nematology Department, University of Florida,
Gainesville, FL 32611 0620, USA (with comments on myth, theory, and reality)
There have been 49 indigenous species of fireflies in 8 genera reported to occur in
Florida, with 20 of these in 6 genera being precinctive. This tally includes 11 species
for which I and others (whom I have supplied with living fireflies for research) have
used informal designations (e.g., Photuris sp. "B", Photinus "slow-pulse" consimilis).
These numbers bear only quaint relationship to Florida fireflies in nature. Misi
dentifications of cabinet specimens account for a few names in the literature, these be
ing made before the magnitude of the sibling species problem was appreciated. Some
Florida Entomologist 78(1)
species known to occur in Florida are not counted because they have never been men
tioned in the literature, and some that certainly are here for they are known from lo
calities nearby to the north, but cannot now be counted. One species appears to be a
repeated immigrant from Central America, and may occasionally survive a year or
so before disappearing. The most realistic estimate (not prediction) that I can give,
these problems considered, is that there are 57 indigenous species in 11 genera in
Florida, of which 17 species in 6 genera are precinctive. But, what bearing do such
presumptively good species have to real, that is, actual (isolation of gene pools) diver
sity as it exists in nature? Systematists have multiple species concepts and dissatis
faction with all of them, and I am confident that an interplanetary visitor would avoid
taking sides in this, and probably not do any counting, for scientific not sociable rea
sons. A species count for Florida fireflies is at once myth, theory, and reality.
Sap beetles (Coleoptera: Nitidulidae)
Dale H. Habeck, Entomology & Nematology Department, University of Florida,
Gainesville, FL 32611-0620, USA
There are 51 indigenous species of Nitidulidae in Florida including one species of
Cybocephalinae, a group sometimes given family status. Only 3 species are precinc-
tive and 48 are indigenous but not precinctive. Six species are, or are presumed
to be, adventive (immigrants).
Flat bark beetles (Coleoptera: Laemophloeidae, Silvanidae, Passandridae)
Michael C. Thomas, Florida State Collection of Arthropods, P.O. Box 147100,
Gainesville, FL 32614-7100, USA
Of the 56 species of flat bark beetles recorded from Florida by M. C. Thomas (1993.
The Flat Bark Beetles of Florida (Coleoptera: Silvanidae, Passandridae, Laemophlo
eidae). Arthropods of Florida & Neighboring Land Areas, Vol. 15), a total of 38 species
(Silvanidae, 10; Passandridae, 2; Laemophloeidae, 26) can be considered indigenous.
The other 18 are immigrant species. There are no precinctive species of flat bark
beetles in Florida. Of the indigenous species, the major part of the distributions of 30
species is to the north of Florida; the distributions of the remaining 8 species are pri
marily Neotropical.
Seed beetles (Coleoptera: Bruchidae)
John M. Kingsolver, Florida State Collection of Arthropods, P.O. Box 147100,
Gainesville, FL 32614-7100, USA
Of the 44 species of Bruchidae now recorded from Florida, 30 are indigenous, in
cluding 23 which are part of the eastern U.S. fauna, 2 which are Circumcaribbean,
and 5 common to the West Indies and Florida. There are no precinctive species. Of
the 14 immigrant species, 4 are cosmopolitan "tramp" species in stored legume
seeds, 3 are South American, and 7 are Central American. No species was intro-
duced (deliberately).
Weevils (Coleoptera: Curculionidae, sensu lato)
Charles W O'Brien, Entomology-Biological Control, Florida A&M University,
Tallahassee, FL 32307-4100, USA
There are 526 indigenous species of Curculionidae in Florida. The number of pre-
cinctive species of Curculionidae is 115 and the number of indigenous but not pre-
March, 1995
Behavioral Ecology Symposium '94: Frank & McCoy
cinctive species is 411. Among these species of indigenous Florida weevils there are
46 which have distributions in the West Indies and 35 which have distributions which
include Mexico and/or Central America. It is evident from recent collections, which re
duced the number of species that were previously thought to be precinctive in Florida
but are now known to be in the Greater Antilles and other West Indian islands as well,
that the number of precinctive species will be reduced with further collecting. In ad
edition, 50 adventive species are established in Florida; 5 of these were introduced
(deliberately) for biological control of weeds, and 45 are immigrants.
Leaf-rolling moths (Lepidoptera: Tortricidae)
John B. Heppner, Florida State Collection of Arthropods, P.O. Box 147100,
Gainesville, FL 32614-7100, USA
In Florida are reported to occur 239 indigenous species of Tortricidae, of which 26
(11%) are precinctive. In addition, there are 9 immigrant species.
Clear-winged moths (Lepidoptera: Sesiidae)
Larry N. Brown, Environmental Studies, Inc., P.O. Box 14244
Tallahassee, FL 32317, USA
Historically, the clearing moths (family Sesiidae) have been rather difficult to
collect, because adults mimic wasps, fly very fast, are rather inconspicuous, and are
only emergent for a short period of time. The development of scent attractants (pher
omones) within the last two decades has caused tremendous numbers of clearing
moths (mainly males) to be collected, representing many species. The total number of
species of Sesiidae indigenous to Florida is 41 as documented by L. N. Brown & R. F.
Mizell (1993. The clearing borers of Florida (Lepidoptera: Sesiidae). Tropical Lepi
doptera 4 (suppl. 4): 1-21), in which no immigrant species are recorded. Only two
species are known only from Florida. This is not too surprising because the sesiids
clearly colonized Florida from areas to the north and west.
Measuringworms (Lepidoptera: Geometridae)
John B. Heppner, Florida State Collection of Arthropods, P.O. Box 147100,
Gainesville, FL 32614-7100, USA
In Florida are reported to occur 244 indigenous species of Geometridae, of which
33 (14%) are precinctive. In addition, there are 5 immigrant species.
Butterflies (Lepidoptera: Papilionoidea, Hesperioidea)
Thomas C. Emmel, Zoology and Entomology Departments, University of Florida,
Gainesville, FL 32611-0620, USA
The butterfly fauna of Florida is composed of a mixture of temperate species ex
tending into the peninsula from the north and west, and tropical species invading
from the south. There are 199 indigenous species of butterflies in Florida, including
120 Papilionoidea (10 Papilionidae, 24 Pieridae, 40 Nymphalidae, 8 Satyridae, 3 Dan
aidae, 1 Libytheidae, 33 Lycaenidae, and 1 Riodinidae) and 79 Hesperioidea (3 Mega
thymidae and 76 Hesperiidae). These totals include no precinctive species, and 199
indigenous but not precinctive species. One species, Pieris rapae L., is an immi-
grant.
Florida Entomologist 78(1)
Mosquitoes (Diptera: Culicidae)
P. E. Kaiser, Medical & Veterinary Entomology Research Laboratory, USDA-ARS,
1600 SW 23rd Drive, Gainesville, FL 32604, USA
In Florida, the family Culicidae contains 12 genera and 74 indigenous species. The
genera and number of species for each are: Aedes (18), Anopheles (18), Coquillettidia
(1), Culex (14), Culiseta (2), Deinocerites (1), Mansonia (2), Orthopodomyia (2), Psoro
phora (10), Toxorhynchites (1), Uranotaenia (2), and Wyeomyia (3). Only one species,
Anopheles quadrimaculatus sibling species C,, is precinctive to Florida, and addi
tional research may extend its range to southern Georgia. The other 73 species have
distributions outside Florida. There also are 4 immigrant species.
Horseflies and deerflies (Diptera: Tabanidae)
Richard H. Roberts, Florida State Collection ofArthropods, PO. Box 147100,
Gainesville, FL 32614-7100, USA
Ninety-nine species of Tabanidae were listed by C. M. Jones & D. W. Anthony
(1964. The Tabanidae (Diptera) of Florida. USDA-ARS Tech. Bull. 1295) as occurring
in Florida. Of the species listed in that bulletin (which now needs revision), 3 are pre-
cinctive and none are adventive.
Fruit flies (Diptera: Tephritidae)
Gary J. Steck, Florida State Collection of Arthropods, P.O. Box 147100,
Gainesville, FL 32614-7100, USA
Florida is home to 52 species of indigenous tephritid flies based on published
records, which are easily retrievable from R. H. Foote, F. L. Blanc & A. L. Norrbom
(1993. Handbook of the Fruit Flies (Diptera: Tephritidae) of America North of Mexico.
Comstock; Ithaca, New York). Of these, only 4 species are precinctive and the re
maining 48 are indigenous but not precinctive. Further collecting in Georgia
would almost surely reveal the presence of one of the Florida precinctive species; fur
their collecting in the Caribbean would potentially reveal the presence of one or two of
the others. An additional 6 immigrant fruit fly species have been recorded from Flor
ida, but only two (Caribbean fruit fly and papaya fruit fly) have successfully colonized.
The other 4 immigrant species either have been eradicated (e.g., Mediterranean fruit
fly) or never successfully established.
Ichneumon wasps (Hymenoptera: Ichneumonidae)
Virendra K. Gupta, Entomology & Nematology Department, University of Florida,
Gainesville, FL 32611-0630, USA
In 1979, 185 species of Ichneumonidae were reported from Florida by K. V Krom
bein, P. D. Hurd & D. R. Smith, eds. (1979. A Catalog of Hymenoptera in America
North of Mexico. Smithsonian Institution Press; Washington, DC, 3 vols). Another
160+ species were reported in several revisionary works of G. H. Heinrich, H. K.
Townes, C. E. Dasch and V K. Gupta during 1976-1992. Only about 20 of them are
precinctive and 4-5 are adventive (immigrants). Several additional species were
discovered during surveys in 1982-1986, and my estimate of species occurring in Flor
ida is about 500-600. In the groups studied so far, about 30 new species have been
identified but not yet described. It is difficult to say whether these new species are
precinctive, and the likelihood is that most have a wider distribution, mainly in ad
joining states. Several species occurring in Florida also occur in Central America.
March, 1995
Behavioral Ecology Symposium '94: Frank & McCoy
Aphelinids (Hymenoptera: Aphelinidae)
Gregory Evans, Entomology & Nematology Department, University of Florida,
Gainesville, FL 32611-0620, USA
Worldwide, the family Aphelinidae contains about 1,120 species in 40 genera.
About 42 species in 11 genera are reported from Florida. Of these 42, at least 11 were
introduced as biological control agents for homopterous pests, and there is one immi-
grant, leaving perhaps 30 indigenous species. Of these 30, only 3 are reported to oc
cur only in Florida. Most aphelinid species are closely associated with aphid, scale
insect, or whitefly host species, many of which have hitchhiked around the world in
ships, and later in planes, since the time of Columbus. Knowledge of North American
aphelinids is very poor. Knowledge of Florida species has expanded recently because
of surveys of parasitoids of Bemisia tabaci (Gennadius) and of diaspine scales, but
much remains to be done, and an accurate estimate of the number of species is impos
sible.
Ants (Hymenoptera: Formicidae)
Mark A. Deyrup, Archbold Biological Station, P.O. Box 2057,
Lake Placid, FL 33852, USA
There are 149 indigenous species of ants known from Florida (74.2% of the entire
fauna). This figure is based on 11 years of survey work, and is not expected to change
by more than 10 species. This number includes 14 apparently precinctive species,
and 135 indigenous but not precinctive species. The remaining 52 species (25.8%
of the fauna) are immigrants. The most secure precinctives are a group of 5 species
found in xeric uplands in the central peninsula. Eight apparent precinctives might oc
cur to the north of Florida, and one might be West Indian. Relative to Florida, the
other intensively studied southeastern state (North Carolina) has a similar number
of indigenous species (145), but these are a larger percent of the fauna (97.0%), and
there is only one precinctive species.
DISCUSSION
Our estimate of the total number of insect species in Florida is made roughly, but
should be approximately correct. The proportions of species in the subcategory intro-
duced should be accurate. The proportions in the other 3 subcategories, precinc-
tive, indigenous but not precinctive, immigrant, are based on the sample shown
in Table 1 and should be approximately correct: we have no reason to think the sample
is badly biased. We hope that anyone with better methods for deriving estimates will
challenge us and publish them. Overall, we estimate that precinctive species are
about 13% of the indigenous insect species, and about 12% of the total insect species,
in Florida (Table 2). If the estimate of 12,500 insect species in Florida is accepted, and
knowing that 42 introduced species have become established, then the proportions
and numbers in the other subcategories must be approximately as in Table 2.
The differences between the entomofaunal compositions of Florida and Hawaii are
striking (Table 2). Almost all (98.4%) of the Hawaiian indigenous fauna is precinctive,
whereas only about 13% of the indigenous Florida fauna is precinctive. At least part
of the explanation for this difference is the extreme isolation of Hawaii, but other abi
otic and biotic attributes of the Hawaiian environment also may have contributed (see
Mooney & Drake 1986). A much greater proportion (33.5%) of the Hawaiian fauna
than of the Florida fauna (7.9%) also is adventive, despite the greater isolation of Ha
waii. This difference, because it is calculated as a proportion, is accentuated by the
relatively smaller size of the indigenous Hawaiian fauna. Nevertheless, Hawaii has a
Florida Entomologist 78(1)
TABLE 2. A COMPARISON OF THE INSECT FAUNAS OF FLORIDA AND HAWAII.
Florida Hawaii'
Number Percent Number Percent
Indigenous species 11,512s 92.14 5,059 66.5
Precinctive species 1,5145 12.14 4,980 65.5
Indigenous but not precinctive
species 9,9985 80.04 79 1.0
Adventive species 9885 7.94 2,549 33.5
Immigrant species 9465 7.64 2,137 28.1
Introduced species 42 0.33 412 5.4
Total species 12,5002 100 7,608 100
'The numbers for Hawaii are based on number of species now recorded (from Nishida 1994). estimates of the
total number existing, and 'consequences of these estimates. It is not necessarily true that more species occur in
Florida than in Hawaii. 'estimates derived from Table 1, and 'consequences of these estimates.
much greater burden of immigrant species (at least 2,137 vs. about 946). The ratio of
immigrant to indigenous species in Florida, based on our estimates, is about 1:12,
while in Hawaii the ratio is about 1: 2.5 (Table 2). The immigrants to Hawaii are
likely, even more so than immigrants to Florida, to be mainly stowaways in cargoes,
because the barrier of distance precludes much aerial dispersal and rafting. This is
not to say that aerial dispersal and rafting did not occur: they must have been the
methods used by the insects ancestral to the present indigenous population (350-400
species; US Congress 1993). We assume that most of the insects introduced into Ha
waii were introduced for purposes of biological control, as is true of Florida. Their
number in Hawaii is exaggerated by including (apparently) all the species released,
whereas we include for Florida only those species known to have become established.
The high percentages of adventive species in Hawaii (33.5%) and Florida (7.9%) are
strikingly greater than the 1.7% estimated for the contiguous states of the USA
(Sailer 1978), and likely for most of those states individually (US Congress 1993).
ACKNOWLEDGMENTS
We are indebted to Michael C. Thomas (Florida State Collection ofArthropods) for
permitting us to use information from his computerized catalog of Coleoptera, and to
him and all the other specialists who contributed the notes under their names in
cluded in this paper. Randy Lundgren (Gainesville) checked a file of data on Sta
phylinidae. We thank John L. Capinera and J. Patrick Parkman for reviewing a draft
of this manuscript. Roberto Barerra R. provided the Spanish abstract. We thank
George E. Ball (University of Alberta) for bringing the word precinction to our atten
tion. This is Florida Agricultural Experiment Station journal series R-04301.
LITERATURE CITED
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Study of Insects. 4th edn. Holt, Rinehart; New York.
BRIGGS, J. C. 1966. Oceanic islands, endemism, and marine paleotemperatures. Syst.
Zool. 15: 153-163.
March, 1995
Behavioral Ecology Symposium '94: Frank & McCoy
BRIGGS, J. C. 1969. Oceanic islands and endemism: A reply. Syst. Zool. 18: 145-147.
ERWIN, T. L. 1982. Tropical forests: Their richness in Coleoptera and other arthropod
species. Coleopt. Bull. 36: 7475.
ERWIN, T L. 1988. The tropical forest canopy: The heart of biotic diversity, p. 123-129
in E. O. Wilson [ed.]. Biodiversity. National Academy Press; Washington, DC.
FRANK, J. H., AND E. D. MCCOY. 1990. Endemics and epidemics of shibboleths and
other things causing chaos. Florida Entomol. 73: 19.
FRANK, J. H., AND E. D. MCCOY. 1992. The immigration of insects to Florida, with a
tabulation of records published since 1970. Florida Entomol. 75: 128.
FRANK, J. H., AND E. D. MCCOY. 1993. The introduction of insects into Florida. Florida
Entomol. 76: 153.
FRANK, J. H., AND E. D. MCCOY. 1994. Commercial importation into Florida of inver
tebrate animals as biological control agents. Florida Entomol. 77: 120.
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283-296.
GASTON, K. J. 1992. Regional numbers of insect and plant species. Func. Ecol. 6: 243
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GUILLORY, V. 1979. A possible explanation for the absence of endemic fishes in Loui
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Florida Entomologist 78(1)
THE FIRST COMMERCIAL BUTTERFLY FARM AND PUBLIC
EXHIBITION IN THE UNITED STATES
RONALD BOENDER
Founder, Butterfly World Ltd., 3600 West Sample Road,
Coconut Creek, FL 33073-4400
ABSTRACT
Butterfly World rears and displays at any time up to 60 species of butterflies, from
5 continents. The two areas of Butterfly World (farming and public exhibition) have
four or five levels of containment. These are designed to prevent escape of the butter
flies and their larvae, whose presence in nature might damage horticultural or agri
cultural plants.
Key Words: Florida, butterfly, native, exotic
RESUME
Butterfly World ("El Mundo de las Mariposas") cria y mantiene en exhibici6n per
manente, cerca de 60 species de mariposas de cinco continents. Las dos areas, de
crianza y de exhibici6n, cuentan con cuatro o cinco niveles de aislamiento designadas
para impedir la salida de las mariposas y sus larvas al exterior, donde pudieran pro
ducir algun dano a la horticulture o agriculture.
Butterfly World displays a minimum of 2,500 butterflies at all times. During each
year about 150 species are housed, and at any time up to 60 species, from 5 continents,
are on display. Butterflies are imported and reared, and some are exported. Butterfly
World, like other zoological gardens, has several roles. The obvious ones are enter
tainment and education of the public. The less obvious ones are research into rearing
methods, and supply of living specimens to researchers at universities. A potential
role is restocking of endangered species of butterflies to their native lands, once the
environmental disruptions that caused endangerment are rectified.
However, caterpillars (the larvae of butterflies and moths) are phytophagous, and
therefore are classified under federal law and state law as "plant pests." Importation
of "plant pests" into the USA is regulated by USDA-APHIS, and importation of all ar
thropods into Florida is regulated by FDACS-DPI. These laws are designed to prevent
the escape into nature of non-native "plant pests" (federal laws) and non-native ar
thropods in general (Florida law).
The federal and state agencies permit importation of butterflies into escape
proofed holding facilities. Here, I explain how Butterfly World complies with the re
quirements suggested by federal and state officials. Federal and state concerns are ex
pressed by Firko (1994) and Thomas (this symposium).
BUTTERFLY FARMING
Butterflies in nature are attacked at all 4 life stages by parasites, predators, and
pathogens. Farming butterflies requires many methods of protection from, and pre
vention of these, natural enemies. I will deal only with containment from escape in
this symposium, even though some of the following safeguards and construction
evolved from the need to protect the butterflies from natural enemies.
This article is from Florida Entomologist Online, Vol. 78, No. 1 (1995).
FEO is available from the Florida Center for Library Automation gopher (sally.fcla.ufl.edu)
and is identical to Florida Entomologist (An International Journal for the Americas).
FEO is prepared by E. O. Painter Printing Co., P.O. Box 877, DeLeon Springs, FL. 32130.
March, 1995
Behavioral Ecology Symposium '94: Boender
Our buildings, laboratory, outdoor rearing areas, and flight areas, were designed
and constructed to ensure that butterflies could not escape from their containment, ei
their as caterpillars or as adults. Planning resulted from a partnership with Clive Far
rell, owner of the London Butterfly House (England), and the design was created by
James Gardner (of England). Butterfly World opened in 1988, and it has an advisory
board of biologists.
Butterfly larvae are raised both indoors and outdoors depending on species and
food-plant preference. Most are reared from egg to adult indoors. A laboratory is con
structed in the inner part of the building, with hallways leading to the outside and a
minimum of two doors to the outdoors. All walls and floors are kept spotless and are
cleaned daily. All eggs and larvae are kept in special rearing containers which are
sealed for the entire egg and larval period. The larvae raised outdoors are held in 183
x 183 x 244 cm (6' x 6' x 8') screened, enclosed cubicles. The base of each door is
equipped with a rubber sweep. For a larva to escape to the wild, it would have to crawl
through 5 doors, a series of hallways, and a distance of about 46 m (150').
The general public has no access to the larval-growth areas. Any special visitors al
lowed into these areas must be accompanied by laboratory personnel. All plants re
moved from the larval-growth areas are placed in a screen-enclosed nursery with a 2
door vestibule-like entry/exit. If any larvae or pupae were left on the plants, they
would hatch in this enclosed environment.
The adult butterflies in the breeding areas are likewise kept in 183 x 183 x 244 cm
cubicles. To escape, they first must get through the door of their cubicle, which puts
them in a narrow hallway and very visible. From the hallway, they must get through
two more doors to enter a protected screened nursery which has two more doors with
vestibule to the outdoors.
EXHIBITION
The public exhibition areas are designed to contain adult butterflies for public
viewing. The only egg-laying females or larvae allowed in these areas are of native
species for educational purposes. Host plants for non-native species are not kept in
the public areas. The general public has one entrance and one exit to the exhibition
areas. The entrance requires passage through two doors, a long indoor hallway, and
a high velocity blower. Butterflies cannot orient indoors without polarized light, so the
two doors, hallway, and blower provide four levels of protection. At the exit, the public
is reminded to check clothing for hitchhikers, then must pass through a set of doors,
a set of plastic strips, a high velocity blower, and another set of doors. These give five
levels of protection.
There are three openings to the public exhibition for workers from the laboratory
or horticulture. Each opening consists of a two-door vestibule which opens into
screened nurseries which again have two-door vestibules to the outdoors.
The grounds surrounding the public exhibition are planted with thousands of nec
tar-bearing plants (upon which adult butterflies might feed) and host-plants (upon
which female butterflies might oviposit). This is designed to attract and retain any es
capees.
CONCLUSION
The two areas of Butterfly World (public exhibition and farming) have four or five
levels of containment. These are designed to prevent escape of the butterflies, whose
presence in nature might damage horticultural or agricultural plants. The safeguards
to escape have been refined since opening of Butterfly World in 1988.
Florida Entomologist 78(1)
In reality, few species of butterflies pose a threat to agriculture or horticulture.
Among non-native butterflies which have become important pests in the USA are Pi
eris rapae (L.) [called "small white" in England, and "imported cabbageworm" in the
USA including Florida, though Gerberg & Arnett (1989) call it "European cabbage
butterfly"]. Its close relative Pieris brassicae (L.) [called "large white" in England, and
"European cabbageworm" in the USA] has not yet colonized the USA and is a prime
example of a butterfly species whose arrival would harm agriculture. It was against
P rapae that the first biological control project in the USA was attempted (Van Den
Bosch et al. 1982).
Even native species of butterflies can be harmful to horticultural and agricultural
plants. The atala butterfly (Eumaeus atala Poey subspecies florida Roeber) was con
sidered virtually extinct in Florida from the late 1950s, but was reintroduced from a
surviving population on Key Biscayne, and by the end of the 1970s was again wide
spread (Emmel 1991). Its larvae eat leaves of native and introduced species of Zamia
(Cycadales), which have ornamental value, so the butterfly larvae may be considered
to be pests. Larvae of Dione vanilla (L.) subspecies nigrior Michener (the gulf fritil
lary) feed on leaves of Passiflora spp., and those of various skipper butterflies feed on
leaves of Canna spp. and bean plants, and are pests to those who try to grow these
plants. It becomes a question of whether the grower of plants is willing to sacrifice
damage to the plants in return for the pleasure awarded by the sight of the butterflies.
REFERENCES CITED
EMMEL, T. C. 1991. Butterflies. Mallard Press; New York.
FIRKO, M. J. 1994. The USDA permitting process. in Invertebrates in Captivity, 2nd
Annual Conference, Proceedings. Tucson, AZ.
GERBERG, E. J., AND R. H. ARNETT. 1989. Florida butterflies. Natural Science Publi
cations; Baltimore, MD.
THOMAS, M. C. 1995. Invertebrate pets and the Florida Department of Agriculture
and Consumer Services. Florida Entomol. 78:
VAN DEN BOSCH, R., P. S. MESSENGER, AND A. P. GUTIERREZ. 1982. An introduction to
biological control. Plenum; New York.
March, 1995
Behavioral Ecology Symposium '94: Thomas
INVERTEBRATE PETS AND THE FLORIDA DEPARTMENT OF
AGRICULTURE AND CONSUMER SERVICES
MICHAEL C. THOMAS
Division of Plant Industry, Florida Department of Agriculture and Consumer Services
P.O. Box 147100, Gainesville, FL 32614-7100
ABSTRACT
The Division of Plant Industry (DPI) of the Florida Department of Agriculture and
Consumer Services now regulates importation into Florida of all arthropods except
Crustacea, no longer just those of actual or potential agricultural importance. The op
rating law is Chapter 581.083 of the Florida Statutes, and the operating procedure
is Title 5B-57.004 of the Florida Administrative Code. The current law was proposed
because of importation by the pet trade of species that did not already occur in Florida
and were potentially harmful to the environment. The Division requires specimens
(for confirmation of identification) to accompany applications for permits.
Key Words: Exotic species, introduction, Florida, permits, insects
RESUME
La Division de la Industria de los Vegetales (DPI) del Departamento de Agricul
tura y Servicios al Consumidor de la Florida, ahora regular la importaci6n a la Florida
de todos los artr6podos excepto crustaceos) y no unicamente de aquellos con impor
tancia real o potential para la agriculture. La ley es el Capitulo 581.083 de los Esta
tutos de la Florida, y el procedimiento operative es el Titulo 5B-57.004 del C6digo
Administrative de la Florida. La ley actual fue propuesta debido a la importaci6n por
los comerciantes de mascotas de species que no existen naturalmente en Florida y
que potentialmente pueden ser daninas al medioambiente. La Division require que
las solicitudes de permisos sean acompannadas por especimenes (para confirmar la
identificaci6n).
For the pet industry the days of "how much is that doggy in the window" are long
gone. Now it's "how much is that tarantula in the window", and the one with the wag
gly tail may very well be a scorpion.
In the ever-increasing search for novelty, more and more exotic invertebrates are
being offered for sale in pet stores. A perusal of price lists from pet suppliers reveals
tarantulas, scorpions and solpugids, whip scorpions and wolf spiders, centipedes and
millipedes, mantids and walking sticks, spider wasps and velvet ants, dung beetles
and blister beetles that originate from 4 continents, Africa, Asia, Central America,
and South America. There are 108 species of tarantulas alone in the pet trade.
In most of the continental United States, these tropical arthropods are relatively
benign curios, but in Florida-especially subtropical south Florida-they may pose
unknown agricultural or environmental hazards. This brings such exotic arthropods
directly under the purview of the Florida Department of Agriculture and Consumer
Services (hereafter referred to as department).
For plants and vertebrates the proportion of exotics in south Florida is alarming
(Ewel 1986). The invertebrates are much more poorly known, but Frank & McCoy
This article is from Florida Entomologist Online, Vol. 78, No. 1 (1995).
FEO is available from the Florida Center for Library Automation gopher (sally.fcla.ufl.edu)
and is identical to Florida Entomologist (An International Journal for the Americas).
FEO is prepared by E. O. Painter Printing Co., P.O. Box 877, DeLeon Springs, FL. 32130.
Florida Entomologist 78(1)
(1992) listed 271 immigrant species of insects reported from Florida in a 20-year pe
riod. For this reason, the Division of Plant Industry of the department now regulates
the importation of all arthropods and other possible invertebrate plant pests into the
state. This seems to be an unprecedented step by a state department of agriculture.
Although the department has regulated the importation of plant pests and parasi
toids of plant pests for years, mostly for research or biological control purposes (Den
mark & Porter 1973), the regulation of the pet trade in arthropods is a whole new
ballgame, and policies and procedures are still evolving as the department gains ex
perience.
HISTORY
The story begins on 30 May 1989 with a newspaper article in the Tampa Tribune
(Chen 1989a). The cute feature article reported on a Tampa pet store selling Mada
gascan hissing cockroaches (Gromphadorhina sp.) for pets (Fig. 1). The pet store had
sold six of the roaches for $6.00 a piece. The news story had two results: first, the pet
store was inundated by telephone calls from people wanting to buy a roach; second,
the Commissioner of Agriculture's office was receiving calls from people wanting to
know how roaches could be sold as pets in Florida, a state renowned for its roach prob
lems (Chen 1989b).
Some quick telephone calls found that neither the U.S. Department of Agricul
ture's Animal and Plant Health Inspection Service (APHIS) nor the U.S. Public
Health Service was interested in the Madagascan hissing cockroach. Concerned over
the possibility that yet another roach might be added to the state's non-native roach
fauna, and acting under its general statutory authority, the department issued a stop
sale order to the pet store two days after the first newspaper story appeared (Chen
1989b). In the meantime, the pet store had sold the remaining six roaches it had in
stock. Four of the roaches were sold to an unidentified man who released them in his
back yard because he was afraid the department would hurt them (Chen 1989c). All
of this, of course, was followed gleefully in the press. The publicity seemed to fuel the
popularity of the roaches and the next thing we knew a pet store in Miami was selling
the former $6.00 Madagascan hissing cockroaches for $19.95. The roaches were con
fiscated by department inspectors (United Press International 1989).
Several things became apparent during this time. The new attention on the pet
trade revealed that the Madagascan hissing cockroach was literally just the tip of an
arthropod iceberg hiding in pet stores around the state. Many exotic arthropods were
being imported and sold as either pets or pet food. Although several Federal and state
statutes apply to plant-feeding or disease-vectoring insects, there were gaping loop
holes that allowed such things as roaches and spiders to be imported and distributed
with virtually no regulation.
It is well known that Florida, particularly south Florida, is especially vulnerable
to the establishment of exotic organisms (Ewel 1986). The pet trade is responsible for
many of those problems, and certain aquarium plants are now prohibited from being
sold in Florida. The Florida Game & Fresh Water Fish Commission regularly inspects
pet stores and is responsible for issuing permits for the sale of exotic vertebrates. The
question naturally arose: Is there an arthropod equivalent of melaleuca, walking cat
fish, or cane toad being sold in pet stores?
The department's enabling legislation, which authorizes the regulation of plant
pests and parasites of plant pests, was not adequate for this problem. In January
1990, House Bill 2163 was introduced to amend Chapter 581.083 of the Florida Stat
utes. It passed on 29 May and became effective on 1 October. The amendment' and
March, 1995
Behavioral Ecology Symposium '94: Thomas
Rule 5B-57 give the department the authority to regulate any arthropod (with the ex
ception of crustaceans) and require a permit to import into the state or distribute any
arthropod that may pose a threat to the agricultural industry or to the environment.
CURRENT SITUATION
The department has now had more than a year of experience with the new proce
dure, and the arthropod iceberg seems to be getting bigger and bigger. With some ex
ceptions, the department has concentrated on regulating suppliers and breeders
rather than individual pet stores. Department inspectors visited pet stores informing
owners of the new regulations and gathering addresses of suppliers who were con
tacted and notified of the new requirements.
The Florida Game & Fresh Water Fish Commission, whose personnel regularly in
spect pet stores, has been reluctant to expand its inspections to cover invertebrates,
but it did supply the department with a list of 3700 businesses and individuals in
Florida permitted by the Commission to have and sell exotic vertebrates. This list was
the basis of an informational mailing. In the past year, over 70 permit applications
were submitted for invertebrate pets; most of those came in the two months following
the informational mailing.
Permit applications come from zoos, museums, and schools, as well as from dis
tributors, breeders, and pet stores. For the most part, permits are handled on a case
by-case basis, and the proposed use of the organism plays an important part in the de
cision-making process. For example, a permit is much more likely to be issued for a
zoo or museum exhibit than for retail sale. Several criteria are considered in reaching
a recommendation. The organism should not be a threat to the state's agricultural in
dustry It should not be a threat to the public health. If it is likely to become estab
lished under Florida climatic conditions, it should not compete with native species.
Based on these criteria, there are certain organisms that either would not be per
mitted or would be permitted under very tight restrictions. Among these are: plant
feeding terrestrial snails (we are regularly contacted by people wanting to farm brown
garden snails); all cockroaches; scorpions of the family Buthidae; stick insects and
grasshoppers; all millipedes. Desert tarantulas are not considered a problem, but the
genera Avicularia and Phormictopus, which contain arboreal species, are restricted.
The house cricket, Acheta domesticus, has been sold as fish bait and reptile food for
'Florida Statutes 581.083. Introduction or release of plant pests, noxious weeds, or organisms
affecting plant life. The introduction into or release within this state of any plant pest, noxious
weed, or genetically engineered plant or plant pest, or any other organism which may directly or
indirectly affect the plant life of this state as an injurious pest, parasite, or predator of other or
ganisms, or any arthropod, is prohibited, except under special permit issued by the department
through the division, which shall be the sole issuing agency for such special permits. Except for re
search projects approved by the department, no permit for any parasitic organism shall be issued
unless the department has determined that the parasite, predator, or biological control agent is a
target organism or plant specific and not likely to become a pest of plants or other beneficial or
ganism. The department may rely on the findings of the Department of Natural Resources and the
United States Department of Agriculture in making any determination about organisms used for
the biological control of aquatic plants.
Florida Administrative Code 5B-57.004 Possession or Movement of Arthropods, Plant Pests, or
Noxious Weeds Regulated by the Department.
(1) It is unlawful to introduce, possess, move, or release any arthropod or noxious weed regu
lated by the department except under permit issued by the department. No permit shall be issued
unless the department has determined that the arthropod or noxious weed can be contained to
prevent escape into the environment or that it will not pose a threat to agriculture, beneficial or
ganisms, or the environment or become a public nuisance...
Florida Entomologist 78(1)
Fig. 1. Madagascan hissing roaches sold by pet stores. Photo courtesy of Associated
Press Photos.
decades; it has not become established in the wild in Florida and is not considered a
problem. Generally, exotic insects, even pest species, are permitted if they are already
established in the state.
Procedures
Arthropods falling under the jurisdiction of the USDA must obtain a USDA/
APHIS PPQ form 526, which is sent to Hyattsville, MD with the department's recom-
mendation either to approve or disapprove. Arthropods not falling under the jurisdic
March, 1995
Behavioral Ecology Symposium '94: Thomas
tion of the USDA are covered under the department's PI-208 permit, which is handled
in Gainesville. All permit applications must be submitted with voucher specimens of
the species to be imported. As I will discuss later, this is an important step since one
of the most frequent problems encountered is misidentification by the applicant. The
final decision on approval is made by the division's assistant director, acting on the
recommendation from the technical sections in the Bureau of Entomology, Nematol
ogy, and Plant Pathology.
Specific Cases
The potential hazards of invertebrate pets are not entirely theoretical. In the
1960s, a Miami family carried two giant African snails (Achatina fulica Bowditch)
home with them as pets from a trip to Hawaii. Eventually they tired of the snails and
released them in their back yard. It took a million-dollar campaign by the department
to eradicate the resulting infestation. Just recently, a pet store in Tallahassee was dis
covered to have another, related giant African snail (Archachatina marginata (Swain
son)) for sale. The supplier was identified and through the supplier several other
Florida pet stores were found to be carrying the snail in stock.
In another case, five specimens of a giant Neotropical grasshopper (Tropidacris c.
cristata (L.)) were collected over a period of about a month in 1992 in a small area in
Broward County. How the grasshoppers arrived in central Broward County has never
been determined, but since this is one of the largest and most spectacular grasshop
pers in the world, it was suspected that they were escapees from a shipment destined
for sale in the pet trade.
To illustrate the potential problems inherent in the unregulated trade of exotic in
vertebrates, I will discuss three specific cases with which the department has dealt
since the new rules became effective.
Blaberus roaches. The New World genus Blaberus contains several species of very
large roaches that are popular in zoo and educational displays, and, it turns out, as
reptile food. Two species, Blaberus craniiferBurmeister, the Cuban death's head cock
roach, and Blaberus discoidalis Serville occur in extreme south Florida. Whether they
are native, are the result of natural dispersal, or were hitchhikers in cargoes is open
to debate, but both are widely distributed in the Caribbean and may be considered a
natural component of the Florida Keys fauna (Atkinson et al. 1990). A Tampa zoo re
quested permission to maintain its colony of Blaberus giganteus (L.), which were be
ing used as reptile food and which originally had been obtained from a well-known
biological supply house. Examination of voucher specimens from the zoo revealed that
the species in question was neither Blaberus giganteus nor Blaberus craniifer Instead
it was most similar to an unidentified species of Blaberus from Ecuador in the Florida
State Collection of Arthropods. In this case we reached a compromise by which the zoo
destroyed its colony of exotic roaches and the department supplied specimens of Blab
erus craniifer to start a new culture. By the way, Blaberus giganteus is attracted to
light. If central Florida residents are upset at the appearance at their lights of the
Asian cockroach (Blattella asahinai Mizokubo), think of their reaction to the arrival
of a cockroach the size of a small bird.
Zophobas beetles. Many pet stores carry giant mealworms. These are the larvae of
a large darkling beetle that are popular as food for pet birds and especially lizards.
They are also sold as fish bait. They are said by suppliers to belong to the species Zo
phobas morio (Fabricius), which has been listed from south Florida and which is well
represented in the Florida Collection of Arthropods with specimens from the lower
Keys. Specimens of this genus are virtually unidentifiable, but according to Charles
Triplehorn (Museum of Biological Diversity, Columbus, OH) the proper name of the
Florida Entomologist 78(1)
Florida species seems to be Zophobas rugiceps Kirsch, which is widely distributed in
the Caribbean. Unfortunately, the species being sold is not conspecific with the Flor
ida examples and may have originated in Central or South America. The department
has in the past denied permits to suppliers to import this beetle but, as it is easy to
culture, many pet stores and individuals have their own breeding colonies. Its pest po
tential is unknown but it is related to several stored-products pests.
Chilecomadia moths. "Butterworms" are advertised by the distributor as "the soft
est worm" and are sold as reptile food in the United States and Europe. In his permit
application, the importer spelled the scientific name incorrectly, did not know the
family, claimed the larvae were found under rocks in Chile, and that they would im
mediately die if removed from refrigeration. Eventually, butterworms turned out to be
the caterpillars of a Chilean cossid moth, Chilecomadia morrei Silva Figueroa. Re
moved from refrigeration, they lived at least three weeks and fed readily on artificial
diet. Cossids are wood-borers as larvae, and recorded hosts for this species in Chile in
clude willows. A related Chilean species is recorded from willow, acacia, and apple.
The permit was denied.
CONCLUSION
There is no doubt that invertebrate pets are growing in popularity and that they
pose a real threat to Florida's agriculture and environment. Efforts by the Florida De
apartment of Agriculture and Consumer Services to regulate the importation into the
state of exotic arthropods and other possibly harmful invertebrates will minimize, but
hardly eliminate, the hazards.
ACKNOWLEDGMENTS
I thank G. B. Edwards, Maeve McConnell, and Michelle Faniola, Division of Plant
Industry, for their help in compiling information, and Drs. Edwards and Wayne Dixon
for criticizing the manuscript. Manuel Balcazar L. kindly translated the abstract into
Spanish. This is Entomology Contribution No. 810, Bureau of Entomology, Nematol
ogy and Plant Pathology, Division of Plant Industry, Florida Department of Agricul
ture and Consumer Services.
REFERENCES CITED
ATKINSON, T H., P. G. KOEHLER, AND R. S. PATTERSON. 1990. Annotated checklist of
the cockroaches of Florida (Dictyoptera: Blattaria: Blattidae, Polyphagidae,
Blattellidae, Blaberidae). Florida Entomol. 73: 303-327.
CHEN, G. 1989a. Roaches crawl into pet market. The Tampa Tribune, 30 May 1989. p.
1B-6B
CHEN, G. 1989b. Roaches give officials something to hiss about. The Tampa Tribune,
3 June 1989. p. 1A-10A.
CHEN, G. 1989c. Sympathetic roach owner frees critters. The Tampa Tribune, 6 June
1989. p. 1B
DENMARK, H. A., AND J. E. PORTER. 1973. Regulation of importation of arthropods into
and of their movement within Florida. Florida Entomol. 56: 347-358.
EWEL, J. J. 1986. Invasibility: lessons from south Florida, p. 214-230 in H. A. Mooney
and J. A. Drake [eds.] Ecology of Invasions of North America and Hawaii.
Springer-Verlag; New York.
FRANK, J. H., AND E. D. MCCOY. 1992. The immigration of insects to Florida, with a
tabulation of records published since 1970. Florida Entomol. 75: 128.
UNITED PRESS INTERNATIONAL. 1989. Booted from Tampa, roaches turn up in Miami.
The Tampa Tribune-Times, 22 October 1989.
March, 1995
Behavioral Ecology Symposium '94: Center et al.
BIOLOGICAL INVASIONS: STEMMING THE TIDE IN FLORIDA
TED D. CENTER', J. HOWARD FRANK2, AND F. ALLEN DRAY, JR.
'USDA, ARS, Aquatic Weed Control Research Laboratory, 3205 College Ave.,
Fort Lauderdale, FL 33314
2University of Florida, Department of Entomology and Nematology,
Gainesville, FL 32611-0620
3University of Florida, Fort Lauderdale Research and Education Center,
3205 College Ave., Fort Lauderdale, FL 33314
ABSTRACT
Invasive, adventive species present a significant challenge to environmental re
source managers. Unless this problem is addressed, natural areas face loss of biodi
versity and habitat integrity. Traditional control methods are often inappropriate or
impractical for use in natural areas. Strategies using biological control, a discipline of
applied ecology, offer the best hope for reducing deleterious impacts of invaders. Ar
guments by some ecologists that classical biological controls contribute to the problem
appear unwarranted. These criticisms should not be dismissed out of hand, however.
Instead, they should foster in biocontrol scientists a renewed dedication to the safe
practice of their discipline and an increased concern for collateral impacts of released
organisms on native species.
Key Words: Biological control, invasive species, weeds, insects, Florida
RESUME
Las species adventivas e invasoras presentan un desafio significativo para los ad
ministradores de recursos ambientales. A no ser que este problema sea considerado,
las areas naturales encaran p6rdidas en la biodiversidad y en la integridad del medio
ambiente. Los m6todos tradicionales de control son frecuentemente inapropiados o
impracticos para ser usados en areas naturales. Las estrategias que usan control bio
16gico, lo cual es una discipline de la ecologia aplicada, ofrecen la mayor esperanza
para reducir los impacts daninos de los invasores. Los arguments de algunos ec6lo
gos de que el control biol6gico clasico contribute al problema parecen ser injustifica
dos. Sin embargo estas critics no deben de ser desechadas de inmediato. En su lugar
deben de alentar en el cientifico dedicado al control biol6gico una renovada decidica
ci6n a la practice segura de su discipline y un aumento en su preocupaci6n por los im
pactos paralelos de los organismos liberados en las species naturales.
Environmentalists and conservationists have often failed to appreciate the threat
posed by invasive, adventive species to biodiversity in natural areas (see, for example,
Soule & Wilcox 1980). In recent years, however, the impact of exotic organisms on bi
logical communities, particularly in natural areas, has become a compelling environ
mental issue (McKnight 1993). This is particularly true in Florida and a briefing
document for the state legislature has recently been prepared on this subject by a del
egation of experts assembled by the Florida Department of Environmental Protection.
The best documented cases are those evolving from purposeful importations of non-in
This article is from Florida Entomologist Online, Vol. 78, No. 1 (1995).
FEO is available from the Florida Center for Library Automation gopher (sally.fcla.ufl.edu)
and is identical to Florida Entomologist (An International Journal for the Americas).
FEO is prepared by E. O. Painter Printing Co., P.O. Box 877, DeLeon Springs, FL. 32130.
Florida Entomologist 78(1)
digenous plants. The magnitude of this problem cannot be exaggerated. About 456
million exotic plants were imported through the 16 U.S. plant introduction facilities
during 1993, with nearly 80% of these coming through the port of Miami (pers. comm.
-D. R. Thompson, Operations Officer, USDA-APHIS Port Operation, Hyattsville,
MD). These imported plants represent a huge pool of potential invaders, directly
through their own escape and naturalization, and indirectly through the insects and
other pests that they might harbor.
The number of organisms imported for biological control purposes pales in compare
ison, yet biocontrol is increasingly being identified as contributing to the problem
rather than proffering a cure (Howarth 1983, Simberloff 1992). This viewpoint repre
sents more concern for the "mole hill" than for the "mountain". Still, the concerns ex
pressed are not altogether unwarranted. It would behoove biological control
practitioners, therefore, to take a proactive stance in order to ensure that biological
control does not come to be regarded as an ecological pariah.
THE PROBLEM
Introduced and immigrant plant species represent a severe challenge for conser
vationists. Those that successfully invade natural areas may outcompete native spe
cies and develop extensive monocultures. These monocultures not only exclude native
ecological homologs, but frequently also exclude many associated species. In extreme
cases, such invasions can convert a 1.. li ., diverse biological community into a bar
ren monoculture.
The susceptibility of pristine areas to invasion by exotic species is partially related
to disturbance and the size of reserves. Disturbed edge habitats presumably function
as staging areas from which exotic species invade the surrounding landscape. Other
things being equal (see Londsdale 1992), smaller areas with proportionately more
edge habitat are more susceptible to invasions than large contiguous conservation ar
eas (see Ewel 1986 for other theories). This suggests that the establishment of large
reserves might impede invasions by exotics. However, vast size alone does not pre
clude problems. Perhaps the best example of a large preserve is Kakadu National
Park (13,000 km2) and adjacent aboriginal reserves in Australia's Northern Territory.
Together, these comprise one of the world's largest protected natural areas which en
compasses the entire Alligator River drainage basin. Yet, the pristine nature of this
area is threatened by invasions of adventive species. The weedy legume Mimosa pel
lita Humb. & Bonpl. ex. Willd. (=M. pigra L.) now occupies 450 km2 of seasonally in
undated floodplain in nearby areas. The establishment of this species was facilitated
by yet another adventive species, the water buffalo (Bubalus bubalis), which tram
pled the floodplains, thereby creating disturbed habitat. These buffalo also browsed
competing vegetation. M. pellita has now effectively transformed a wide range of
structural vegetation types to homogenous tall shrublands, thus causing disastrous
consequences to wildlife (Beckman 1990, Londsdale & Braithwaite 1988; Braithwaite
et al. 1989). This plant also blocks river and wetland access to local fauna while the
floating fern Salvinia molesta Mitchell impedes access to seasonal ponds (billabongs).
These freshwater habitats are the principal source of water for wildlife during the
long dry season, so this transformation has far-reaching impacts. Furthermore, Afri
can grasses which are taller with deeper root systems than native species, fuel hotter
fires later in the dry season than those typically carried by native grasses. These hot
ter fires destroy the otherwise fire-resistant sclerophyllous woodlands (Breeden &
Wright 1989). Hence, invasive exotic plants are degrading aquatic and upland habi
tats alike.
March, 1995
Behavioral Ecology Symposium '94: Center et al.
Ecological complexity has also been linked to the susceptibility of natural commu
nities to invasions, species-rich communities supposedly being less susceptible than
species-poor ones (Ewel 1986). The fynbos of South Africa is one example where this
generalization fails, however. This distinct floral kingdom is perhaps the most diverse
non-tropical system on earth, harboring as many as 121 plant species within a 100 m2
area (van Rensburg, undated). Despite this high diversity, the fynbos is threatened by
invasive exotic plant species like Acacia spp., Hakea spp., Pinus spp., Sesbania puni
cea (Cav.) Benth., etc. (Taylor 1978). Likewise, rubber vine (Cryptostegia grandiflora
R. Br.) from Madagascar grows rampant in subtropical and tropical Queensland, an
other highly diverse region, covering trees up to 30 m tall and choking out native veg
etation (McFadyen & Harvey 1991).
An example of an invasion by an exotic species into a species-rich, relatively un
disturbed area is provided by Salvinia molesta. This South American native was prob
ably released in New Guinea from aquaria. A few plants wound up in aquatic sites on
the Sepik River floodplain in about 1971-72. The plant spread rapidly, with nearly di
sastrous consequences (Mitchell et al. 1980, Thomas & Room 1986a,b).
Exceptions can be found to most generalizations pertaining to factors contributing
to site invasibility. This is because invasibility depends upon characteristics of both
the invading species and the habitat being invaded. Thus, a particular site might be
very susceptible to invasion by one species but resistant to another. Likewise, a single
exotic species might easily invade at one site, but be unsuccessful at another. One fac
tor remains paramount, however. Potential invaders must be available. Proximity
and availability of a pool of invasive species is a preeminent factor. This factor is ig
nored by most ecologists who study biological invasions, being either too obvious or
perhaps merely biologically uninteresting.
The main source of potential invaders appears to be the commercial importation of
plants. As noted previously, vast numbers of plants are imported to the United States
each year. This creates a tremendous pool of potential invaders. Obviously, the more
exotic species that are present, and the higher the frequency with which they are im
ported, the greater the likelihood that one or more will invade natural areas.
Ewel (1986) observed that few mammals or trees have invaded the mature forests
of the Amazon basin, New Guinea, or Zaire, as compared to Great Britain or New
Zealand. He suggested that high species richness and absence of disturbance insu
lates these communities from invasion. We suggest that lack of economic incentives
for the importation of large quantities of ornamental species also explains much of the
disparity. In the case of New Zealand, for instance, active "acclimatization" societies
have existed since the colonial period (Booz 1991). These societies were dedicated, un
til the early 1900s, to the introduction of all plant and animal species that they con
sidered desirable. Hundreds of species were thus imported and released. Many of
these invaded natural communities. Were it not for these societies, many of these in
vasions would never have occurred. Although formal acclimatization societies don't
exist in Florida, efforts to introduce non-native species (including plants, fish, birds,
reptiles, etc.) have been at least as intensive. Florida's biota now includes over 1300
adventive species (U.S. Congress 1993). To our knowledge, no comparable effort has
ever been made to introduce species into the aforementioned Amazon basin, New
Guinea, or Zaire.
Examples of commercially imported plants "gone bad" are readily available. The
paperbark tree (Melaleuca quinquenervia (Cav.) S. T Blake) in Florida (Bodle et al.
1994, Hofstetter 1991), Chinese tallow tree (Sapium sebiferum (L.) Roxb.) in the
Southeast (Farnsworth 1988), and purple loosestrife (Lythrum salicaria L.) in the
northern U.S. (Thompson et al. 1987, Malecki et al. 1993) devastate valuable wet
Florida Entomologist 78(1)
lands. Austin (1978), in fact, reported that M. quinquenervia reduces biodiversity by
60-80% when it invades wet prairie or marsh communities. It now occupies an esti
mated 489,000 acres in southern Florida (pers. comm. A. Ferriter, South Florida Wa
ter Management District, West Palm Beach, FL).
Brazilian peppertree (Schinus terebinthifolius Raddi) was reported as being com-
mon in cultivation but rare in the wild in southern Florida as recently as 1959 (Austin
1978). It now infests 602,000 acres (pers. comm. A. Ferriter, South Florida Water
Management District, West Palm Beach, FL) in a wide variety of habitats, displacing
native vegetation in both upland and wetland communities (Myers & Ewel 1990).
Acreages would be considerably higher if estimates from the rest of Florida were
available. Australian pine (Casuarina equisetifolia J. R. Forst. & G. Forst.) interferes
with the nesting activities of sea turtles and American crocodiles in coastal communi
ties (Austin 1978) and infests 373,000 acres in southern Florida (pers. comm. A. Fer
riter, South Florida Water Management District, West Palm Beach, FL). This species
is also reported to inhibit growth of native plants and to open beaches and dunes to
erosion. Austin further noted that as few as a dozen species typically occur in the un
derstory, most of which are adventive. Brazilian peppertree and Australian pine were
both introduced as landscape plants.
Cogongrass (Imperata cylindrica (L.) Beauv.) was imported into Florida in the
1940s for erosion control and as a source of forage. It failed to be useful for either pur
pose and now displaces native plants (Coile & Shilling 1993). Another plant intro
duced for erosion control in Florida and other portions of the Southeast is the
notorious kudzu (Pueraria lobata (Willd.) Ohwi) (Baker 1986). Like the madagascar
ine rubber vine in Australia, it blankets tall trees and smothers native vegetation.
Other vines cause similar problems in Florida with the Japanese climbing fern (Lygo
dium microphyllum (Cav.) R. Brown), air potato (Dioscorea bulbifera L.), and skunk
vine (Paederia spp.) being good examples. Austin (1978) recorded L. microphyllum
populations from several counties in southern Florida, and it has recently been re
ported to infest 26,000 acres, mostly in Palm Beach and Martin counties (pers. comm.
-A. Ferriter, South Florida Water Management District, West Palm Beach, FL).
Aquatic habitats seem particularly vulnerable to invasion. The neotropical float
ing waterhyacinth (Eichhornia crassipes (Mart.) Solms.) blankets open water sur
faces of lakes and rivers in Florida as well as most other subtropical and tropical
areas of the world. Infestations limit access to fishing areas by indigenous peoples in
undeveloped countries, increase habitat for disease vectors, reduce the supply of fresh
water available to wildlife, and lower oxygen levels in the submersed community.
Drifting mats scour native vegetation and destroy nesting sites and foraging areas for
rare species (such as the snail kite in Florida). This plant was introduced to decorate
garden ponds. The submersed weed hydrilla (Hydrilla verticillata (L.f.) Royle) was in
produced through the aquarium trade. It invades aquatic sites by growing from the
hydrosoil to the water surface where it forms a thick canopy The resultant dense beds
readily displace other submersed aquatic species. As a result, diverse aquatic commu
nities become monocultures. These often lack phytophagous consumers and harbor
less desirable detritivore-based faunal assemblages (e.g., Hansen et al. 1971, Dray et
al. 1993).
Imported plants threaten the preservation of "pristine" natural areas in other
ways. Exotic insects, many of which attack native plants, are often imported on orna
mental plants. A recent study estimated that, as of 1992, 271 exotic insect species
have immigrated into the state of Florida during the previous two decades. In con
trast, only 151 species have been introduced into Florida for biological control pur
poses in the past century In 1980 over 18,000 immigrant insects were intercepted by
March, 1995
Behavioral Ecology Symposium '94: Center et al.
the U.S. Department of Agriculture (APHIS) at ports of entry (Frank & McCoy 1992,
1993). These were mostly transported on imported plants, 99% of which are not in
spected.
Some of these immigrants (e.g., the gypsy moth in northern areas) have the capac
ity to reduce biodiversity in native plant communities. A good example is the cactus
moth (Cactoblastis cactorum (Bergroth)) in Florida, which was purposely released in
the Caribbean region during the 1950s for biological control of Opuntia spp. Recent
evidence (pers. comm. R. Pemberton, U.S. Department of Agriculture, Agricultural
Research Service, Aquatic Weed Control Laboratory, Fort Lauderdale, FL) suggests
that it arrived in Florida within exotic cacti, truckloads of which are routinely im
ported from the Dominican Republic and Brazil. Once here, it began to attack several
species of native cacti (Simberloff 1992), including the endangered semaphore cactus
(Opuntia corallicola (Small) Werdermann in Backeberg).
The weevil Metamasius callizona (Chevrolat) arrived in Florida from Mexico in
shipments of exotic bromeliads (O'Brien & Thomas 1990). It now infests Tillandsia
utriculata L., T fasciculata Sw., and T paucifolia Baker, all native bromeliad species
(Frank & Thomas 1994), and has nearly extirpated T utriculata from several south
ern Florida hammock communities (TDC, pers. obs.). A related weevil M. hemipterus
(L.), first discovered in Florida in 1984, feeds on a wide range of hosts including ba
nanas, sugarcane, and palms (Woodruff & Baranowski 1985, Giblin-Davis etal. 1994).
It could jeopardize the few native royal palms (Roystonea elata (Bartr.) F Harper)
that remain in southern Florida.
A neotropical leaf beetle (Neolochmaea dilatipennis (Jacoby)), discovered near Mi
ami in 1975, feeds on the Florida "endemic" Borreria terminalis Small (White 1979).
It has also recently wiped out ornamental plantings of the beach creeper, Ernodia lit
toralis Sw (TDC, pers. obs.), a native coastal species listed as of special concern (Craig
1979). A Central American weevil (Eubulus trigonalis Champion), recently discovered
in Dade Co., Florida (pers. comm. J. Pena, University of Florida, Tropical Research
and Education Center, Homestead, FL), probably arrived in non-indigenous cycads
that were imported for the nursery trade. Unfortunately, it attacks native cycads
(Zamia spp., commonly known as coontie) which are also "threatened" species.
An adventive tortoise beetle (Chelymorpha cribraria (F.)) was discovered in Flor
ida in 1993 which feeds on native morning glories (Duquesnel 1994). The little fire ant
(Wasmannia auropunctata (Roger)) which arrived on Santa Cruz Island in the Gal
apagos where it displaced several native ant species including two endemicss" (Hll-
dobler & Wilson 1990), also occurs in southern Florida. It is apparently adventive
throughout both Old and New World tropics (Creighton 1950). The red imported fire
ant (Solenopsis invicta Buren) displaced the native fire ant (S. geminata (F.)) in Texas,
perhaps inducing a restructuring of the entire arthropod community (Porter et al.
1988). This species has been naturalized in Florida for some time now. Many more "bi
logical pollutants" have been discussed in several recent publications (McKnight
1993, Van Driesche 1994, U.S. Congress 1993).
BIOLOGICAL CONTROL AS A POSSIBLE SOLUTION
Traditional control methods (pesticides, etc.) are useful against these invasive spe
cies when they occur at an incipient stage. In these cases, the aim is generally towards
eradication. Eradication is most likely when the introduced species is already known
to be noxious, it is found early, and funds are readily available for an all out assault.
However, most invaders of natural systems are not recognized as problems until
they've gotten out of hand (this is especially true of insect pests). By then, it's often too
Florida Entomologist 78(1)
late to realistically expect to eradicate or even to contain them using traditional mea
sures. This is due to the inaccessibility of the habitats, the difficulty of detecting un
seen infestations, and the associated expenses involved. The identification of host-
specific natural enemies from within the native range of the target pest, and their
subsequent importation into the pest's adopted range, offers considerable promise as
an additional control measure in the arsenal of natural resource managers. Austra
lians are introducing host-specific plant-feeding insects and phytopathogens to con
trol Mimosa pellita in the Northern Territory (Forno 1992). South Africans have
successfully controlled Sesbania punicea, Acacia longifolia (Andr.) Willd., and Hakea
sericea Schrader in the fynbos using highly specific insects that destroy plant repro
ductive tissues (Dennill & Donnelly 1991, Hoffman & Moran 1991, Kluge & Neser
1991). Populations of Salvinia molesta in Australia, New Guinea, Sri Lanka, India,
Botswana, and Namibia were reduced by 99% within a year after introduction of the
weevil Cyrtobagous salviniae Hustache (Thomas & Room 1986, Room 1990, Room et
al. 1981). Alligatorweed, a notorious mat-forming aquatic species, has been almost to
tally controlled in many areas by a flea beetle (Agasicles hygrophila Selman & Vogt)
and a moth (Vogtia malloiPastrana) (Spencer & Coulson 1976). Waterhyacinth is less
of a problem in many parts of the world, including Florida, due to the introduction of
biological control agents (Center et al. 1990). Prospects for biological control of purple
loosestrife appear promising (Malecki et al. 1993, Hight 1993). All of these biological
control agents are highly host specific and none exploit native plants as development
tal hosts.
How DOES BIOCONTROL WORK?
A common belief is that imported species become problems by being introduced
into a new area without the repressive forces (i.e., natural enemies) that held them in
check in their native habitats (see Ewel 1986). Under this paradigm, biological control
represents a remedial attempt to restore some sort of natural balance. This is an er
roneous perspective. Biological control programs do not strive to duplicate the popu
nation regulatory processes of a pest organism's native environment. When natural
enemies hold a species in check in natural conditions, multiple species, including both
specialists and generalists, are involved. Biological control relies on the introduction
of only a selected few of these species, most often only specialists judged capable of re
pressing the pest population. Obviously, as Ewel (1986) notes (using Kudzu, Pueraria
lobata, as an example), many species are just as invasive in their native range as they
are in adventive areas. The organisms that might otherwise repress these species are
oftentimes themselves controlled by numerous species of natural enemies. However,
when these agents are introduced into new areas for biological control purposes, their
natural enemies are excluded. In theory, at least, higher populations are thereby at
stained in their adopted range thus resulting in better control than in the homeland.
In many cases, biological control agents are sparse in their native range, but be
come abundant when introduced into their host's adventive range. For example, par
asitism and competition prevent the bud-galling wasp Trichilogaster
acaciaelongifoliae Froggatt from becoming highly abundant on its host (Acacia long
folia) in Australia (Neser 1985). Released from these regulators, however, this wasp
became an abundant and effective biocontrol agent in South Africa (Dennill 1985).
This is just one of many examples that could be cited demonstrating that successful
biological control agents are not necessarily effective regulators in their native habi
tats. Of course, obvious effectiveness in their homeland is always a good sign.
March, 1995
Behavioral Ecology Symposium '94: Center et al.
In general, potential biocontrol agents are released into a pest's adventive range
only if the possibility for collateral damage to native species is negligible, as demon
strated through intensive host range trials. However, it may at times be prudent to ac
cept modest levels of collateral damage to native species in order to prevent more
extreme levels of habitat destruction by an immigrant or introduced pest. Australian
government scientists, for example, are introducing plant-feeding insects and phyto
pathogens from Madagascar to control the aforementioned rubber-vine (McFadyen &
Harvey 1991). They released one of the insects, the moth Euclasta whalleyi Popescu
Gorj & Constantinescu, with the knowledge that it would also feed on a related native
vine, Gymnanthera nitida R. Br. They reasoned that the possibility of reducing the
abundance of one native species was a small price to pay for the sake of preserving
many others.
FUTURE CONSIDERATIONS
Environmental problems caused by adventive species in Florida are among the
most severe in the United States (U.S. Congress 1993). Invasive plant species are the
most obvious problem, and are particularly easy to track after they achieve nuisance
proportions. Populations of introduced vertebrates are also relatively easy to follow.
Adventive invertebrates (e.g., insects) are much harder to assess, however. Limited
knowledge of many native invertebrates, together with the sheer volume of species
present in Florida, make monitoring for effects of adventive species a daunting and
expensive proposition. Further, problems with invader species are exacerbated by the
increasing pressure on public lands caused by Florida's rapidly growing human pop
ulation. The Florida Department of Environmental Protection recently assembled a
statewide panel of biologists and ecologists to assess these problems and develop rec
ommendations for remedial actions. These recommendations are still pending. How
ever, a few points are already apparent.
If the source of the problem is the wanton introduction of exotic species for eco
nomic gain, then the ultimate solution is largely dependent on political processes. The
importation of exotic species is economically lucrative, so legislative attempts to reg
ulate this practice are bound to be met by stiff opposition. It is ironic that about the
only activity involving the introduction of exotic species (aside from prohibitions
against use of plants on the federal noxious weed list) that is routinely subjected to in
tense scrutiny is the introduction of biological control agents. Just about anyone can
introduce anything, provided that their intent is not to use that organism for biologi
cal control purposes.
All importations of living organisms should be intensively regulated, but such reg
ulation is unlikely to be implemented in the near term. Inspectors are already unable
to meet APHIS' goal for examining 2% of the plants passing through Miami's ports of
entry, so increased levels of inspections are unlikely. Restricting importations to seeds
might provide some relief, but would be strongly contested. Routine fumigation of all
plant shipments might eliminate invertebrate stowaways, but the costs and logistics
of such a program would be overwhelming. Public education campaigns encouraging
use of native plants and advocating patronage of nurseries providing only native spe
cies have yet to be initiated on any substantive scale. In any event, changing con
sumptive habits of the general populace is a slow process. These realities dictate that
we deal with the symptoms of the problem, rather than the cause.
Biological control would seem to offer the best strategy for dealing with these
symptoms. Concurrently, integrated control methods must be developed and natural
areas must be managed to maintain the integrity and health of native ecosystems. To
Florida Entomologist 78(1)
gether, these offer the best hope for dealing with invasive, adventive species. We has
ten to add that biological control is not a panacea and that legitimate criticisms
should be addressed. The impacts of biological control agents on native species, for ex
ample, have often not been appraised during the screening process. Fortunately, this
is rapidly changing and possible effects of introduced biological control agents on non
economic native species are now routinely considered.
In order for biological control to develop fully as a pest control alternative, safety
must not be compromised. Even one unwise introduction could set all biological con
trol programs back many years, resulting in even greater regulation and slower
progress. This places onerous responsibility on each and every biological control sci
entist. However, the increased demand that we are now experiencing for biological
control agents could easily compromise safety. For example, if increased funds become
available on a competitive basis and are thinly distributed among many laboratories,
the end result might be the creation of many poorly-funded projects. The associated
competition and demand for productivity with inadequate funding could force com
promises that would not favor safety. A wiser approach would be to develop a few,
well-funded projects based at "first-class" facilities so as not to jeopardized objectivity
in the reckless pursuit of research dollars (Drea 1993).
The increased demand for biological controls could also result in pressure to de
velop programs more quickly, thus compromising the care and caution normally em
played. Researchers oftentimes perceive (whether justified or not) the potential loss of
funds if a biological control candidate that has undergone research for several years
must be abandoned. This insecurity could lead to attempts to introduce agents that
might not otherwise be considered. This should not be allowed to happen. Researchers
should have the security of knowing that their budget will not be affected by these de
cisions. This again points to the need for adequate and stable funding. The lure of new
funding tends to make experts out of dilettantes. This could be problematic if novices
begin to introduce biological control agents without following proper protocol (Drea
1993). It might therefore become necessary to develop certification procedures for bi
logical control specialists. Safety still depends on the integrity and honesty of the re
search scientists, even though the release of a biological control agent is dependent
upon review by state and federal agencies.
CONCLUSION
Florida is a major point of entry for non-native species into the United States.
Many become permanent residents in Florida, whether by design or by accident. Fur
their, some demonstrate an unfortunate propensity for invading natural areas. These
invasive adventive species can reduce biodiversity, thereby challenging efforts to con
serve natural areas. Careful, scientific introduction of biological control agents is an
appropriate mitigative strategy. The arguments presented by Howarth (1983) that
biocontrol agents might be part of the problem, rather than part of the solution, are
not convincing (see Lai 1988). More data are needed, though, on unintended effects of
recent introductions. This issue must be resolved in a manner that avoids the cre
ation of crippling, bureaucratic regulatory institutions. We must proceed with the de
velopment of environmentally sound pest management practices to protect the
integrity of both natural and agricultural ecosystems in Florida. Classical biological
control typically represents a solution that has no market profit, so public funding is
required. The recognition of biological control as applied ecology and development of
specialized curricula heavily weighted towards ecology in the training of future bio
logical control specialists would help. Also, research leading to the release of new
March, 1995
Behavioral Ecology Symposium '94: Center et al.
agents should be focused at a few "first-class" facilities and priority projects should be
provided with adequate, long-term public funding.
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Florida Entomologist 78(1)
RESPONSES OF MACRODACTYLUS SPP. (COLEOPTERA:
SCARABAEIDAE) AND OTHER INSECTS TO FOOD
ATTRACTANT IN TLAXCALA AND JALISCO, MEXICO
HUGO CESAR ARREDONDO-BERNAL'3, JUAN CIBRIAN-TOVAR' AND ROGER N. WILLIAMS2
'Centro de Entomologia y Acarologia Colegio de Postgraduados, 56230 Montecillo,
Estado de Mexico
2Department of Entomology Ohio Agricultural Research and Development Center
The Ohio State University 1680 Madison Avenue, Wooster, OH 44691-4096
3Current address: Centro Nacional de Referencia de Control Bioldgico, Apartado
Postal 133, Tecoman, Colima 28130, Mexico
ABSTRACT
The effects of a food attractant [trinary mixture of hexanoic acid, valeric acid and
octyl butyrate (1:1:1)] were evaluated in a trapping trial for scarab beetles in the Mex
ican states of Tlaxcala and Jalisco. This mixture was highly attractive to Macrodac
tylus nigripes Bates in Tlaxcala and M murinus Bates in Jalisco, capturing a mean
of 50.2 and 84 individuals per trap per sampling date, respectively. In addition, all
other insects which were taken at the traps were identified to family and classified by
feeding habits. Only one non-scarabeid species appeared to be attracted to the baited
traps, i.e. Apis mellifera L.; all other insect families averaged less than one individual
per trap.
Key Words: Macrodactylus nigripes, M. murinus, semiochemicals, trapping
RESUME
Se evalu6 el efecto de un atrayente alimentario en la capture de escarabajos en los
estados de Tlaxcala y Jalisco, Mexico. El atrayente fue una mezcla de acido hexan6ico,
acido valerico y octil-butirato (1:1:1). Esta mezcla fue altamente atractiva para la cap
tura Macrodactylus nigripes Bates en Tlaxcala (un promedio de 50.2 individuos por
trampa por muestreo) y para M murinus Bates en Jalisco (un promedio de 84 indivi
duos por trampa por muestreo). Otros insects capturados fueron identificados a nivel
de familiar y clasificados de acuerdo a sus habitos alimentarios; el efecto del atrayente
alimentario sobre estas poblaciones fue selective.
There are at least 28 known species in the genus Macrodactylus, all from the Ne
arctic region. The 20 species of Macrodactylus from Mexico are known as "frailecillos,"
teaches, or "burros" and feed on a wide variety of cultivated and wild plants (Moron
& Terr6n 1988). The larvae (grubs) are strictly root feeders. However, the adult stage
causes damage to leaves, flower buds and fruits of many cultivated plants (Moron &
Terr6n 1988; Williams et al. 1990).
In Huamantla, Tlaxcala, and Manantlan, Jalisco, the adults of Macrodactylus ni
gripes Bates and M. murinus Bates are important pests of maize (Altieri & Trujillo
1987). The adults emerge after the first rains and appear to be synchronized with the
This article is from Florida Entomologist Online, Vol. 78, No. 1 (1995).
FEO is available from the Florida Center for Library Automation gopher (sally.fcla.ufl.edu)
and is identical to Florida Entomologist (An International Journal for the Americas).
FEO is prepared by E. O. Painter Printing Co., P.O. Box 877, DeLeon Springs, FL. 32130.
March, 1995
Arredondo-B. et al: Macrodactylus spp. Respond to Lure 57
development of the maize crop. Macrodactylus spp. consume the pollen in the tassels,
thereby reducing pollination. When the infestation is heavy, the beetles also consume
the silks (styles), preventing pollination, and thus prohibiting the formation of grain.
Insecticides have been widely utilized against this group of insects in Mexico. How
ever, in the Manantlan Biosphere Reserve where pesticides are prohibited, we are
searching for an alternate means for control which would be sustainable and environ
mentally sound.
Many studies have been carried out to determine efficacy of food attractants, e.g.,
for Japanese beetle, Popilliajaponica Newman (Fleming 1969). For Macrodactylus,
the first report of luring adult beetles to feeding attractants was mentioned by
Johnson (1940), who collected Macrodactylus species at baits designed for Japanese
beetles. In 1982, Williams & Miller determined that various aromatic compounds
were attractive to adults of Macrodactylus subspinosus (F.) in Ohio and that hexanoic
acid and valeric acid were the best attractants. Later Williams et al. (1990) conducted
a study in which they evaluated more than 60 compounds with the objective of finding
the best attractant for monitoring populations of M subspinosus. The results of these
studies showed that the mixture of valeric acid, hexanoic acid, and octyl butyrate, in
the ratio of 1:1:1 exhibited the best attraction. In Chapingo, Cibrian et al. (1990) ob
served that this mixture was attractive to M. mexicanus Burmeister and various
other insects. At the same time, they determined that trap color did not influence the
capture of M. mexicanus. The objective of the present study was to determine the ef-
fects of this same food attractant on the capture of M nigripes, M murinus, and other
insect taxa in Huamantla, Tlaxcala, and Manantlan, Jalisco.
MATERIALS AND METHODS
The attraction of the test mixture on M. nigripes in Huamantla, Tlaxcala, was de
termined with 48 Yellow Super Traps (Reuter Laboratories, Manassas VA) placed in
a field of maize known to be infested during the previous seasons. The traps were
evenly distributed in an area of the field 0.5 ha in size. The objective was to measure
the total capture of "frailecillos" per week. The first captures were based on collections
of 16 traps.
At the second location, Manantlan, Jalisco, 36 traps were utilized to determine
numbers of Macrodactylus murinus caught each fortnight. Traps were distributed
uniformly in a maize field which was 0.375 ha in area. At the time the traps were set,
the maize was in early florescence.
The traps were hung from galvanized pipes at approximately 1 m above the soil
surface. A plastic bag attached to the bottom of each trap served as a receptacle to col
lect the beetles. Each bag was perforated with tiny holes near the bottom to avoid wa
ter accumulation during the rainy season, thus partially avoiding biological
decomposition in the bags. Five ml of the volatile mixture of valeric acid, hexanoic
acid and octyl butyrate were deposited in small green containers (Loral Poly-Cons) de
scribed in Klein & Edwards (1989). These containers were placed in the traps with
their openings downward in order to avoid dilution of the attractant by rain or decom
position by direct sunlight.
At the same time, the effect of the trap density (4 or 8 = 64 or 128 per ha) on the
capture of M. nigripes was determined in 1/16 ha plots in Huamantla, Tlaxcala. Each
treatment was replicated four times using randomized blocks. With these parame
ters, we were able to measure the number of insects captured per trap. Means were
compared by t test.
Florida Entomologist 78(1)
The effect of these attractants on other groups of insects was determined in Tlax
cala by recording the number of captures per trap per week. In Jalisco, the captures
were recorded fortnightly. The identification of the majority of insects was made to
family and, in some cases, to species.
RESULTS AND DISCUSSION
In Huamantla, Tlaxcala, 5,832 M. nigripes were collected in 48 traps over a 10
week period. Based on trap captures, the maximum adult response at this location
was from July 4 to July 15 (2,295 beetles). Collections decreased after that until the
end of the season. However, there was an irregular pattern the week of July 30 -Au
gust 6, which was lower than the two adjacent weeks. After September 10, no more
beetles were caught (Fig. 1). The differences in the numbers of specimens captured in
the week of August 6 13 perhaps was due to a dry period followed by rain which stim
ulated adult emergence. In some parts of Mexico, adults are active for approximately
a four-month period. In Chapingo, Mexico, studies conducted by Cibrian et al. (1990)
showed that the capture of M. mexicanus is similar to that of M. nigripes in Hua
mantla, Tlaxcala.
In Manantlan, Jalisco, where 36 traps were set, the capture of M murinus over the
entire collecting period was 12,102 beetles. The maximum capture was between Sep
tember 18 and October 2, with 10,613 beetles captured for the period. During the next
fortnight, collections decreased by 93% to only 470 beetles. After October 30, no M
murinus adults were collected, indicating the end of the adult activity period (Fig. 2).
An average of 50 specimens of M nigripes were captured per trap over the entire
experiment, while 84 M. murinus were captured per trap. These figures are low com
3000
2700
2400
2100
1800
1500
1200
900
600
300
1124
901
375
28 10
JUL JUL JUL JUL
AUG AUG
WEEKS
20-27 27-03 03-10
AUG SEP SEP
FIG. 1
Fig. 1. Trapping of Macrodactylus nigripes Bates with a food attractant in 48 yel
low traps, Huamantla, Tlaxcala, Mexico, 1990.
March, 1995
Arredondo-B. et al: Macrodactylus spp. Respond to Lure 59
0 / 10613
12000
I-
< 10000
.I 8000
I-
w
m 6000
L,
0
c 4000
a 740 749
3 2000 0
z
0 0
0
H- 18-02 02-16 16-30 30-15
SEP OCT OCT NOV
FIG. 2
Fig. 2. Capture of Macrodactylus murinus Bates with a food lure in 36 yellow
traps, Manantlan, Jalisco, Mexico, 1990. (Fortnightly)
pared to those reported by Williams et al. (1990) with the same attractant in Ohio
where 125 M. subspinosus were captured per trap. Of course, these collections can not
be directly compared but are mentioned here as a reference to the abundance of Mac
rodactylus spp. when present. Here, we are dealing with different species, thus trap
catches may reflect the degree of efficacy in response to attractant rather than popu
lation density.
Because maize was the major host being considered in this study, it would seem
that Macrodactylus spp. may have built up to higher numbers due to the extended
flowering period in which the maize plant is vulnerable. The flowering period of maize
is locally extensive because the maize is planted over an elevation gradient of more
than 500 m and the maize flowers at different times, depending upon the elevation.
Having studied the collection and behavior of the populations, it was determined
that the use of feeding attractants is a viable option for monitoring Macrodactylus
adult activity. However, when the traps and attractants are used experimentally, it is
necessary to correlate the number of insects captured with the density required to
cause damage (economic threshold). This information might aid in a better under
standing of the degree of protection offered by trapping the beetles.
The capture of beetles using two different trap densities was compared on popular
tions of M. nigripes in parcels of 1/16 ha. It was determined that the higher density of
traps captured significantly (t = 3.77, P = 0.05) greater numbers of beetles. Fig. 3
shows the differences in the numbers of beetles which were captured on different
dates of the experiment. Effects of trap densities were observed on local populations
of Macrodactylus spp. where correlated studies were conducted with differing num
bers of traps, insects captured and numbers of these insects.
The results indicate that the food lure in these trials could be used for behavioral
studies of the two species of Macrodactylus.
60 Florida Entomologist 78(1) March, 1995
S800 667 4 TRAPS
mE 800 I_
S567
C0 700
6 8 TRAPS
U o 600 425
-J
S500
w 293
LU 271 293
m 400 -
LL
O 300
M 100
m 200 25 8
z 100
-J
S 0
O 16-23 23-30 30-06 06-13 13-20 20-27 27-03 03-10
JUL JUL JUL AUG AUG AUG SEP SEP
WEEKS
FIG. 3
Fig. 3. Response of Macrodactylus nigripes Bates to a food attractant using trap
densities of 4 and 8 traps in 1/16 ha, Huamantla, Tlaxcala, Mexico, 1990.
Specimens of other insect groups trapped include a variety of families with diverse
feeding habits. Interestingly, the phytophagous insect caught in greatest quantities
was another scarab, "mayate de la calabaza," Euphoria basalis Burmeister. An aver
age of 0.38 E. basalis beetles were collected per week per trap. Cibrian et al. (1990)
captured similar numbers of E. basalis in Chapingo. Other phytophagous families col
elected in descending order included Mordellidae, Elateridae, Meloidae, Scarabaeidae
(other than Macrodactylus and Euphoria), Curculionidae, Noctuidae, Nitidulidae,
Chrysomelidae, Miridae, Tenebrionidae, Pentatomidae, Lygaeidae, Anthicidae, Cer
ambycidae, Tephritidae, Cicadellidae, and Coreidae.
Of the insect predators captured, Cleridae were caught in the greatest numbers
(0.96 beetles per trap per week). Insects from other predaceous families were cap
tured less frequently (less than 0.107 beetles per trap per week). The major families
collected were: Thomisidae, Histeridae, Coccinellidae, Staphylinidae, Carabidae,
Lampyridae, Asilidae, Malachiidae, Sphecidae, and Nabidae. Of the pollinating in
sects, Apis mellifera L. was the species which was captured in greatest numbers; the
average collected per trap each week was 1.69. Other species of the families Antho
phoridae, Colletidae, Megachilidae, Andrenidae and other Apidae were captured less
frequently.
Parasitoids were trapped in lesser numbers. Thiphiidae, Ichneumonidae, and Bra
conidae were all trapped in very small quantities (less than 0.0158 per trap).
Fewer insects were captured in Manantlan, Jalisco, and the trapping was limited
to phytophagous, pollinating and predaceous insects. The collections in this zone were
generally less than 0.25 insects per trap per fortnight. Of the phytophagous insects
captured, E. basalis was the most abundant in Manantlan, as well as in Huamantla.
Perhaps one of the reasons why insects were captured less frequently than in Hua
mantla, is that the traps were set out in autumn when populations M. murinus were
Arredondo-B. et al: Macrodactylus spp. Respond to Lure 61
more abundant than populations of the other insects, thus the total number of organ
isms decreased.
In general, the effect of the attractants on other insect groups was low indicating
that the attractant mixture demonstrated a selectivity in the capture of scarabs, Mac
rodactylus in particular. The most captured insect, other than Macrodactylus, was
Apis mellifera; however, they did not surpass 2 insects per trap per week.
ACKNOWLEDGMENTS
Many thanks to Ing. Tonathiu Noyola, Head of the Plant Protection Program of the
Secretary of Agriculture and Hydraulic Resources, and the Natural Laboratory, Las
Joyas in Jalisco, and to Dr. Bruce Benz for his invaluable collaboration making this
investigation possible. Manuscript number 82-94.
REFERENCES CITED
ALTEIRI, M. A., AND J. TRUJILLO. 1987. The agroecology of corn production in Tlaxcala,
Mexico. Hum. Ecol. 15:189-220.
CARRILLO-S., J. L. 1959. Estudios taxon6micos sobre las species mexicanas del g6-
nero de Macrodactylus Latr. y observaciones biol6gicas de algunas species. Te
sis Profesional. Escuela Nacional de Agricultura, Chapingo, Mexico.
CIBRIAN-T., J., H. ARREDONDO-BERNAL, AND R. N. WILLIAMS. 1990. Evaluaci6n de un
atrayente alimenticio para la capture de Macrodactylus spp., pp:27-28 en: C. B.
Landeral, R. Dominguez y J. Sanchez E. [eds.]. Avances de la Investigaci6n
1990. CENA. Colegio de Postgraduados, Montecillo, Mexico.
FLEMING, W. E. 1969. Attractants for the Japanese beetle. USDA. Agric. Tech. Bull.
1399. 87 p.
KLEIN, M. G., AND D. C. EDWARDS. 1989. Captures of Popillialewisi (Coleoptera: Scar
abaeidae) and other scarabs on Okinawa with Japanese beetle lures. J. Econ.
Entomol. 82(1): 101-103.
JOHNSON, J. P. 1940. Results of trapping rose chafers. Conn. Agric. Exp. Stn. Bull.
(New Haven) 434:314.
MORON, M. A., AND R. A. TERRON. 1988. Entomologia practice. Institute de Ecologia,
A.C. Mexico. pp. 210-243.
WILLIAMS, R. N., AND K. V. MILLER. 1982. Field assay to determine attractiveness of
various aromatic compounds to rose chafer adults. J. Econ. Entomol. 75:196
198.
WILLIAMS, R. N., T. P. MCGOVERN, M. G. KLEIN, AND D. S. FICKLE. 1990. Rose chafer
(Coleoptera: Scarabaeidae): improved attractants for adults. J. Econ. Entomol.
83:111-116.
Florida Entomologist 78(1)
PROTEIN FEEDING ATTENUATES ATTRACTION OF
MEXICAN FRUIT FLIES (DIPTERA: TEPHRITIDAE) TO
VOLATILE BACTERIAL METABOLITES
DAVID C. ROBACKER AND DANIEL S. MORENO
Crop Quality & Fruit Insects Research, Agricultural Research Service,
U. S. Department of Agriculture, 2301 S. International Blvd.
Weslaco, TX 78596
ABSTRACT
We tested the hypothesis that Mexican fruit flies [Anastrepha ludens (Loew)] are
attracted to odor of tryptic soy broth cultures of Staphylococcus aureus (Rosenbach)
because they are hungry for protein. First, we demonstrated that attraction to the
odor was attenuated by feeding on a relatively complete diet containing sugar, pro
tein, fats, vitamins, and minerals compared to feeding on sugar only; second, we
showed that feeding on a diet of casein hydrolysate and sugar in which the percentage
of protein was equal to that in the complete diet attenuated attraction to the same de
gree as the complete diet; and third, we showed that attraction to bacterial odor de
creased as percentage of protein increased in a diet containing casein hydrolysate and
sugar. Results of the three experiments support the hypothesis that flies are attracted
to odor of S. aureus cultures largely to find protein. Dietary vitamins, minerals, fats,
and percentage of protein as amino acids had no effect.
Key Words: Anastrepha ludens, kairomones, bacteria, specific-hunger
RESUME
Se puso a prueba la hip6tesis de que la mosca Mexicana de la fruta [Anastrepha lu
dens (Loew)] es atraida por el olor de cultivos en caldo de soya de la bacteria Staphylo
coccus aureus por estar avida de protein. Primeramente, se comprob6 que la
atracci6n de las moscas hacia el olor fue mas tenue cuando estas se alimentaron de
una dieta relativamente complete (azfcar, protein, aceite, vitamins y minerales)
que cuando se alimentaron de una dieta que contenia solamente azfcar; en segundo
lugar, se comprob6 que alimentandose de una dieta que contenia caseina hidrolizada
y azucar (cantidad de protein equivalent a la dieta relativamente complete) la res
puesta de las moscas fue tenue y del mismo grado que cuando se alimentaron de la
dieta relativamente complete; en tercer lugar, se comprob6 que la atracci6n de las
moscas hacia el olor de la bacteria disminuyd con el incremento de caseina hidrolizada
en la dieta. Los resultados de los tres experiments apoyan la hip6tesis de que las
moscas son atraidas por el olor de los cultivos de S. aureus porque estas buscan pro
teina para alimentarse. Los compuestos nutritivos de vitamins, minerales, aceites,
y porcentaje de protein, en forma de amino acidos, no afectaron las respuestas.
Odors produced by numerous species of bacteria have now been shown to be at
tractive to adults of various species of Tephritidae (Drew et al. 1983, Courtice & Drew
1984, Drew & Lloyd 1989, Jang & Nishijima 1990, MacCollom et al. 1992). The Mex
ican fruit fly [Anastrepha ludens (Loew)] is strongly attracted to odors produced dur
ing fermentation of culturing media by bacteria from at least four families (Robacker
et al. 1991, Martinez et al. 1994). Robacker et al. (1993) later presented evidence that
the attractive chemicals, hereafter referred to as bacterial odor, are probably volatile
metabolites of the bacterial fermentation process.
This article is from Florida Entomologist Online, Vol. 78, No. 1 (1995).
FEO is available from the Florida Center for Library Automation gopher (sally.fcla.ufl.edu)
and is identical to Florida Entomologist (An International Journal for the Americas).
FEO is prepared by E. O. Painter Printing Co., P.O. Box 877, DeLeon Springs, FL. 32130.
March, 1995
Robacker & Moreno: Attraction ofA. ludens to Bacteria 63
The reason for the attractiveness of bacterial odor has been studied in recent work
with the Mexican fruit fly but remains unresolved. Robacker (1991) showed that flies
fed yeast hydrolysate and sugar were much less responsive to odor of cultures of the
bacterium Staphylococcus aureus (Rosenbach) than flies fed only sugar and concluded
that bacterial odor attracted flies hungry for protein, which is present in yeast hy
drolysate. However, Robacker & Garcia (1993) later found that flies fed yeast hydroly
sate up until the time of bioassays nevertheless were strongly attracted to bacterial
odor. They also showed that sugar deprivation greatly depressed attraction of flies to
the odor. This raised the question of whether decreased attraction to bacterial odor in
tests where flies had been fed yeast hydrolysate may have been at least partly due to
insufficient sugar in the yeast hydrolysate/sugar diets. The role of protein hunger in
attraction to bacterial odor was again open for debate. During scrutiny of earlier data,
another point of uncertainty came up regarding the composition of yeast hydrolysate
itself. As yeast hydrolysate contains fats, vitamins and minerals in addition to pro
tein, we now had to ask if the effects of feeding flies yeast hydrolysate on reducing at
traction to bacterial odor may have been due to some nutrient or nutrients other than
protein. This seemed like a strong possibility in light of recent work showing that two
species of predatory mites fed a diet deficient in carotenoid vitamins were attracted to
kairomones produced by prey that contain the carotenoids, while the same two mite
species fed diets containing carotenoids did not respond to those kairomones (Dicke et
al. 1986, Dicke 1988).
The purpose of this work was to determine how feeding by adult Mexican fruit flies
on diets containing various nutrients affected attraction of the flies to bacterial odor
produced by action of S. aureus strain RGM-1 (Robacker et al. 1991) on tryptic soy
broth media. This was done in three experiments. First, a comparison was made of at
traction of flies fed a diet containing a relatively complete mixture of nutrients vs only
sugar to verify that some nutrient or nutrients in the complete diet would in fact at
tenuate responses of the flies to the bacterial odor. Next, a comparison was made of at
traction of flies fed the complete diet vs a diet containing an equal amount of protein,
but no other nutrients (except sucrose), to determine the role of nutrients other than
protein. Finally, we tested for effects of diets containing various percentages of protein
and sugar and no other nutrients.
MATERIALS AND METHODS
Flies were from a colony maintained for approximately 400 generations with no
wild-fly introductions. Mixed-sex groups of 180-200 flies were held in bioassay cages
from eclosion with water and various test diets that will be described below. To ensure
that flies would not respond strongly to water in both the treatments and the controls,
water was provided to them in a light spray during the morning at least one h before
bioassays began. Laboratory conditions, both for holding flies and conducting experi
ments, were 22 + 2'C (range), 55 + 15% RH (range) and a photoperiod of 13:11 (L:D).
Laboratory lighting was a combination of fluorescent and natural light through glass
windows.
The bacterial attractant was produced by fermentation of the bacterial strain
RGM 1 previously identified as a probable new strain of S. aureus from the mouth
parts of a female laboratory-strain Mexican fruit fly (Robacker et al. 1991). While this
bacterium probably was introduced into the fruit fly culture from human contact, its
cultures are nevertheless very attractive to adult Mexican fruit flies.
RGM 1 was cultured in tryptic soy broth (DIFCO Laboratories, Detroit, MI) in a
shaker for 144 h at 30'C. Bacterial culture was centrifuged at 10,000 rpm for 20 min.
Florida Entomologist 78(1)
The resulting supernatant contained highly attractive material that was used as the
attractant source in this research. Previous research had demonstrated that the at
tractive material in the supernatant was neither bacterial cells nor the tryptic soy
broth itself (Robacker et al. 1993). Rather, the attractiveness probably was due to
odorant chemicals produced by the bacteria during metabolism of nutrients in the
tryptic soy broth.
Bioassays were conducted in 0.3 x 0.3 x 0.3 m, aluminum framed,
aluminum screened cages. Cage-top bioassays (Robacker et al. 1991) were used in all
experiments because this system has provided rapid, quantitative evaluation of at
tractants ranging from slightly to very attractive. Briefly, the bioassay consisted of
placing two filter paper triangles (three cm per side) containing 10 pl of supernatant
of bacterial culture and two papers containing 10 pl of water, each on one corner on
the top of a bioassay cage, and counting the flies beneath the papers 10 times at one
minute intervals. Filter papers were raised 0.5 cm above the cage top to ensure that
olfaction was solely responsible for attraction of the flies to the filter papers. Bioas
says were conducted using 7 to 11 day-old flies. Flies were used for one bioassay, then
discarded.
Three experiments were conducted. The purpose of Experiment 1 was to test the
hypothesis that flies fed a diet presumed to be more or less nutritionally complete
would be less responsive to bacterial odor than flies fed sugar only, as was suggested
by results of earlier research (Robacker 1991, Robacker & Garcia 1993). In Experi
ment 1, two diet types were tested. Ten cages of flies were set up with sugar and water
only. Sugar was provided as four sucrose "dainty cubes"" (Imperial Sugar Co., Sugar
land, TX) placed in petri dishes inside the cages. Water was provided in a plastic vial
with a cotton wick inside cages. A second ten cages were prepared with water and a
relatively "complete" diet. Water was provided in plastic vials as above and the com
plete diet was provided in a plastic petri dish. The complete diet was a dry powder
mixture containing 20% enzymatic yeast hydrolysate, 20% torula dried yeast, 4%
casein, 2% Vanderzant's vitamin fortification mixture for insects, 0.05% cholesterol,
52.35% sucrose (all obtained from U.S. Biochemical Corp., Cleveland, OH), and 1.6%
Beck's salts (BIO-SERV, Inc., Frenchtown, NJ). Both enzymatic yeast hydrolysate
and torula dried yeast contained about 50% protein while casein was about 97% pro
tein, according to the manufacturers. Thus the total protein in the complete diet was
about 24%. Free amino acids were less than 10% of the diet. The other 50% of yeast
hydrolysate and torula dried yeast consisted of unspecified carbohydrates, ash, water,
and fiber according to information provided by U.S. Biochemical Corp., and probably
small percentages of fats, minerals, and vitamins (Long 1961). Finally, additional su
crose was provided as two sugar cubes (Imperial Sugar Co.) located in the petri dish
with the complete diet. The reason for additional sugar was to allow flies to
"self select" the amounts of sugar and protein in their diet (Waldbauer & Friedman
1991). Flies were fed these diets from eclosion and diets were not removed from cages
when bioassays were conducted. Experimental procedure was to test two cages, one
each of the two diet types, side by side (one m apart) at the same time. Five cages of
each diet type were set up and tested as one set. The experiment was repeated with a
second set of five cages of each diet set up and tested two weeks later.
Experiment 2 was conducted to determine if nutrients other than protein affect at
traction of the flies to bacterial odor. Cages of flies were again set up with one of two
diet types. Twenty cages were prepared with the complete diet, two additional sugar
cubes and water vials as in Experiment 1. Another 20 cages were prepared with a
casein hydrolysate and sugar diet, two additional sugar cubes and water vials. The
casein hydrolysate diet was a dry powder mixture containing 27.4% vitamin and
March, 1995
Robacker & Moreno: Attraction ofA. ludens to Bacteria 65
salt-free casein hydrolysate (ICN Biomedicals, Inc., Irvine, CA) and 72.6% sucrose
(U.S. Biochemical Corp.). The casein hydrolysate was about 87.5% protein with little
or no other nutrients, according to information provided by ICN Biomedicals. The to
tal protein in the diet was 24%, the same as in the complete diet. Free amino acids
were about 18.5% of the diet. Experimental procedure was the same as in Experiment
1. Again, five cages of each diet type were set up and tested as one set. Four sets were
tested at two week intervals. Also, two cages fed only four sugar cubes as in Experi
ment 1 were prepared and tested with each set to verify that low attraction of flies fed
the two test diets was not due to fly batch.
Experiment 3 was conducted to determine the relationship between percentage of
protein in the diet and attraction of the flies to bacterial odor. Each replication of the
experiment consisted of eight cages set up with dry powder diets containing 0, 1, 2, 4,
8, 16, 32, or 64% protein. Casein hydrolysate (ICN Biomedicals, Inc.) was the protein
source. Sucrose (U.S. Biochemical Corp.) made up the remainder of the diets. No ad
ditional sugar cubes were provided. Water was again provided in plastic vials. Exper
mental procedure was to set up the eight cages as described above using flies from the
same batch and to test them within two h on the same day. The experiment was re
peated eight times, each about two weeks apart.
Experiments 1 & 2 were analyzed by paired t tests of cages paired by test time
(Snedecor & Cochran 1967). Data used in these ttests were differences between total
counts at bacterial odor and water from each bioassay. Experiment 3 was subjected to
2-way analysis of variance of differences between counts at bacterial odor and water,
separating out effects of test day and percentage of protein (Snedecor &Cochran
1967). Effect of percentage of protein was partitioned into linear regression of attrac
tion on percentage of protein on the log, scale. Paired ttests were also used to compare
counts at bacterial odor to counts at water in some cases. Although count differences
were used for statistical analyses, means and standard errors (SE) shown in figures
were calculated using response ratios from individual bioassays because these were
more appropriate for presentation. The response ratio from an individual bioassay
was defined as the ratio of the total count at bacterial odor in that bioassay to the
mean of total counts at all water-controls in the experiment that included that bioas
say
RESULTS AND DISCUSSION
The results of Experiment 1 are shown in Fig. 1. Flies fed the complete diet were
much less responsive to bacterial odor than were flies fed sugar only (t= 10.4, df = 9,
P< 0.001). We interpret this to mean that flies fed only sugar were strongly attracted
to bacterial odor because they associate bacterial odor with the presence of certain re
quired nutrients that were deficient in the sugar diet. Conversely, flies that fed on the
complete diet were not as strongly attracted to bacterial odor because the complete
diet partially satisfied their hunger for whatever nutrients they associate with bacte
rial odor.
Despite lower attraction of flies fed the complete diet compared to flies fed sugar
only (Fig. 1), bacterial odor was significantly more attractive than water controls for
flies fed the complete diet (t= 8.5, df = 9, P< 0.001). Three possible explanations for
this result are: 1) not all of the flies' nutritional needs were met by the complete diet
compared to what they associate with bacterial odor; 2) the complete diet has every
thing they need but the attraction response to bacterial odor does not turn off com-
pletely unless hunger of flies is completely satiated, a state that may occur only when
their crops are completely full; and/or 3) the bacterial odor contains one or more at
tractive chemicals that are not associated with the hunger response.
Florida Entomologist 78(1)
16
O 14
o 2
0 12-
0
0W 6
4
SUGAR COMPLETE DIET
DIET FED TO FLIES
Fig. 1. Attraction to bacterial odor (+ SE) of Mexican fruit flies fed sugar or a com-
plete diet containing a balance of required nutrients. Bars are response ratios of at
traction to bacterial odor relative to attraction to water controls. Attraction of flies fed
the two diets was significantly different by a paired ttest (P< 0.001, df = 9).
There was no difference in attraction of flies fed the complete diet or the casein hy
drolysate/sugar diet (t= 1.4, df = 19, P= 0.2) (Fig. 2). Note that the two diets were
equal in percentage of protein but differed in every other nutrient. For example, the
casein hydrolysate diet contained almost no nutrients other than protein and sugar
while the complete diet contained protein, sugar, vitamins, minerals, fats, etc. Fur
their, the casein hydrolysate diet contained nearly twice as much of its protein as
amino acids as did the complete diet. Indications are that the equal percentage of pro
tein in the two diets was the primary factor determining equal attraction to the bac
trial odor. This suggests that flies are attracted to bacterial odor largely because they
associate it with the presence of protein.
As in Experiment 1, attraction to bacterial odor of flies fed diets containing protein
in Experiment 2 was considerably lower than attraction of flies that were fed sugar
only (Fig. 2). Also as in Experiment 1, attraction to bacterial odor nevertheless was
March, 1995
Robacker & Moreno: Attraction ofA. ludens to Bacteria
0 T 12-
0 10
SUGAR COMPLETE DIET CASEIN/SUGAR
8
0
6
co 4
SUGAR COMPLETE DIET CASEIN/SUGAR
DIET FED TO FLIES
Fig. 2. Attraction to bacterial odor (+ SE) of Mexican fruit flies fed sugar, a com-
plete diet containing a balance of required nutrients, or a diet containing casein hy
drolysate and sugar in which the percentage of protein was the same as that of the
complete diet. Bars are response ratios of attraction to bacterial odor relative to at
traction to water controls. Attraction of flies fed the complete diet and the casein hy
drolysate diet was not significantly different by a paired ttest (P= 0.2, df = 19).
significantly greater than attraction to water controls for flies fed the two
protein containing diets (complete diet: t 8.6, df = 19, P< 0.001; casein hydrolysate/
sugar diet: t 8.5, df= 19, P< 0.001).
In Experiment 3, attraction of flies to bacterial odor was affected by diet fed to the
flies (F = 44.2; df = 6,42; p < 0.001). Attraction decreased nearly linearly with the log,
of the percentage of protein (r2 0.55, P< 0.001) (Fig. 3). Data for 64% protein were
not included in Fig. 3 or in the analysis of variance because over 60% of the flies in the
cages were dead by the test day, and most of the remaining flies appeared weak. The
actual response ratio for the 64% protein diet was 0.6 indicating that fewer flies came
to the bacterial odor than to water.
The results of Experiment 3 can be interpreted two ways. One explanation is that
attraction of flies to bacterial odor decreased as percentage of protein in the diet in
creased because protein hunger decreased. This explanation corroborates our conclu
sion from Experiment 2 that flies are attracted to bacterial odor because they
associate it with the presence of protein. However, the percentage of sugar in the diets
decreased as the percentage of protein increased so the possibility that diminishing
response by the flies may be due to increasing sugar hunger must be considered. This
Florida Entomologist 78(1)
10
8
oa
-
0 4-
(0
LL 2
0
0 1 2 4 8 16 32
% PROTEIN IN DIET FED TO FLIES
Fig. 3. Attraction to bacterial odor (+ SE) of Mexican fruit flies fed diets containing
sugar and various percentages of casein hydrolysate protein. Bars are response ratios
of attraction to bacterial odor relative to attraction to water controls. Attraction of
flies decreased nearly linearly with the log, of percentage of protein (r = 0.55, P <
0.001).
explanation is plausible because Robacker & Garcia (1993) showed that sugar hunger
greatly depresses attraction of Mexican fruit flies to bacterial odor.
We believe the explanation for the results of Experiment 3 is that the decrease in
attraction was due to a decrease in protein hunger rather than an increase in sugar
hunger. There are several reasons for this contention. First, the diets depicted in Fig.
3 all contained at least 68% sugar. This percentage is well above the percentage of
sugar (52.35%) in the complete diet that was found to optimize Mexican fruit fly fe
cundity and longevity (D.S.M. unpublished data). Second, most of the effect was man
ifest before the percentage of sugar in diets had dropped below 92%, a decrease in
relative percentage of sugar of only 8% from the 100% sugar diet. At the same time,
protein percentage increased from 0 to 8%, a large increase in relative percentage of
protein. Thus, the change in sugar percentage probably was insignificant compared to
the change in protein. Finally, the results of Experiment 2 in which attraction to bac
trial odor were unaffected by a decrease in sugar percentage from 72.6% in the casein
hydrolysate/sugar diet to 52.35% in the complete diet suggest that sugar percentage
is unimportant as long as it is higher than some undetermined threshold level.
We conclude that attraction of Mexican fruit flies to odor of tryptic soy broth cul
tures of S. aureus strain RGM 1 is primarily due to hunger for protein. Presence or ab
sence of fats, vitamins, and minerals seems unimportant. We suggest this is a
March, 1995
Robacker & Moreno: Attraction ofA. ludens to Bacteria 69
specific hunger" (Dethier 1976) for protein that translates into appetitive search for
protein food sources due to an innate neural association of bacterial odor with the
presence of protein. Possibly, attraction of fruit flies to bacteria generally may be gov
erned by protein-hunger, based on the work of Drew & Lloyd (1989) that implicated
bacteria as a natural protein source for fruit flies.
ENDNOTE
We thank Jose Garcia and Maura Rodriguez for technical assistance and Sammy
Ingle for insects. Mention of a proprietary product does not constitute an endorsement
or recommendation for its use by the USDA.
REFERENCES CITED
COURTICE, A. C., AND R. A. I. DREW. 1984. Bacterial regulation of abundance in trop
ical fruit flies (Diptera: Tephritidae). Australian Zool. 21: 251 268.
DETHIER, V. G. 1976. The Hungry Fly. Harvard University Press, Cambridge, Massa
chusetts.
DICKE, M., M. W SABELIS, AND A. GROENEVELD. 1986. Vitamin A deficiency modifies
response of predatory mite Amblyseius potentillae to volatile kairomone of
two-spotted spider mite, Tetranychus urticae. J. Chem. Ecol. 12: 1389-1396.
DICKE, M. 1988. Prey preference of the phytoseiid mite Typhlodromus pyri 1. Re
sponse to volatile kairomones. Exp. Appl. Acarol. 4: 1-13.
DREW, R. A. I., A. C. COURTICE, AND D. S. TEAKLE. 1983. Bacteria as a natural source
of food for adult fruit flies (Diptera: Tephritidae). Oecologia. 60: 279-284.
DREW, R. A. I., AND A. C. LLOYD. 1989. Bacteria associated with fruit flies and their
host plants, pp. 131-140 in A. S. Robinson and G. Hooper [eds.], Fruit Flies:
Their Biology, Natural Enemies and Control. Vol. 3A. Elsevier, Amsterdam.
JANG, E. B., AND K. A. NISHIJIMA. 1990. Identification and attractancy of bacteria as
sociated with Dacus dorsalis (Diptera: Tephritidae). Environ. Entomol. 19:
1726-1731.
LONG, C. 1961. Biochemists' Handbook. Van Nostrand, Princeton, New Jersey.
MACCOLLOM, G. B., C. R. LAUZON, R. W WEIRES, JR., AND A. A. RUTKOWSKI. 1992. At
traction of adult apple maggot (Diptera: Tephritidae) to microbial isolates. J.
Econ. Entomol. 85: 83-87.
MARTINEZ, A. J., D. C. ROBACKER, J. A. GARCIA, AND K. L. ESAU. 1994. Laboratory and
field olfactory attraction of the Mexican fruit fly (Diptera: Tephritidae) to me
tabolites of bacterial species. Florida Entomol. 77: 117-126.
ROBACKER, D. C. 1991. Specific hunger in Anastrepha ludens (Diptera: Tephritidae):
Effects on attractiveness of proteinaceous and fruit-derived lures. Environ. En
tomol. 20: 1680-1686.
ROBACKER, D. C., J. A. GARCIA, A. J. MARTINEZ, AND M. G. KAUFMAN. 1991. Strain of
Staphylococcus attractive to laboratory strain Anastrepha ludens (Diptera: Te
phritidae). Ann. Entomol. Soc. America. 84: 555-559.
ROBACKER D. C. AND J. A. GARCIA. 1993. Effects of age, time of day, feeding history,
and gamma irradiation on attraction of Mexican fruit flies (Diptera: Tephriti
dae), to bacterial odor in laboratory experiments. Environ. Entomol. 22:
1367-1374.
ROBACKER D. C., W C. WARFIELD, AND R. F ALBACH. 1993. Partial characterization
and HPLC isolation of bacteria-produced attractants for the Mexican fruit fly,
Anastrepha ludens. J. Chem. Ecol. 19: 543-557.
SNEDECOR, G. W, AND W G. COCHRAN. 1967. Statistical Methods. The Iowa State
University Press, Ames, Iowa.
WALDBAUER, G. P., AND S. FRIEDMAN. 1991. Self selection of optimal diets by insects.
Annu. Rev. Entomol. 36: 4363.
Florida Entomologist 78(1)
HOST SPECIFICITY OF SEVERAL PSEUDACTEON(DIPTERA:
PHORIDAE) PARASITES OF FIRE ANTS (HYMENOPTERA:
FORMICIDAE) IN SOUTH AMERICA
SANFORD D. PORTER,' HAROLD G. FOWLER,2 SOFIA CAMPIOLO,2
AND MARCOS A. PESQUERO3
'Medical and Veterinary Entomology Research Laboratory, USDA, Agricultural
Research Service, PO. Box 14565, Gainesville, FL 32604
Departamento de Ecologia, Institute de Biociencias, Universidade Estadual
Paulista, 13500, Rio Claro, SP, Brazil
3Departamento de Zoologia, Institute de Biociencias, Universidade Estadual Paulista,
18610, Botucatu, SP, Brazil
ABSTRACT
We tested the host specificity of several parasitic Pseudacteon scuttle flies in South
America with 23 species of ants in 13 genera. None of these ant species attracted
Pseudacteon parasites except Solenopsis saevissima (F. Smith) and to a lesser extent
Solenopsis geminata (Fab.). This result is encouraging because it indicates that the
Pseudacteon flies tested in this study would not pose an ecological danger to other ant
genera if these flies were introduced into the United States as classical biological con
trol agents of imported fire ants. This prediction of host specificity will, of course, need
to be validated with potential hosts in the United States before these flies can be re
leased.
Key Words: Biocontrol, Solenopsis, Brazil
RESUME
Probamos la especificidad de hospedero de varias moscas parasitas del g6nero
Pseudacteon contra 23 species de hormigas pertenecientes a 13 g6neros en America
del Sur. Ninguna de las hormigas atrajo moscas parasitas, con la excepci6n de Sole
nopsis saevissima (F. Smith) y, en menor escala, Solenopsis geminata (F.). Este resul
tado es alentador porque indica que las moscas Pseudacteon probadas en este ensayo
no harian danos ecoldgicos a otros g6neros de hormigas, si estas fueran introducidas
en los Estados Unidos como agents de control bioli6gico conta las hormigas de fuego.
Tal predicci6n de la especificidad de hospedero, claro, necesitaria ser valorada con
hospederos potenciales en los Estados Unidos, antes que las moscas fueran liberadas.
When fire ants were introduced into the United States, they left behind almost all
of their natural enemies in South America (Jouvenaz 1983). Consequently, release
from natural enemies is a likely explanation for the 5 to 10-fold increase in fire ant
densities reported in North America (Porter et al. 1992). A number of organisms have
been considered as possible biological control agents for exotic fire ant populations, in
cluding micro-organisms, nematodes, a parasitic wasp, parasitic phorid flies, and
other ants (Buren 1983, Feener & Brown 1992, Heraty et al. 1993, Jouvenaz et al.
1988, Patterson & Briano 1993).
This article is from Florida Entomologist Online, Vol. 78, No. 1 (1995).
FEO is available from the Florida Center for Library Automation gopher (sally.fcla.ufl.edu)
and is identical to Florida Entomologist (An International Journal for the Americas).
FEO is prepared by E. O. Painter Printing Co., P.O. Box 877, DeLeon Springs, FL. 32130.
March, 1995
Porter et al.: Phorid Fly Host Specificity
Phorid or scuttle flies of the genus Pseudacteon Coquillett were proposed as biolog
ical control agents because of their dramatic impacts on fire ant foraging rates and the
stereotypical defensive reactions of fire ant workers to scuttle fly attacks (Feener &
Brown 1992, Porter et al. 1995a). But no matter how effective phorid flies might be in
fire ant biocontrol, they cannot be released into the United States until it can be dem
onstrated that they will not cause ecological problems for native non-target organ
isms.
Available collection data indicates that individual Pseudacteon species are almost
always specific to one genus of ants (Borgmeier 1962, 1963, 1969; Borgmeier & Prado
1975; Disney 1991, 1994; Williams & Banks 1987). The European species Pseudacteon
formicarum (Verrall) has been reported from Lasius and several other ant genera (Do
nisthorpe 1927), but tests by Wasmann (1918) indicate that it is specific to Lasius.
One rare South American species (Pseudacteon convexicauda Borgmeier) has been
collected over Solenopsis and Paratrechina nests (Borgmeier 1962), but no details are
given and this has not been confirmed by other collectors or the presence of developing
larvae. A report that Pseudacteon borgmeieri Schmitz attacks both Solenopsis and
Camponotus ants (Disney 1994) is based on a mistranslation of Borgmeier (1922),
who actually stated that he only found this fly over Solenopsis nests even though he
also inspected other ant nests including two species of Camponotus.
Sixteen South American Pseudacteon species have only been reported from Sole
nopsis ants (Disney 1994), including 13 with lobed ovipositors and three with unlobed
ovipositors. Three additional South American Pseudacteon species plus several from
North America have been reported attacking other ant genera. All of the new-world
species reported from genera other than Solenopsis have unlobed ovipositors. The 20
or more new-world species of Pseudacteon with bilobed or trilobed ovipositors are re
ported to attack only Solenopsis ants (Borgmeier 1962, 1963, 1969; Borgmeier &
Prado 1975; Disney 1991).
Many of the Pseudacteon species that attack fire ants in South America are
broadly distributed (Borgmeier 1963, Borgmeier & Prado 1975) across the ranges of
several fire ant species (Trager 1991). Pseudacteon litoralis Borgmeier, Pseudacteon
tricuspis Borgmeier, Pseudacteon obtusus Borgmeier, Pseudacteon wasmanni
(Schmitz) and Pseudacteon curvatus Borgmeier have all been collected attacking both
Solenopsis invicta Buren and Solenopsis saevissima (F Smith) (Williams 1980, Porter
et al. 1995b, unpublished data). However, the fact that four Pseudacteon species in the
United States all attack Solenopsis geminata (Disney 1991, Feener 1987), but not
sympatric populations of the imported fire ant, S. invicta, suggests that some flies
may also be specific to particular fire ant species or species groups (Feener & Brown
1992).
The objective of this study was to determine if the Pseudacteon flies that attack So
lenopsis fire ants in South America will also attack other genera of South American
ants.
MATERIALS AND METHODS
In order to test the species specificity of Pseudacteon flies, we collected 23 species
of ants in 13 genera. These ants were separated from their nest material and placed
into white plastic trays coated with fluon so they could not escape. We used either 30
by 40 cm trays that contained 10-cm petri dish nests or 13 by 30 cm trays that con
trained water tube nests (Banks et al. 1981). Only one type of nest and tray was used
at each location. During tests, lids on the petri dish nests were removed or ants were
shaken out of nest tubes to expose as many ants as possible to potential phorid at
tacks. The number of ants in a tray varied between several hundred and several thou
Florida Entomologist 78(1)
sand depending on their size and availability. During tests, trays were carried to a
test site and placed in shaded locations several m apart. All scuttle flies that appeared
over the trays were collected using a double-chambered Allen aspirator (BioQuip",
Gardena, CA). This style of aspirator was particularly effective in capturing attacking
flies (>90%) because the long flexible collection tube was easily maneuvered over the
trays as the flies darted back and forth. A second advantage was that the inner cham-
ber is a small vial that can be easily shaded with a hand so that the flies move into the
light while the vial is being exchanged. Use of this aspirator was a considerable im
provement over the snap-cap vial technique used by previous researchers (Williams
1980).
Tests were conducted using two different protocols. In the first set of tests, ants
were set out for 75 min at a single location on the Rio Claro campus of Sao Paulo State
University (UNESP-Rio Claro). Each test included one tray of fire ants (S. saevissima)
and four to eight trays containing other species of ants. This procedure was repeated
19 times over a 27-day period from 11 December 1992 to 7 January 1993. The second
set of tests was conducted in February, 1994 at five sample sites around each of two
cities (Rio Claro, SP and Vicosa, MG). Sample sites were 1-10 km apart. Two clusters
of 4-5 trays were set out at each site for 30-45 min; each cluster contained one fire ant
colony and 3-4 other species of ants. Voucher specimens of ants and flies have been de
posited with the Museu de Zoologia, Universidade de Sao Paulo, Brazil.
RESULTS AND DISCUSSION
The Pseudacteon flies in our tests were specific to the genus Solenopsis. In the first
series of tests at the single site on the UNESP Rio Claro campus, we collected Pseu
dacteon phorids from the tray with S. saevissima on 74% (14/19) of the observation
days. Altogether, we collected 50 Pseudacteon flies: 47 litoralis, 2 tricuspis, 1
P wasmanni. No Pseudacteon flies were observed flying over any of the other ants
tested (number of trials is shown in parentheses): Atta sexdens (18), Monomorium
pharaonis (16), Camponotus rufipes (14), Paratrechina sp. (7), Odontomachus minu
tus (6), Myrmelachista autori (6), Ectatomma quadridens (5), Pachycondyla striata
(5), Pheidole sp. 2 (5), Crematogaster sp. (4), Pheidole oxyopus (4), Camponotus ab
dominalis (3), Camponotus blandus (2). We also collected 11 Myrmosicarius grand
cornis Borgmeier phorid flies from trays with Atta sexdens on eight different
occasions. Two unidentified phorids (not Pseudacteon) appeared to be attracted to a
Paratrechina sp. colony on two occasions.
Results for the second set of tests at sites around Rio Claro and Vicosa were simi
lar. We collected Pseudacteon phorids at 75% of the nests with S. saevissima (7/10 in
Rio Claro and 8/10 in Vicosa). We collected 23 Pseudacteon phorids at the Rio Claro
sites (3 curvatus, 3 tricuspis, 7 P. pradei, 8 wasmanni, 1 litoralis, 1
P borgmeieri) and 12 more at the Vicosa sites (2 pradei, 10 wasmanni). We also
collected three phorids (1 pradei, 2 P wasmanni) that were attracted to a nest
tray with black Solenopsis geminata (Fab.) at two of the five Vicosa sites. The other 10
species of ants tested did not attract phorid flies (the number of tray periods is shown
in parentheses; two species have 10 periods because two trays were used at each site):
Rio Claro Area Odontomachus brunneus (5), Acromyrmex rugosus (10), Pheidole
sp.(5), Camponotus angulatus (10); Vicosa Area -Odontomachus haematodus (5), Do
rymyrmex sp. (5), Atta sexdens (5), Camponotus rufipes (5), Camponotus sp. 3 (5),
Paratrechina longicornis (5).
When we compared the number of fire ant trays attracting Pseudacteon flies to the
number of non-fire ant trays attracting Pseudacteon, the results were very significant,
regardless of whether we analyzed results from the two tests separately or combined
March, 1995
Porter et al.: Phorid Fly Host Specificity
(x2 tests, P < 0.0001). When we summed the numbers of scuttle flies collected from the
campus tests with the numbers collected at the two multiple-site tests, four Pseudac
teon species (P litoralis, P wasmanni, P pradei, and P tricuspis) were significantly
more likely to be caught with fire ants than with non-fire ants (x2 tests, P < 0.001, P
< 0.001, P < 0.002, and P < 0.05, respectively). Two species (P curvatus and P borg
meieri) were not collected frequently enough to make a determination. The 88 flies we
collected over fire ant colonies were sufficient to have detected non-fire ant attraction
rates as small as 3.5% at P < 0.05 (i.e.; 0.96588). Statistical sensitivity for individual
ant species was, of course, dependent on the number of scuttle flies collected when a
particular ant species was available for attack. Statistical sensitivity ranged from 5%
for Atta sexdens to about 25% for ant species only tested five times around the Vicosa
area. Nevertheless, even if Pseudacteon flies had been attracted to other ant genera
at some low rate, this would not necessarily mean that they would oviposit in them or
that these ants would be suitable hosts for larval development.
Both S. saevissima and S. geminata were collected in the Vicosa area. Solenopsis
saevissima was sparsely distributed in urban and agricultural sites while S. geminata
was only found at two urban sites. No scuttle flies were found attacking S. geminata
at either of its collection sites, although several scuttle flies were collected while at
tacking a S. saevissima colony at one of these sites.
In order to further investigate Pseudacteon attacks on S. geminata colonies, we re
turned to one of the Vicosa sites where we had previously captured phorids attacking
S. saevissima nests. Trays with S. saevissima and S. geminata were set out alter
nately. When the S. saevissima trays were present, we observed 3-5 phorids continue
ously flying around the trays and attacking workers. After the S. saevissima trays
were removed and the S. geminata trays were set out, we observed only 1-2 phorids
in the trays and the number usually declined to 0-1 after a couple of minutes. Within
a minute or two after returning the S. saevissima trays, the number of scuttle flies in
creased to 3-5 again. This pattern was observed through three cycles of replacing S.
saevissima colonies with S. geminata colonies. Careful observations of scuttle flies in
the S. geminata colonies indicated that they did attempt to oviposit on some of the
workers, but attempts were not very frequent, and the workers did not respond with
the stilting behavior normally seen after S. saevissima workers have been attacked
(Porter et al. 1995a). Many of the S. geminata workers were observed in a standard
defensive posture with the head raised and the gaster curled under the thorax
(Feener & Brown 1992), but general colony immobility was not observed (Porter et al.
1995a). Further tests will be necessary to determine if eggs are actually laid in S.
geminata workers and whether they can produce viable larvae. At the end of the test,
we collected four P pradei, two P. wasmanni, and six Pseudacteon affinis Borgmeier
over the S. saevissima nests.
Information from this study together with previous collection records (Borgmeier
1962, 1963, 1969; Borgmeier & Prado 1975) strongly indicate that most Pseudacteon
parasites of fire ants will meet a critical requirement of a good biological control
agent; that is, host specificity. The phorid flies tested in this study appear to be specific
to a single genus of ants (Solenopsis) and perhaps to a specific subcomplex within that
genus. These results are encouraging and should justify further and more extensive
tests with ants from North America. Tests will also need to be done with other groups
of insects, but it is highly unlikely that Pseudacteon flies would pose a threat to any
arthropod group other than ants, considering their oviposition behavior, their highly
specialized ovipositors, their specialized adaptations for pupation in the head cap
sules of worker ants (Porter et al. 1995b), and the fact that virtually all phylogeneti
cally related phorid genera are ant parasites (Brown 1993, Disney 1994).
Florida Entomologist 78(1)
ACKNOWLEDGMENTS
Thanks are extended to T M. C. Della Lucia (UVF, Vicosa) and E. F Vilela (UVF,
Vicosa) for providing logistical support and laboratory space in Vicosa. Special thanks
are also extended to G. M. Rodrigues (UVF, Vicosa) for his invaluable field assistance
and expertise. B. V Brown (L.A. County Museum), D. H. Feener (Univ. of Utah), L. E.
Gilbert (Univ. of Texas), and D. P Wojcik (USDA-ARS, MAVERL) read the manuscript
and provided many helpful comments. Thanks are extended to B. V Brown for his
early, but essential help with phorid identifications and to both B. V Brown and D. H.
Feener for general discussions concerning the host specificity of parasitic phorids.
This work was partially funded with a grant from the U.S.-Brazil Science and Tech
nology Initiative through the USDA-OICD-IRD. Mention of a commercial product
does not imply endorsement by the authors or their employers.
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BANKS, W. A., C. S. LOFGREN, D. P. JOUVENAZ, C. E. STRINGER, P. M. BISHOP, D. F.
WILLIAMS, D. P. WOJCIK, AND B. M. GLANCEY. 1981. Techniques for collecting,
rearing, and handling imported fire ants. USDA, SEA, AATS-S-21, 9 p.
BORGMEIER, T. 1922 (1921). Zur Lebensweise von Pseudacteon borgmeieri Schmitz (in
litt.) (Diptera: Phoridae). Zs. Deut. Ver. Wiss. Kunst Sao Paulo 1: 239-248.
BORGMEIER, T 1962. Cinco esp6cies novas do genero Pseudacteon Coquillett. Arq.
Mus. Nac. (Rio de Janeiro) 52: 2730.
BORGMEIER, T 1963. Revision of the North American phorid flies. Part I. The Phori
nae, Aenigmatiinae, and Metopininae, except Megaselia (Diptera: Phoridae).
Stud. Entomol. 6: 1256.
BORGMEIER, T 1969. New or little-known phorid flies, mainly of the Neotropical re
gion (Diptera: Phoridae). Stud. Entomol. 12: 33-132.
BORGMEIER, T., AND A. P. PRADO. 1975. New or little known Neotropical phorid flies,
with description of eight new genera (Diptera: Phoridae). Stud. Entomol. 18: 3
90.
BROWN, B. V 1993. Taxonomy and preliminary phylogeny of the parasitic genus Apo
cephalus, subgenus Mesophora (Diptera: Phoridae). Syst. Entomol. 18:191-230.
BUREN, W. F 1983. Artificial faunal replacement for imported fire ant control. Florida
Entomol. 66: 93-100.
DISNEY, R. H. L. 1991. The fire-ant parasitoids of the Pseudacteon spatulatus complex
(Diptera, Phoridae; Hymenoptera, Formicidae). Sociobiology 18: 283-298.
DISNEY, R. H. L. 1994. Scuttle flies: the Phoridae. Chapman & Hall, London, 467 p.
DONISTHORPE, H. S. J. K. 1927. The guests of British ants, their habits and life histo
ries. George Routledge & Sons, London, 244 p.
FEENER, D. H., JR. 1987. Size-selective oviposition in Pseudacteon crawfordi (Diptera:
Phoridae), a parasite of fire ants. Ann. Entomol. Soc. America 80: 148-151.
FEENER, D. H., JR., AND B. V. BROWN. 1992. Reduced foraging of Solenopsis geminata
(Hymenoptera: Formicidae) in the presence of parasitic Pseudacteon spp.
(Diptera: Phoridae). Ann. Entomol. Soc. America 85: 8084.
HERATY, J. M., D. P. WOJCIK, AND D. P. JOUVENAZ. 1993. Species of Orasema parasitic
on the Solenopsis saevissima-complex in South America (Hymenoptera: Eucha
ritidae, Formicidae). J. Hymen. Res. 2: 169-182.
JOUVENAZ, D. P. 1983. Natural enemies of fire ants. Florida Entomol. 66: 111-121.
JOUVENAZ, D. P., D. P. WOJCIK, M. A. NAVES, AND C. S. LOFGREN. 1988. Observations
on a parasitic nematode (Tetradonematidae) of fire ants, Solenopsis (Formi
cidae), from Mato Grosso. Pesq. Agropec. Brasil. 23: 525-528.
PATTERSON, R. A., AND J. A. BRIANO. 1993. Potential of three biological control agents
for suppression of Solenopsis invicta, red imported fire ant, p. 35-43 in K. B.
Wildey and W. H. Robinson [eds.] Proceedings of the 1st international confer
ence on insect pests in the urban environment. BPCC Wheatons Ltd., Exeter,
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March, 1995
Porter et al.: Phorid Fly Host Specificity 75
PORTER, S. D., H. G. FOWLER, AND W. P. MACKAY. 1992. Fire ant mound densities in
the United States and Brazil (Hymenoptera: Formicidae). J. Econ. Entomol.
85: 1154-1161.
PORTER, S. D., R. K. VANDER MEER, M. A. PESQUERO, S. CAMPIOLO, AND H. G.
FOWLER. 1995a. Reactions of Solenopsis fire ants to attacks of Pseudacteon
phorid flies in southeastern Brazil. Ann. Entomol. Soc. America (In press).
PORTER, S. D., H. G. FOWLER, S. CAMPIOLO, AND M. A. PESQUERO. 1995b. Rearing
Pseudacteon phorid fly maggots (Diptera: Phoridae) in the heads of Solenopsis
fire ant workers (Hymenoptera: Formicidae). Environ. Entomol. (submitted)
TRAGER, J. C. 1991. A revision of the fire ants, Solenopsis geminata group (Hy
menoptera: Formicidae: Myrmicinae). J. New York Entomol. Soc. 99: 141-198.
WASMANN, E. 1918. Zur Lebensweise und Fortpflanzung von Pseudacteon form
carum Verr. (Diptera, Phoridae). Biol. Zentbl. 38: 317-329.
WILLIAMS, D. F., AND W. A. BANKS. 1987. Pseudacteon obtusus (Diptera: Phoridae) at
tacking Solenopsis invicta (Hymenoptera: Formicidae) in Brazil. Psyche 94: 9
13.
WILLIAMS, R. N. 1980. Insect natural enemies of fire ants in South America with sev
eral new records. Proc. Tall Timbers Conf. Ecol. Anim. Control Habitat Man
age. 7: 123-134.
++++++++++++++++++++++++++++++++++++++++++++++++++++
McAuslane et al.: Resistance in Peanut to B. argenifolii
EVALUATION OF PEANUT BREEDING LINES FOR
RESISTANCE TO SILVERLEAF WHITEFLY (HOMOPTERA:
ALEYRODIDAE)
HEATHER J. MCAUSLANE, DAVID A. KNAUFT' AND FREDDIE A. JOHNSON
Department of Entomology & Nematology, P.O. Box 110630, University of Florida,
Gainesville FL 32611 0630
'Agronomy Department, P.O. Box 110500, University of Florida,
Gainesville FL 32611 0500
Current address: Crop Science Department, North Carolina State University,
P.O. Box 7620, Raleigh NC 27695-7620
ABSTRACT
Silverleafwhitefly, Bemisia argentifolii Bellows & Perring, n. sp., is a new and oc
casionally damaging pest of peanut, Arachis hypogaea L., in Florida and other south
ern states. In 1992 and 1993, elite germplasm from the peanut breeding program at
the University of Florida and several commercial cultivars were evaluated for resis
tance to silverleaf whitefly In 1992, 52 genotypes that were chosen based on their
performance in previous trials were evaluated. Numbers of whitefly red-eyed nymphs
on peanut genotypes differed significantly. However, only two genotypes supported
fewer whiteflies (although not significantly) than the cultivar 'Southern Runner'. In
1993, we evaluated selections of crosses between Florida parent material (81206 and
567A) and a North Carolina parent (GP-NC343) with multi-insect resistance. All se
elections tested had higher numbers of whitefly eggs and red-eyed nymphs than either
'Florunner' or 'Southern Runner'. No resistance to silverleaf whitefly was found in the
peanut germplasm tested.
This article is from Florida Entomologist Online, Vol. 78, No. 1 (1995).
FEO is available from the Florida Center for Library Automation gopher (sally.fcla.ufl.edu)
and is identical to Florida Entomologist (An International Journal for the Americas).
FEO is prepared by E. O. Painter Printing Co., P.O. Box 877, DeLeon Springs, FL. 32130.
Florida Entomologist 78(1)
Key Words: Plant resistance, Arachis hypogaea, Bemisia argentifolii, pest manage
ment
RESUME
La mosco blanca, Bemisia argentifolii Bellows & Perring, n. sp., es una nueva
plaga que ocasionalmente dana el mani, Arachis hypogaea L., en la Florida y otros es
tados del sur. En 1992 y 1993, la resistencia a la mosca blanca fue evaluada en ger
moplasma elite del program de propagaci6n de mani de la Universidad de la Florida
y en various cultivares comerciales. En 1992, fueron evaluados 52 genotipos escogidos
sobre la base de su comportamiento en pruebas previas. El numero de ninfas en es
tado de ojos rojos sobre los genotipos de mani difiri6 significativamente. Sin embargo,
solamente dos genotipos sportaron menos moscas blancas que el cultivar "Southern
Runner". En 1993, evaluamos selecciones de cruces entire material parental de Flo
rida (81206 y 567A) y de Carolina del Norte (GP-NC343) con resistencia a multiples
insects. Todas las selecciones probadas tuvieron mayor nfmero de huevos de mosca
blanca y ninfas en estado de ojos rojos que "Florunner" y "Southern Runner". No se en
contr6 resistencia a la mosca blanca en el germoplasma de mani probado.
The silverleaf whitefly, Bemisia argentifolii Bellows & Perring [previously known
as B strain of the sweetpotato whitefly, Bemisia tabaci (Gennadius)], has become a
key pest of many agronomic, ornamental and vegetable crops since its first appear
ance in 1986 in Florida greenhouses (Price et al. 1987). B. argentifolii differs from B.
tabaci, present in Florida since at least 1897 (Quaintance 1900), in host range (Byrne
& Miller 1990), virus transmission capabilities, biology (Bethke et al. 1991, Costa &
Brown 1991), production of honeydew (Byrne & Miller 1990), and insecticide resis
tance (Prabhaker et al. 1985). This whitefly caused at least $500,000,000 in losses to
the agricultural community in 1991 alone (Perring et al. 1993). The damage produced
by the whitefly includes plant debilitation due to feeding by immature stages and
adults, product contamination with honeydew and resulting sooty mold, transmission
of plant-pathogenic viruses and induction of physiological disorders.
Peanut, Arachis hypogaea L., is one of the new host plants infested by the silver
leaf whitefly Whiteflies were observed feeding in large numbers on peanut in north
ern Florida in 1988 and 1989, and many growers resorted to weekly applications of
broad spectrum insecticides in an attempt to reduce populations (F.A.J., unpublished
data). Despite heavy use of insecticides, some growers attributed yield losses of 459.5
kg per ha (2,500 lb per acre) to this whitefly (Leidner 1991).
In 1991, we initiated a search for resistance to silverleaf whitefly among common
cultivars and breeding lines from the University of Florida peanut breeding program.
Field trials in Georgia indicated that 'Southern Runner' appeared to be more resis
rant than 'Florunner' (Lynch & Chamberlin 1993); however, we found no significant
differences among these cultivars and another four cultivars commonly grown in Flor
ida (McAuslane et al. 1994). We screened 150 breeding lines and cultivars in 1991,
and chose 52 of those with low whitefly infestations for further evaluation in 1992.
This paper presents the results of the 1992 evaluation, and a 1993 test of several
breeding lines incorporating North Carolina germplasm containing multi-insect re
distance. The North Carolinan germplasm (GP-NC343) was originally released for re
distance to southern corn rootworm, Diabrotica undecimpunctata howardi Barber
(Campbell et al. 1971). Later field research revealed that crosses incorporating GP
NC343 were resistant to thrips, leafhoppers, and defoliators (Campbell et al. 1987).
March, 1995
McAuslane et al.: Resistance in Peanut to B. argenifolii
MATERIALS AND METHODS
Tests-1992. On 29 June, 52 peanut selections (42 elite breeding lines and 10 re
leased cultivars) were planted in a 0.3-ha field on the campus of the University of
Florida, Gainesville, Alachua County. Plots were single rows, 6.1 m in length, spaced
by 90 cm, and were replicated four times in a randomized complete block design. Ba
cillus thuringiensis [Dipel 2X, Abbott Laboratories, North Chicago, IL, (1.12 kg for
mulation per ha)] was applied on 18 and 23 September, and 9 October for control of
lepidopterous defoliators. Chlorothalonil [Bravo 720, ISK Biotech Corp., Mentor, OH,
(1.18 kg AI per ha)] was applied on 13 and 25 August, 11 and 23 September, and 9 and
27 October for control of early leaf spot, Cercospora arachidicola Hori, and late leaf
spot, Cercosporidium personatum Berk & Curt Deighton.
Plots were sampled at 10-d intervals from 6 August until 4 November by selecting
10 leaflets per plot. Leaflets were chosen from the fourth fully expanded leaf (any one
of the four leaflets in the tetrafoliolate) below the terminal leaf on lateral branches.
Previous research indicated that the greatest densities of red-eyed nymphs occurred
in this region of the plant canopy (McAuslane et al. 1993). Leaflets were transported
to the laboratory in a cooler, then refrigerated until immature whiteflies could be
counted (48 h maximum). Red-eyed nymphs were counted on the bottom surface of
each leaflet under 12x magnification. We measured the areas of leaflets sampled on 26
October using a leaf area meter (LI-COR, Model 3000, Lincoln, NE). Counts were
standardized based on leaflet surface area. All data were converted to numbers of red
eyed nymphs per 5 cm2 (= approximate area of one leaflet).
Tests-1993. On 3 June, seven pedigreed breeding lines (three produced by crossing
81206 with GP-NC343 and four produced by crossing 567Awith GP-NC343), the par
ent with multi-insect resistance (GP-NC343), and two commercial cultivars ('Florun
ner' and 'Southern Runner') were planted in the same field that was used in 1992.
Plots were two rows wide (row spacing of 90 cm) and 6.1 m long, and were replicated
four times in a randomized complete block design. Bacillus thuringiensis and chlo
rothalonil, at the same rates as in 1992, were applied on 16 and 26 July, 6 and 26 Au
gust, and 20 September.
Plots were sampled as in 1992 at 10-d intervals from 15 July until 4 October, ex
cept that whitefly eggs and red-eyed nymphs were counted on the top and bottom sur
faces of 20 leaflets per plot. The areas of leaflets sampled on 4 August and 23
September were measured using a leaf area meter. All data were converted to number
of whitefly stages per 5 cm2. Leaflet areas recorded on 4 August were used to convert
whitefly counts obtained on the first five sample dates, and areas recorded on 23 Sep
member were used to convert counts on the last four dates.
Data were analyzed using the GLM procedure (SAS Institute 1987). Prior to anal
ysis, count data were square root (x+ 1)transformed to correct for nonnormality of the
data and proportion data were arcsin (x)-transformed to correct for nonhomogeneity
of variance. Means were separated using least significant differences at a significance
level of 5% (SAS Institute, 1987). Untransformed means are presented in all tables
and figures.
RESULTS AND DISCUSSION
Tests-1992. Numbers of red-eyed nymphs counted on the lower surfaces of leaflets
differed significantly among genotypes (F= 1.57; df = 51, 153; 0.01 < P< 0.05). When
genotypes were analyzed by date, they differed significantly on four of ten dates (4, 15,
and 25 September and 15 October; F= 1.51; df = 51, 153) (Fig. 1). When genotypes
were ranked by season-long infestation, F1138 (0.031 + 0.011 red-eyed nymphs per 5
Florida Entomologist 78(1)
March, 1995
cm2 leaflet surface) and F1084 (0.044 0.015) were least infested, and 87118 was most
infested (0.220 + 0.042). In an adjacent test [(McAuslane et al. 1994)], 'Southern Run
ner'was also infested with very low numbers of red-eyed nymphs (0.049 + 0.009). This
adjacent cultivar experiment was treated and sampled in the same manner as the
genotype trial. Although whitefly numbers on 'Southern Runner' cannot be compared
statistically to numbers of whiteflies on the genotypes in this study, the data indicate
that, under these infestation levels, no University of Florida genotypes were more re
sistant than cultivars already commonly grown in Florida. Up to 80% of whiteflies on
the genotypes were parasitized by the end of the season (data not shown). Parasitism
may have contributed to the low whitefly infestations observed in this trial.
Tests-1993. Date was a significant source of variability in numbers of eggs (F
12.54; df 8, 240; P< 0.01) and red-eyed nymphs (F= 10.58; df = 8, 240; P< 0.01).
There were no interactions between date and cultivar. Genotype significantly influ
enced number of eggs (F= 20.14; df = 9, 27; P< 0.01) and red-eyed nymphs (F= 3.44;
df = 9, 27; P< 0.01). GP-NC343 and all breeding lines except F1384 supported more
whitefly eggs than either 'Florunner' or 'Southern Runner' (Table 1). However, only
F1436, F1435 and GP-NC343 supported significantly more red-eyed nymphs than the
two cultivars (Table 1). Numbers of eggs on genotypes differed significantly on all
dates except the first and the last, while red-eyed nymph counts differed significantly
on only four dates (13 and 24 August, and 3 and 23 September) (Fig. 2). Crosses be
tween 81206 and GP-NC343 were significantly more infested with eggs than were
crosses between 567A and GP-NC343. Cultivar 81206 is late maturing and produces
new vegetation throughout the season while 567A, which is early maturing and more
determinant, slows vegetative growth at the end of the season. (The presence of suc
S0.6
a) **
S 0.5
'
S0.4-
o **
4 0.3
U 0.2
w
C 0.1-
6
Z 0
8/6 8/20 8/26 9/4 9/15 9/25 10/5 10/1510/26 11/4
Date
Fig. 1. Average number of red-eyed nymphs per peanut leaflet in Gainesville, FL,
1992. Counts were made on the lower surfaces of leaflets and data from all peanut se
elections were combined. Asterisks indicate dates on which counts differed signifi
cantly among genotypes (* 0.01 < P < 0.05, ** P < 0.01). Error bars are one
standard error of the mean.
McAuslane et al.: Resistance in Peanut to B. argenifolii
TABLE 1. AVERAGE NUMBER OF SILVERLEAF WHITEFLY EGGS AND RED-EYED NYMPHS
(REN) PER PEANUT LEAFLET (STANDARDIZED 5 CM2 AREA) IN GAINESVILLE,
FL, 1993.
Accession
Number Parentage Pedigree/Cultivar Mean + SEM'
Eggs REN
F1437 81206xGPNC343 8815B-4-2-2-3-B 2.67+0.18a 0.16+0.02bc
F1436 81206xGP-NC343 8815B-4-2-2-1-B 2.10 + 0.12b 0.21 +0.02ab
F1435 81206xGP-NC343 8815B-3-2-11b3 1.90 + 0.10b 0.25 0.03a
F1386 567AxGP-NC343 8816B-Bx4-TV 5-b3 1.54 0.11c 0.12 0.01cd
GP-NC343 1.36+0.08c 0.22+0.02a
F1383 567AxGP-NC343 8816B-Bx4-RV 1-b2 1.36 + 0.08c 0.13 + 0.02cd
F1385 567AxGP-NC343 8816B-Bx4-TV 3-b3 1.26 + 0.07cd 0.13 + 0.02cd
F1384 567AxGP-NC343 8816B-Bx4-TV 1 b3 1.15 + 0.08de 0.10 + 0.02d
'Florunner' 1.12 + 0.07e 0.13 + 0.02cd
'Southern Runner' 1.07 + 0.06e 0.14 + 0.02cd
1Numbers within a column followed by the same letter did not differ significantly at a = 0.05 (least significant
difference test on square root [x + 1] transformed data).
culent new growth may have induced ovipositing whiteflies to lay eggs preferentially
on the crosses incorporating 81206 germplasm.
In 1993, whitefly lifestages were counted on both surfaces of the peanut leaflet.
McAuslane et al. (1993) found that up to 35% of whitefly red-eyed nymphs may occur
on the top surface of peanut leaflets. Lynch & Simmons (1993) reported that the pro
portion of whitefly immature stages on top and bottom surfaces of 'Florunner' leaves
changed over the course of sampling, with whiteflies becoming more common on the
upper surface of leaflets at the end of the sample period. In this study, the distribution
of eggs between top and bottom leaflet surfaces differed significantly among dates (F
23.55; df= 8, 240; P< 0.01), and among cultivars (F= 9.45; df= 9, 27; P< 0.01), rang
ing from 76% of eggs on the bottom surface of F 1435 leaflets to only 59% on the bottom
surface of F1383. There was no date by cultivar interaction for either eggs or red-eyed
nymphs. The distribution of red-eyed nymphs between top and bottom surfaces dif
fered among dates (F= 2.75; df = 7, 133; 0.01 < P< 0.05), but not among cultivars (F
1.62; df = 9, 27; P> 0.05), averaging 61.3% on the bottom leaflet surface. Distribu
tion of eggs and red-eyed nymphs between top and bottom leaflet surfaces followed a
similar trend. Whiteflies were more common on the bottom surface of leaflets early in
the season but were about equally abundant on top and bottom surfaces at the end of
the sampling period. These results are similar to the findings of Lynch & Simmons
(1993).
Three years of sampling silverleaf whitefly on peanut genotypes held by the Uni
versity of Florida yielded no resistant germplasm. The germplasm evaluated repre
sented an extensive cross-section of all four market types (runner, valencia, Spanish
and virginia), and included a wide range of parent material. Many lines tested had
multiple insect resistance (e.g., NC GP343), and multiple pest resistance (e.g., 81206
lines have broad disease and nematode resistance). Under the infestation conditions
experienced in 1992 and 1993, the cultivars commonly grown in Florida were more re
Florida Entomologist 78(1)
March, 1995
4.0 .. 1.0 a
"1 '. 0
w 3.5- 0 .
S- 0.8
3.0 -. ,- j.
:3 Eggs
S2.5 REN 0.6
C. 2.0 .. Eggs J-h a--
0 E- REN **
in 1.5
a 1.0 -
o 0.2 (
0.5 0
0 0
7/15 7/25 8/4 8/13 8/24 9/3 9/13 9/23 10/4
Date S
Fig. 2. Average number of eggs and red eyed nymphs per peanut leaflet (bars) and
proportion of each stage occurring on the bottom leaflet surface (lines) in Gainesville,
FL, 1993. Whiteflies were counted on upper and lower surfaces of each leaflet, and
data from all peanut selections were combined. Asterisks indicate dates on which
counts differed significantly among genotypes (* 0.01 < P< 0.05; ** P< 0.01). Er
ror bars are one standard error of the mean.
sistant than were the genotypes tested. These data indicate that breeding for peanut
resistance to silverleaf whitefly is likely to be difficult, and that alternative manage
ment strategies should be emphasized. Previous research (McAuslane et al. 1993,
1994) has indicated that native aphelinid parasitoids contribute heavily to whitefly
mortality in peanut fields when Bacillus thuringiensis is the only insecticide used.
Management of silverleaf whitefly in Florida peanuts may depend on cultural prac
tices (such as early planting or trap cropping), and on conservation of populations of
natural enemies by avoiding the use of broad spectrum insecticides.
ACKNOWLEDGMENT
We thank D. Boyd, S. Wineriter and P. Ruppert (Department of Entomology &
Nematology, University of Florida) for collection and processing of field samples, and
A. Smith and K. Portier (Statistics Department, University of Florida) for help with
data analysis. Thanks also go to J. Bennett (Agronomy Department, University of
Florida) for use of the leaf area meter, and to H. Alborn (Department of Chemical Ecol
ogy, G6teborg University, Sweden) and T X. Liu (Southwest Florida Research and Ed
ucation Center, Immokalee, University of Florida), for critical reviews of the
manuscript. Funding was provided by the Florida Peanut Grower's Association
Check-off Fund and Hatch Grant FLA-ENY 03194. This is Florida Agricultural Ex
periment Station Journal Series No. R-03873.
McAuslane et al.: Resistance in Peanut to B. argenifolii
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BYRNE, D. N., AND W. B. MILLER. 1990. Carbohydrate and amino acid composition of
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433-440.
CAMPBELL, W. V., D. A. EMERY, AND W. C. GREGORY. 1971. Registration of GP-NC343
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CAMPBELL, W. V., J. C. WYNNE, M. KEERATI-KASIKORN, S. SIRISINGH, C. ADALLA, AND
E.P. CADAPAN. 1987. Resistance of an international collection of peanut geno
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COSTA, H. S., AND J. K. BROWN. 1991. Variation in biological characteristics and es
terase patterns among populations of Bemisia tabaci, and the association of
one population with silverleaf symptom induction. Entomol. Exp. Appl. 61: 211-
219.
LEIDNER, J. 1991. Sweetpotato whiteflies: sticky pests threaten to spread. Prog.
Farmer 106: 36-37.
LYNCH, R. E., AND J. R. CHAMBERLIN. 1993. p. 120 in T. J. Henneberry, N. C. Toscano,
R. M. Faust and J. R. Coppedge [eds.], Sweetpotato whitefly: 1993 supplement
to the five-year national research and action plan-first annual review. USDA
ARS Publ. no. 112.
LYNCH, R. E., AND A. M. SIMMONS. 1993. Distribution of immatures and monitoring
of adult sweetpotato whitefly, Bemisia tabaci (Gennadius) (Homoptera: Aley
rodidae), in peanut, Arachis hypogaea. Environ. Entomol. 22: 375-380.
MCAUSLANE, H. J., F. A. JOHNSON, D. A. KNAUFT, AND D. L. COLVIN. 1993. Seasonal
abundance and within-plant distribution of parasitoids of sweetpotato whitefly,
Bemisia tabaci (Homoptera: Aleyrodidae) in peanuts. Environ. Entomol. 22:
1043-1050.
MCAUSLANE, H. J., F. A. JOHNSON, AND D. A. KNAUFT. 1994. Population levels and
parasitism of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) on peanut
cultivars. Environ. Entomol. 23: 1203-1210.
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1993. Identification of a whitefly species by genomic and behavioral studies.
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McAuslane et al.: Resistance in Peanut to B. argenifolii 82
Florida Entomologist 78(1)
EFFICACY OF EMAMECTIN BENZOATE AND BACILLUS
THURINGIENSISAT CONTROLLING DIAMONDBACK MOTH
(LEPIDOPTERA: PLUTELLIDAE) POPULATIONS ON CABBAGE
IN FLORIDA
GARY L. LEIBEE', RICHARD K. JANSSON2, GREGG NUESSLY3 AND JAMES L. TAYLOR4
'University of Florida Central Florida Research and Education Center
Institute of Food and Agricultural Sciences 2700 East Celery Avenue
Sanford, FL 32771
Merck Research Laboratories P O. Box 450 Hillsborough Road
Three Bridges, NJ 08887
3University of Florida Everglades Research and Education Center
Institute of Food and Agricultural Sciences P. O. Box 8003
Belle Glade, FL 33430
4Merck Research Laboratories P. O. Box 1893
Sanford, FL 32772
ABSTRACT
Emamectin benzoate (MK-244; Merck & Co., Rahway, NJ), used alone and alter
nated with Bacillus thuringiensis (Berliner) ssp. aizawai (Bta), Bta alone, and B. thu
ringiensis ssp. kurstaki (Btk) alone, were evaluated for control of diamondback moth,
Plutella xylostella (L.), in head cabbage at three locations in Florida. Additional treat
ments unique to each location were also evaluated. Emamectin benzoate alone, Bta
alone, emamectin benzoate alternated with Bta, and mevinphos were shown to be ef
fective. Btk was less efficacious than Bta at two locations.
Key Words: Plutella xylostella, emamectin benzoate, Bacillus thuringiensis, field effi
cacy
RESUME
El benzoato de emamectina (MK-244; Merck & Co., Rahway, NJ) usado solo y al
ternado con Bacillus thuringiensis (Berliner) ssp. aizawai (Bta), Bta solo, y B. thur
ingiensis ssp kurstaki (Btk) solo, fueron evaluados para el control de la polilla de
diamante, Plutella xylostella (L.), en col de repollo en tres localidaes de la Florida.
Tambien fueron evaluados tratamientos adicionales unicos en cada localidad. El ben
zoato de emamectina solo, Bta solo, el benzoato de emamectina alternado con Bta, y
el mevinf6s mostraron ser efectivos. Btk fue menos eficaz que Bta en las dos localida
des.
The diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), a world
wide pest of cruciferous crops (Talekar 1986), was easily managed in Florida until the
onset of insecticide resistance in the 1980s (Leibee & Savage 1992a,b). Loss of efficacy
with pyrethroids and methomyl caused growers to switch to intensive use of other in
This article is from Florida Entomologist Online, Vol. 78, No. 1 (1995).
FEO is available from the Florida Center for Library Automation gopher (sally.fcla.ufl.edu)
and is identical to Florida Entomologist (An International Journal for the Americas).
FEO is prepared by E. O. Painter Printing Co., P.O. Box 877, DeLeon Springs, FL. 32130.
March, 1995
Leibee et al.: Diamondback Moth Contol
secticides, especially Bacillus thuringiensis (Berliner) ssp. kurstaki (Btk). Shelton et
al. (1993) documented resistance to Btk and control failures with Btk products in sev
eral populations of diamondback moth in Florida in 1992. At present, the diamond
back moth has become very difficult to control with any of the currently registered
synthetic insecticides and Btk based products. The recently introduced products
based on B. thuringiensis (Berliner) ssp. aizawai (Bta) appear to be providing effective
control of diamondback moth in Florida. This is consistent with reports describing re
distance to Btk, but not to Bta, in Florida (Leibee & Savage 1992c, Shelton et al. 1993).
The development of new insecticides that circumvent the mechanisms of resis
tance that have developed in the diamondback moth has become extremely impor
tant, not only for control, but also for management of insecticide resistance. The
availability of several new insecticides with different chemistry and mode of action
would allow the implementation of management schemes designed to slow down the
selection for resistance to any one insecticide. Emamectin benzoate (MK-244) is a new
avermectin insecticide in development at Merck Research Laboratories targeted for
control of lepidopterous pests on a variety of crops.
This study was conducted to compare the efficacy of emamectin benzoate used
alone and alternated with Bta, Bta alone, and Btk alone for control of diamondback
moth on cabbage at three locations in Florida. Additional treatments unique to each
location were also evaluated.
MATERIALS AND METHODS
Studies were conducted in Florida during 1992 at the Central Florida Research
and Education Center (CFREC) in Sanford, Everglades Research and Education Cen
ter (EREC) in Belle Glade, and the Tropical Research and Education Center (TREC)
in Homestead. Additional studies were conducted during 1993 at the EREC.
Insecticidal Treatments
The insecticides common to all three locations were emamectin benzoate [MK-244
0.16 EC (emulsifiable concentrate), Merck Research Laboratories, Merck & Co., Rah
way, NJ] at 0.0084 kg (AI)/ha, B. thuringiensis ssp. aizawai (Bta) (XenTari, Abbott
Laboratories, North Chicago, IL) at 1.12 kg/ha, and B. thuringiensis ssp. kurstaki
(Btk) (DiPel 2X, Abbott Laboratories, North Chicago, IL) at 1.12 kg/ha. Additional in
secticides, adjuvants, and combinations tested at TREC were: Btk [AC 513,696 2X WP
wettablee powder), American Cyanamid Co., Princeton, NJ] at 1.12 kg/ha; Btk [AC
513,696 48 LC (liquid concentrate), American Cyanamid Co.] at 2.8 liter/ha; Btk
[Larvo-Bt LC (liquid concentrate), Knoll Bioproducts Co., Inc., Santa Fe, NM] at 0.3
liter/ha alone and at 0.3 liter/ha in combination with a feeding stimulant (Konsume,
Fermone, Phoenix, AZ) at 7.0 liter/ha; AC 513,696 48 LC at 2.8 liter/ha in combination
with Konsume at 7.0 liter/ha; Btktransconjugate [Cutlass WP wettablee powder), Ec
ogen, Inc., Langhorne, PA] at 2.24 kg/ha; and mevinphos [Phosdrin 4 EC (emulsifiable
concentrate), E. I. duPont de Nemours & Co., Wilmington, DE] at 0.56 kg (AI)/ha in
combination with Cutlass WP at 2.24 kg/ha. Additional insecticides and combinations
tested at EREC were: Btk/Bta transconjugate [Condor OF (oil flowable), Ecogen, Inc.,
Langhorne, PA] at 2.34 liter/ha; Btk recombinant (MVP, Mycogen Corp., San Diego,
CA) at 4.67 liter/ha; Cutlass WP at 2.24 kg/ha; Btk [Javelin WG wettablee powder),
Sandoz Agro, Inc., Des Plaines, IL] at 1.12 kg/ha; Btk [Biobit FC (flowable concern
trate), E. I. duPont de Nemours & Co., Wilmington, DE] at 3.5 liter/ha; thiodicarb
[Larvin 3.2 AF (aqueous flowable)], Rhone-Poulenc Ag Co., Research Triangle Park,
Florida Entomologist 78(1)
NC] at 0.9 kg (AI)/ha; methamidophos [Monitor 4 EC (emulsifiable concentrate),
Miles, Inc., Kansas City, MO] at 1.12 kg (AI)/ha; Larvin 3.2 AF at 0.9 kg (AI)/ha in
combination with DiPel 2X at 1.12 kg/ha; esfenvalerate [Asana XL 0.66 EC (emulsifi
able concentrate), E. I. duPont de Nemours & Co., Wilmington, DE] at 0.055 kg (AI)/
ha; Asana XL at 0.055 kg (AI)/ha in combination with DiPel 2X at 1.12 kg/ha;
mevinphos (Phosdrin 4EC) at 1.12 kg (AI)/ha; and mevinphos at 1.12 kg (AI)/ha in
combination with DiPel 2X at 1.12 kg/ha.
Two alternating application patterns were used for emamectin benzoate and Bta
at CFREC. One pattern started with two applications of emamectin benzoate and
then rotated every two applications with Bta; the other alternation started with Bta
and rotated every two applications with emamectin benzoate. Also at CFREC, an ad
ditional Bta treatment was tested in which applications were skipped if the infesta
tion level was < 5%. At TREC, one alternation pattern starting with Bta was used as
described above. At EREC, the pattern tested was three applications of emamectin
benzoate followed by three applications of Bta.
CFREC-Sanford
'Golden Acre' cabbage was transplanted on 4 Mar. 1992 into Myakka fine sand.
Plots consisted of four 9.0 m rows with a 0.76 m row spacing and about a 0.28 m plant
spacing. Four rows were left unplanted between each plot to provide a separation of
3.8 m. Plots were arranged in five blocks and the blocks were separated by 7.6 m al
leyways. All the treatments were assigned to plots in a randomized complete block de
sign with five replications. Conventional cultural practices were used for fertilization
and weed control.
Sprays were applied with a tractor-mounted, compressed-air sprayer. Three
hollow-cone nozzles (D2-25) were used per row; one overhead and one drop on each
side. The delivery rate of spray was 467.4 liter/ha with a boom pressure of about 3.2
kg/cm2 (45 psi) and a speed of 3.2 km/h. Application dates were 26 March, 1, 8, 15, 22,
and 29 April, and 6 and 13 May 1992. A buffer (Helena Buffer PS, Helena Chemical
Co., Memphis, TN) was used to maintain the pH of the spray water at 6.9. A
spreader-sticker (Triton B-1956, Rohm and Haas Co., Philadelphia, PA) was used in
all treatments at the rate of 5.0 ml per 7.6 liter of spray. The nontreated check re
ceived water and spreader-sticker at each application.
Ten plants per plot (5 randomly selected plants in the center of each of the two mid
dle rows) were examined weekly to determine the presence or absence of larvae and
pupae of each species on the bud (or head if formed) and next 4 youngest leaves. At
harvest (14 May), 10 mature plants (5 randomly selected plants in the center of each
of the two middle rows) were each placed into one of six damage categories. The head
and first four wrapper leaves were cut as a unit from the plant. Each wrapper leaf was
removed and inspected and then the head was inspected. A scale of 1 to 6, similar to
that of Greene et al. (1969), was used, in which 1 = no damage; 2 = no head damage
with minor feeding damage on wrapper leaves, found only by close inspection; 3 = no
head damage with obvious damage to wrapper leaves, generally obvious before re
moval of wrapper leaves; 4 = very minor feeding damage on head, not completely
through outer head leaves, evident only by close inspection; 5 = feeding completely
through outer head leaf or further into head; 6 = similar to 5 but more extensive, dam
age radiates further towards or past equator of head from top or bottom and laterally
around head. A damage rating of < 3 is marketable under normal market conditions,
wrapper leaves might be removed to market. A damage rating of < 4 is marketable un
der exceptional market conditions.
March, 1995
Leibee et al.: Diamondback Moth Contol
TREC-Homestead
'Rio Verde' cabbage seeds were incorporated into a germination mix (Pro-Mix) and
direct-seeded into a Krome, very gravelly loam soil on 8 January 1992. The soil was
fumigated with Terr-O Gas (75% methyl bromide, 25% chloropicrin; 246 kg/ha) and
covered with white on black plastic mulch on 27 December 1991. Plants were spaced
0.3-m apart within rows and 0.76-m apart between rows on 1.8 m-center beds. Con
ventional cultural practices were used for fertilization and weed control. All treat
ments except the emamectin benzoate (MK-244)/XenTari rotation treatment were
applied on 7 dates between 14 February and 27 March. Plants receiving the emamec
tin benzoate/XenTari rotation treatment were sprayed with XenTari on 4 dates (14
and 21 February, and 13 and 20 March) and with emamectin benzoate on the three re
maining dates (28 February, and 6 and 27 March). Treatments were replicated 4 times
in a randomized complete block design. Treatment plots were 4 rows (2 beds) by 9.1-m
long. A 1.5-m long section of nontreated plants separated replicates. Applications
were made using a tractor-mounted, single bed boom sprayer that operated at 6.9 kg/
cm2 (100 psi) and delivered 935 liters/ha through 6 D-4 Albuz red disc type ceramic
cone nozzles at 4.8 km/h. All treatments were applied in water. The pH of the water
was maintained between 6.5 and 7.5 using sulfuric acid buffer. All treatments were
applied with a surfactant, Triton B-1956, (0.49 liters/ha). The nontreated check was
not sprayed. Eight plants per plot (4 randomly selected plants in the center of each of
the two middle rows) were examined on 6 dates between 4 February and 19 March to
determine numbers of larvae and pupae per plant. Foliage injury was rated on 24
plants per plot (12 randomly selected plants in the center of each of the two middle
rows) at harvest (6 April), using a scale of 1 6 as previously described. Percentages of
marketable heads were based on ratings < 3.
EREC-Belle Glade
Both the 1992 and 1993 trials were conducted on Lauderhill soil. The following
methods and materials were common to both trials. 'Bravo' cabbage was direct-seeded
to raised beds on 0.91-m centers. Seeds were planted to two rows spaced 0.3-m apart
on each bed and later thinned to 0.3-m spacing between plants within each row. Treat
ments were replicated four times in a randomized complete block design. The non
treated check plots received no treatments. The pH of the spray water ranged from 6.4
to 6.6 and was not adjusted. A CO, pressurized hand sprayer boom was used to spray
two beds simultaneously. Except for the Condor OF treatment in 1992, wetting agents
were used. Leaf Act 80 [PureGro Co., West Sacramento, CA (0.58 liter/ha)] was used
with the emamectin benzoate treatments, and X-77 [Chevron Chemical Co., San
Francisco, CA (0.29 liter/ha)] was used for the rest of the treatments. Conventional
cultural practices were used for fertilization and weed control. Ten plants per plot (5
randomly selected plants in the center of each of the two middle rows) were examined
on each sampling date to determine numbers of larvae and pupae. Marketability was
determined at harvest for heads with wrapper leaves and for heads with no more than
three wrapper leaves removed. Percentages of marketable heads were based on rat
ings < 2 (Greene et al. 1969).
In 1992, seeds were planted on 24 January. Treatment plots were two beds wide (4
rows) and 7.62-m long with a 1.52-m nonplanted buffer zone between plots. Applica
tions were initiated when diamondback moth populations averaged < 1 larva per
plant. Treatments were applied eight times: 5, 17, and 27 March, 9, 16, and 30 April,
and 7 and 22 May. The spray boom had three nozzles over each bed: one centered over
Florida Entomologist 78(1)
each bed and one on each side of the row directed inward. Volume of water applied was
374 liter/ha for the first two sprays. Water volume was increased to 607 liter/ha be
ginning 25 March, and increased again to 748 liter/ha from 16 April until the last
spray on 22 May. Plots were sampled on 3, 10, 20, and 25 March, 1, 13, and 20 April,
and 5 and 19 May. Plants were harvested on 28 May.
In 1993, Diazinon 14G was applied and incorporated into the soil 15 days before
planting for wireworm control. Seeds were planted on 16 March. Applications began
when diamondback moth populations averaged slightly more than 1 larva per plant.
Treatment plots were four beds wide (8 rows) and 6.1-m long with a 1.52-m non
planted buffer zone between plots. Treatments were applied 7 times: 23 and 30 April,
6, 13, and 24 May, and 2 and 6 June. The spray boom had four nozzles over each bed:
one over each row and one on each side of the bed directed inward. Volume of water
applied was 374 liter/ha for the first two sprays. Water volume was increased to 607
liter/ha beginning 6 May, and increased again to 748 liter/ha from 24 May until the
last spray. Plots were sampled on 21 and 29 April, 5, 11, 20, and 26 May, and 8 and 16
June. Plants were harvested on 18 June. The majority of the insect pressure in both
trials was from diamondback moth. Very few southern armyworm, Spodoptera erida
nia (Cramer); beet armyworm, S. exigua (Hiibner); cabbage looper, Trichoplusia ni
(Hibner); and cutworms, probably Agrotis ipsilon (Hufnagel)and Feltia subterranea
(F.), were encountered during the experiment.
Statistical analysis
Data were subjected to analysis of variance [SAS System, Version 6.04 (SAS Insti
tute, Inc., Cary, NC)]. Insect count data from Belle Glade and Homestead were In (x
+ 1) transformed. All percentage data were transformed [ARCSIN (SQRT X)]. Means
were separated by Waller-Duncan K-ratio t-test, (K-ratio = 100).
RESULTS AND DISCUSSION
Sanford
Due to consistently low numbers of diamondback moth and the lack of correlation
between larval counts and marketability in past studies at CFREC-Sanford, the per
centage of plants with the bud (or head) and next 4 youngest leaves infested was used
to measure the activity of diamondback moth. This method was found to work well
when abundance was low and results correlated well with levels of damage at harvest
(G.L.L., unpublished data). We suggest that this method works because efficacious in
secticides prevent development to the adult stage, thus preventing oviposition on the
new growth in the sampling zone which eventually becomes the marketable portion
of the plant. In addition, we suggest that this method also works because there is very
little immigration from adjacent plots which may be producing adults.
Infestation levels increased steadily from 16% on 24 March to 98% on 12 May in
the nontreated check (Table 1). Weekly applications of emamectin benzoate resulted
in very low infestation levels (Table 1) and the highest percentage of marketable cab
bage (Table 2). Starting with emamectin benzoate and alternating every two applica
tions with two applications of XenTari also resulted in very low infestation levels
(Table 1) and a comparable percentage of marketable cabbage (Table 2). Starting with
XenTari and alternating every two applications with two applications of emamectin
benzoate resulted in significantly higher infestation levels and significantly (P <0.05)
less marketable cabbage than the opposite alternation pattern. This difference in ef
March, 1995
Leibee et al.: Diamondback Moth Control 87
7
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Florida Entomologist 78(1)
TABLE 2. EFFECTS OF INSECTICIDES ON MEAN PERCENT OF PLANTS WITH DAMAGE RAT
INGS < 3 AND < 4 IN MATURE HEAD CABBAGE AT CFREC-SANFORD, FL, 1992.
DAMAGE RATED ON A SCALE OF 1-6.
% Plants at Two Levels of Damage (SEM)2
Treatment Rate per Hectare' DR < 3 DR < 4
Nontreated 0 (0.0) d 2 (2.0) e
DiPel 2X 1.12 kg 2 (2.0) d 16 (8.1) e
XenTari 1.12 kg 32 (6.6) b 72 (6.6) be
MK-244 0.16 EC 0.0084 kg (AI) 62 (11.1) a 92 (5.8) a
XenTari R/ 1.12 kg
MK-244 0.16 EC3 0.0084 kg (AI) 20 (8.9) bc 44 (14.7) d
MK-244 0.16 EC R/ 0.0084 kg (AI)
XenTari4 1.12 kg 60 (7.1) a 86 (2.4) ab
XenTarif 1.12 kg 12 (4.9) c 56 (12.9) cd
'Rates expressed as formulated product unless otherwise indicated (AI).
2ANOVA performed on transformed (ARCSIN [SQRT %]) data. Nontransformed means presented. Means fol
lowed by the same letter within each column are not significantly different (P >0.05, Waller-Duncan K-ratio t
test, Kratio= 100).
ZAlternated every two applications starting with XenTari.
Alternated every two applications starting with MK-244 (emamectin benzoate).
'Third application skipped. Applied only water and X-77.
ficacy between the two alternation patterns may have been the result of the signifi
cantly (P <0.05) higher reduction in the level of infestation early (7 April) and late (5
May) in the treatment that started with emamectin benzoate. This was supported fur
their by the fact that the last two treatments in the alternation pattern that started
with emamectin benzoate was XenTari, which was the weaker of the two insecticides
when used alone. XenTari alone was the third most efficacious treatment based on
marketability and resulted in consistently low infestation levels. Using XenTari when
the infestation level exceeded 5% resulted in the elimination of only the third appli
cation. The percent infestation of diamondback moth did not differ significantly (P
>0.05) on any date between the XenTari treatments. However, the percentage of har
vested plants that were rated < 3 was significantly lower in the treatment where the
third application was skipped, suggesting that the third application was important in
maintaining control. Disappointing results with DiPel 2X strongly suggested that this
diamondback moth population was resistant to Btk, especially because Btk resistance
in diamondback moth has been documented in central Florida (Leibee & Savage
1992c, Shelton et al. 1993) and suspected in southern Florida (Jansson 1992).
Homestead
The numbers of diamondback moth were unusually high and peaked at 213.7 lar
vae and pupae per plant in the nontreated check on 16 March (Table 3). All treatments
prevented the high numbers that occurred in the nontreated check. Weekly applica
tions of emamectin benzoate and XenTari and the rotational treatment of these two
insecticides were most efficacious at reducing populations. All remaining treatments
March, 1995
Leibee et al.: Diamondback Moth Control 89
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Florida Entomologist 78(1)
were not very efficacious at reducing larval abundance on plants. Emamectin ben
zoate, XenTari, and their alternation were also the most efficacious at reducing dam-
age to cabbage plants and produced significantly higher (P <0.05) percentages of
marketable heads (Table 4). It is interesting to note that maintaining larvae and pu
pae to 1.0 or less per plant (emamectin benzoate used alone) resulted in only 74%
marketability. The diamondback moth population at Homestead was probably
Btk resistant because Bta (XenTari) was much more effective at reducing numbers
and damage than the Btk based insecticides. The addition of mevinphos to Cutlass
WP provided no significant (P >0.05) benefit over Cutlass WP alone. The addition of
a feeding stimulant (Konsume) to AC 513,696 produced a significant (P<0.05) reduc
tion in larval and pupal numbers over AC 513,696 alone on two dates (2 and 23
March). No significant (P >0.05) reduction of larval and pupal numbers occurred when
a feeding stimulant (Konsume) was added to Larvo-Bt. No benefit was observed from
the addition of the feeding stimulant to either insecticide based on damage rating and
marketability.
Belle Glade
1992 Trial. The numbers of diamondback moth were low (Table 5). Feeding dam-
age on the frame leaves was evident early in the trial. Feeding damage to the wrapper
leaves was not evident until the last three weeks of the trial. Diamondback moth den
TABLE 4. EFFECTS OF INSECTICIDES ON DAMAGE RATING (1-6) AND PERCENT MARKET
ABILITY OF CABBAGE AT TREC, HOMESTEAD, FL, 1992.
Damage Index per % Marketable
Treatment Rate per Hectare' Plant (SEM)2 Heads (SEM)2
Nontreated 5.1(0.1) a 3(1.8) c
AC 513,696 2X WP 1.12 kg 4.6(0.1) ab 17(3.8) bc
AC 513,696 48 LC 2.8 liters 4.6(0.1) ab 16(3.7) bc
Larvo-Bt LC 0.3 liter 4.6(0.1) ab 17(3.8) bc
Larvo-Bt LC + 0.3 liter
Konsume 7.0 liters 4.3(0.1) ab 21(4.2) bc
AC 513,696 48 LC + 2.8 liters
Konsume 7.0 liters 4.5(0.1) b 23(4.3) b
DiPel 2X 1.12 kg 4.0(0.1)b 32(4.8) b
MK-244 0.16 EC 0.0084 kg (AI) 2.7(0.1) c 74(4.5) a
XenTari 1.12 kg 2.8(0.1) c 75(4.4) a
MK-244 0.16 EC R/ 0.0084 kg (AI)
XenTari 1.12 kg 2.6(0.1) c 75(4.4) a
Mevinphos 4 EC + 0.56 kg (AI)
Cutlass WP 2.24 kg 4.3(0.1) b 21(4.2) bc
Cutlass WP 2.24 kg 4.6(0.1) ab 22(4.2) b
1Rates expressed as formulated product unless otherwise indicated (AI).
2Data subjected to ANOVA. Percentage marketable data were transformed (ARCSIN [SQRT %]). Nontrans
formed means presented. Means within the same column followed by the same letter are not significantly differ
ent (P >0.05, Waller-Duncan K ratio ttest, K ratio = 100).
March, 1995
Leibee et al.: Diamondback Moth Control 91
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Leibee et al.: Diamondback Moth Contol
sity did not average above one per plant until after 20 April. Therefore, data from the
last three sampling dates provide the best indicator of efficacy.
Emamectin benzoate, emamectin benzoate alternated with XenTari, XenTari,
mevinphos, and mevinphos in combination with DiPel 2X treatments produced the
lowest numbers of diamondback moth (Table 5) and the highest marketability (Table
6). The addition of DiPel 2X to esfenvalerate and thiodicarb produced cleaner plants
when compared with applications of the chemical insecticides alone. Mevinphos,
alone or in combination with DiPel 2X, was as efficacious as the emamectin benzoate
treatments at reducing numbers and increasing marketability. Thiodicarb alone and
esfenvalerate, alone and in combination with DiPel 2X, did not provide significant
control. Numbers of diamondback moth produced in these treatments were higher
than in the nontreated check in late season, and also the highest numbers produced
in the trial. Counts in the nontreated plots declined at the end of the trial, possibly be
TABLE 6. EFFECTS OF INSECTICIDES ON PERCENT MARKETABILITY OF GREEN CABBAGE
AT EREC, BELLE GLADE, FL, 1992.
% Marketability (SEM)2
Wrapper Leaves Wrapper Leaves3
Treatment Rate per Hectare' Attached Removed
Nontreated
Condor OF
MVP
MK-244 0.16 EC
R/ XenTari
MK-244 0.16 EC
Cutlass WP
XenTari
Javelin WG
DiPel 2X
Biobit FC
Thiodicarb 3.2 AF
Thiodicarb 3.2 AF
+ DiPel 2X
Esfenvalerate XL
Esfenvalerate XL
+ DiPel 2X
Mevinphos 4 EC
Mevinphos 4 EC
+ DiPel 2X
2.34 liters
4.67 liters
0.0084 kg (AI)
1.12 kg
0.0084 kg (AI)
2.24 kg
1.12 kg
1.12 kg
1.12 kg
3.5 liters
0.90 kg (AI)
0.90 kg (AI)
1.12 kg
0.055 kg (AI)
0.055 kg (AI)
1.12 kg
1.12 kg (AI)
1.12 kg (AI)
1.12 kg
8(4.8) d
28(9.5) cd
13(6.3) d
80(4.1) a
75(5.0) a
25(11.9) cd
33(13.8) cd
38(16.5) bcd
25(8.7) cd
18(6.3) d
8(4.8) d
53(14.9) abc
15(8.7) d
15(8.7) d
58(7.5) abc
68(7.5) ab
20(4.1) de
40(13.5) de
20(11.5) e
80(0.0) abc
85(11.9) a
35(6.5) de
60(17.8) a-d
50(13.5) b-e
45(15.0) cde
33(8.5) de
15(2.9)e
63(10.3) a-d
23(13.1) e
35(17.6) de
83(6.3) ab
88(6.3) a
1Rates expressed as formulated product unless otherwise indicated (AI).
2ANOVA performed on transformed (ARCSIN [SQRT %]) data. Nontransformed means presented. Means
within each column followed by the same letter are not significantly different (P >0.05, Waller Duncan K-ratio
ttest, Kratio= 100).
'Marketability rated again after removing no more than three wrapper leaves.
Florida Entomologist 78(1)
cause the plants were so badly damaged that they were no longer attractive to ovipos
iting females. Counts in the esfenvalerate and thiodicarb plots also declined at the
end of the trial.
The marketability of the heads before trimming (Table 6) appeared to be the best
criterion to separate treatments under these conditions of low insect pressure. Ema
mectin benzoate and emamectin benzoate alternated with XenTari provided the high
est percentage of marketable heads. DiPel 2X in combination with thiodicarb
provided slightly better control than did the Bt's alone before trimming. The low mar
ketability ratings for the esfenvalerate plots, even in combination with of DiPel 2X,
demonstrated the problems of season-long use of this pyrethroid.
The Bt-based insecticides performed poorly at this location. Few differences were
observed among the Btk based insecticides in their efficacy at reducing numbers of di
amondback moth and levels of marketability. Bta was comparable to the Btk based in
secticides in this test. Conditions other than insecticide resistance, such as the
lengthy intervals between the applications of the Bts, may have contributed, in part,
to the poor performance of the Bt-insecticides.
1993 Trial. Diamondback moth pressure was much higher in this trial. Pesticides
were applied more regularly except for a rainy period between 15 and 23 May. Popu
nations increased greatly over this period (Table 7). The greater population pressure
was probably responsible for the lack of differences in percent marketability among
treatments before or after wrapper leaves were removed. Therefore, only one set of
marketability values is presented in Table 8.
Emamectin benzoate provided excellent control and out-yielded all other treat
ments despite the 11 day break in treatments. Esfenvalerate provided good early sea
son control; however, it allowed numbers to rise to damaging levels in late season, an
observation also found in 1992. Surprisingly, methamidophos provided better control
than the Bt-based insecticides throughout most of the trial and yielded over 70% mar
ketable heads. Plants treated with DiPel 2X and XenTari supported low numbers of
diamondback moth in early season, but were severely damaged in late season and had
low marketability. XenTari provided better control than DiPel 2X in early season
when applied at regular weekly intervals.
In conclusion, emamectin benzoate alone and rotated with Bta was very efficacious
at controlling diamondback moth. A rotation strategy that started with emamectin
benzoate was more efficacious than one that started with Bta. The lower efficacy of
Btk based insecticides compared with that of Bta suggested that these populations
were developing resistance to Btk, but not to Bta, which concurs with Shelton et al.
(1993).
Given the history of resistance development in the diamondback moth and the doc
umentation of apparent low levels of resistance to Bta in Florida (Shelton et al. 1993),
complete reliance on Bta for control could result in the rapid development of resis
tance to Bta. For these reasons, resistance management programs for Bta and other
effective insecticides are needed to delay the onset of resistance. The use of rotation
strategies, as demonstrated in this study, should help to delay the development of re
distance to all insecticides used in a management program.
ACKNOWLEDGMENTS
We thank L. Finn, K. E. Savage, C. Eudell, C. Pickles, and S. H. Lecrone for their
assistance. This research was supported, in part, by Merck Research Laboratories,
Merck & Co. This is Florida Agricultural Experiment Station Journal Series No. R
03624.
March, 1995
Leibee et al.: Diamondback Moth Contol
TABLE 7. EFFECTS OF INSECTICIDES ON NUMBER OF DIAMONDBACK MOTH LARVAE AND
PUPAE PER PLANT AT EREC, BELLE GLADE, FL, 1993.
Sample Date
Apr 21 Apr 29 May 5 May 11
Rate per Mean (SEM)2 Diamondback Moth Larvae and
Treatment Hectare' Pupae per Plant
Nontreated 1.7(0.2) ns 0.9(0.2) bc 0.8(0.2) ab 5.2(0.3) a
XenTari 0.56 kg 2.1(0.2) 1.5(0.3) a 1.1(0.2) a 1.6(0.2) c
DiPel2X 1.12kg 1.5(0.2) 1.0(0.2) ab 1.1(0.2) a 4.7(0.8) b
MK2440.16EC 0.0084kg(AI) 1.4(0.2) 0.4(0.1) d 0.5(0.1) c 0.1(0.1) e
Methamidophos
4E 1.2 kg (AI) 1.6(0.2) 0.6(0.1) cd 0.6(0.1) bc 0.5(0.1) d
Esfenvalerate XL 0.055 kg (AI) 1.6(0.2) 0.5(0.1) d 0.4(0.1) c 1.6(0.2) c
May 20 May 26 Jun 8 Jun 16
Nontreated 15.9(1.5) a 41.2(6.0) a 6.3(1.0) b 0.8(0.3) d
XenTari 0.56 kg 13.5(1.6) b 24.0(2.4) b 3.4(0.6) c 2.0(0.4) b
DiPel2X 1.12kg 15.6(2.3) b 29.1(3.7) ab 3.1(0.7) c 1.5(0.3) bc
MK244 0.16EC 0.0084kg (AI) 1.2(0.3) d 3.7(1.1) d 0.8(0.3) d 0.7(0.2) d
Methamidophos
4E 1.12 kg (AI) 7.1(0.9) c 8.8(1.3) c 0.5(0.2) d 1.1(0.3) cd
Esfenvalerate XL 0.055 kg (AI) 11.3(1.3) b 21.2(2.1) b 32.8(7.0) a 11.8(3.2) a
'Rates expressed as formulated product unless otherwise indicated (AI).
2ANOVA performed on In (x + transformed data. Nontransformed means presented. Means within each col
umn followed by the same letter are not significantly different (P >0.05, Waller-Duncan Kratio ttest, Kratio
100).
TABLE 8. EFFECTS OF INSECTICIDES ON PERCENT MARKETABILITY OF GREEN CABBAGE
AT EREC, BELLE GLADE, FL, 1993.
Treatment Rate per Hectare' % Marketability (SEM)2
Nontreated 11(0.7) e
XenTari 0.56 kg 45(0.5) c
DiPel 2X 1.12 kg 23(0.9) d
MK 244 0.16 EC 0.0084 kg (AI) 98(0.2) a
Methamidophos 4 E 1.12 kg (AI) 73(0.5) b
Esfenvalerate XL 0.055 kg (AI) 15(0.4) de
'Rates expressed as formulated product unless otherwise indicated (AI).
2ANOVA performed on transformed (ARCSIN [SQRT %]) data. Nontransformed means presented. Means
within each column followed by the same letter are not significantly different (P >0.05, Waller Duncan Kratio
ttest, K ratio= 100).
Florida Entomologist 78(1)
LITERATURE CITED
GREENE, G. L., W. G. GENUNG, R. B. WORKMAN, AND E. G. KELSHEIMER. 1969. Cab
bage looper control in Florida a cooperative program. J. Econ. Entomol. 62:
798-800.
LEIBEE, G. L., AND K. E. SAVAGE. 1992a. Evaluation of selected insecticides for control
of diamondback moth and cabbage looper in cabbage in central Florida with ob
servations on insecticide resistance in the diamondback moth. Florida Ento
mol. 75: 585-591.
LEIBEE, G. L., AND K. E. SAVAGE. 1992b. Toxicity of selected insecticides to two labo
ratory strains of insecticide-resistant diamondback moth (Lepidoptera:Plutel
lidae) from central Florida. J. Econ. Entomol. 85: 2073-2076.
LEIBEE, G. L., AND K. E. SAVAGE. 1992c. Observations on insecticide resistance in di
amondback moth, pp. 41-46 in Seminar Proceedings: Global Management of
Insecticide Resistance In The 90s. Abbott Laboratories, Chicago, IL.
JANSSON, R. K. 1992. Integration of an insect growth regulator and Bacillus thuring
iensis for control of diamondback moth, pp. 147-156 in N. S. Talekar [ed.], Dia
mondback moth and other crucifer pests: Proceedings of the second
international workshop, December 10-14, 1990, Tainan, Taiwan. Publication
92-368, Asian Vegetable Research and Development Center, Taipei.
SHELTON, A. M., J. L. ROBERTSON, J. D. TANG, C. PEREZ, S. D. EIGENBRODE, H. K.
PREISLER, W. T. WILSEY, AND R. J. COOLEY. 1993. Resistance of diamondback
moth (Lepidoptera: Plutellidae) to Bacillus thuringiensis subspecies in the
field. J. Econ. Entomol. 86: 697-705.
TALEKAR, N. S. [ed.]. 1986. Diamondback moth management: proceedings of the first
international workshop, March 11-15, 1985, Tainan, Taiwan. Publication 86
248, Asian Vegetable Research and Development Center, Shanhua, Taiwan.
4444444444444444444444444444444444444444444444444444
March, 1995
Florida Entomologist 78(1)
ATTRACTION OF FEMALE CABBAGE LOOPER MOTHS
(LEPIDOPTERA: NOCTUIDAE) TO MALES IN THE FIELD
PETER J. LANDOLT
United States Department of Agriculture, Agriculture Research Service,
1700 SW 23rd Dr., Gainesville, FL 32604
ABSTRACT
Live male cabbage looper moths, Trichoplusia ni (Hubner), used to bait traps in
cotton fields, attracted conspecific males and females which were captured in the
bucket traps. Females captured in traps baited with males included unmated individ
uals as well as mated ones, with up to 7 spermatophores in the bursa copulatrix. Cab
bage looper moths arrived at cages of males in cotton primarily during the first three
hours of the night, beginning at dusk.
Key Words: Trichoplusia ni, sex pheromone, traps
RESUME
Los machos vivos de la polilla de la col, Trichoplusia ni (Hubner), usados para ce
bar trampas en campos de algod6n, atrajeron machos y hembras conespecificos que
fueron capturados en trampas de cubeta. Las hembras capturadas en las trampas ce
This article is from Florida Entomologist Online, Vol. 78, No. 1 (1995).
FEO is available from the Florida Center for Library Automation gopher (sally.fcla.ufl.edu)
and is identical to Florida Entomologist (An International Journal for the Americas).
FEO is prepared by E. O. Painter Printing Co., P.O. Box 877, DeLeon Springs, FL. 32130.
March, 1995
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