medal et al.: predation of spissistilus festinus 561...

Medal et al.: Predation of

Spissistilus festinus 561

DEVELOPMENTAL STAGES OF

SPISSISTILUS FESTINUS

(HOMOPTERA: MEMBRACIDAE) MOST SUSCEPTIBLE TO HEMIPTERAN PREDATORS

J. C. M

EDAL

1

, A. J. M

UELLER

1

, T. J. K

RING

1

A

ND

E. E. G

BUR

, J

R

.

2

1

University of Arkansas, Department of Entomology, Fayetteville, AR 72701

2

University of Arkansas, Agricultural Statistics LaboratoryFayetteville, AR 72701

A

BSTRACT

The developmental stages of

Spissistilus

festinus

most susceptible to predation byyoung female adults of

Geocoris punctipes

and

Nabis roseipennis

and to

Orius

insid-iosus

of undetermined age and sex was determined in the laboratory. With

G. puncti-pes

, the highest

S. festinus

mortality (90-100%) occurred in the early (1st, 2nd)nymphal stages while

Nabis roseipennis

attacked all nymphal stages equally well. Ingeneral,

O. insidiosus

did not feed on

S. festinus

. This study suggests that

S. festinus

nymphs are potential prey for

G. punctipes

and

N. roseipennis

in the field.

Key Words:

Geocoris punctipes, Nabis roseipennis,

biological control.

R

ESUMEN

En pruebas de laboratorio fueron determinados los estados de desarrolo de

Spis-sistilus festinus

más susceptibles a la depredación por hembras adultas de

Geocorispunctipes

y

Nabis roseipennis

así como por

Orius insidiosus

de edad y sexo indetermi-nados. Con

G. punctipes

, la mortalidad de

S. festinus

más alta (90-100%) ocurrió en losestados ninfales tempranos (1

°

y 2

°

) mientras

N. roseipennis

atacó todos los estadosninfales de la misma manera. En general,

O. insidiosus

no se alimentó de

S. festinus

.Este estudio sugiere que las ninfas de

S. festinus

son presa potencial de

G. punctipes

y

N. roseipennis

en el campo.

The threecornered alfalfa hopper,

Spissistilus festinus

(Say), is considered a pest ofeconomic importance in soybean,

Glycine max

(L.), and other legume crops in severalsoutheastern states. Researchers in Arkansas (Mueller & Dumas 1975) and Louisi-ana (Sparks & Newson 1984, Sparks & Boethel 1987) report yield losses resultingfrom feeding by adults and nymphs of this pest. The main damage is caused when thebase of the main stem is girdled resulting in dead or weakened plants.

The importance of entomophagous arthropods in preventing the increase of lepi-dopterous pest populations in field crops, including soybean, has long been recognized(Lopez et al. 1976, Lawrence & Watson 1979, Richman et al. 1980). A parasitoid (Jor-dan 1952, Herting & Simmonds 1972) and several predators (Spurgeon 1992) of

S. fes-tinus

have been reported. Polyphagous predators such as

Geocoris spp.

,

Nabis spp

.,and

Orius insidiosus

(Say), which are frequently abundant in many soybean-growingareas of the United States (Roach 1980, Barry 1973, Bell & Whitcomb 1963), may sup-press

S. festinus

populations in soybeans. However, the impact of predators on this in-sect pest has not been evaluated.

562

Florida Entomologist

78(4) December, 1995

A laboratory study was designed to determine the developmental stages of

S. fes-tinus

most susceptible to predation by adults of

Geocoris punctipes

(Say),

Nabisroseipennis

Reuter, and

O. insidiosus

.

M

ATERIALS

A

ND

M

ETHODS


were obtained from a laboratory colony maintained on

Phaseolus vulgaris

L. pods at 26

°

±

1 C, 70 to 80% RH, and a photoperiod of 14:10(L:D). The colony was revitalized periodically with field-collected adults to overcomeadverse selection effects of laboratory rearing.

Nymphs of

G. punctipes

and

N. roseipennis

were collected with sweep nets in al-falfa,

Medicago sativa

L., fields in southwestern Arkansas during the spring-summerof 1992. They were fed in the laboratory until the adult stage on second instar soybeanlooper,

Pseudoplusia includens

(Walker). Green bean pods were also provided.

Oriusinsidiosus

adults of undetermined age and sex were collected from an alfalfa field atthe University of Arkansas experimental farm at Fayetteville. Before the experiment,

O. insidiosus

were fed

Helicoverpa zea

(Boddie) eggs and green bean pods. The threeto five-week-old female

G. punctipes

and

N. roseipennis

and adult

O. insidiosus

werestarved for 24h before the experiment.

Potted V2 soybean plants (CV:Bragg) were covered by cages and placed in an en-vironmental chamber at 25

°

±

1 C, 60% RH and a photoperiod of 14:10 (L:D). Cageswere made by cutting off both ends of two-liter clear plastic soda bottles and gluing ascreen cloth at the top end to allow air movement. The soil at the base of the plantswas covered with a brown-paper disc to facilitate finding dead insects. The base of thecage in contact with the soil was sealed by placing tape around the bottom of the cageand the upper rim of the pot.

A completely randomized design with 10 replications was used. Treatments werethree predator species (

G. punctipes, N. roseipennis,

and

O. insidiosus

) and six

S. fes-tinus

developmental stages (nymphal instars 1-5 and adult).


eggswere not tested. One starved adult predator was placed with one

S. festinus

of a singledevelopmental stage (1 predator vs. 1 prey) on a potted soybean plant. Cages contain-ing only plant and prey with no predator served as controls. Mortality was recordedafter 24 h. Any dead

S. festinus

were assumed to have been killed by the predator.Mortality of

S. festinus

was not adjusted for the control because of low (<5%) mortalityin controls. Values of proportion dead were analyzed using a Chi-square test. Meanswere compared by a two-sample binomial test (Ott 1984).

R

ESULTS

AND

D

ISCUSSION

Significant differences in percentage mortality among the

S. festinus

developmen-tal stages between

G. punctipes

and

N. roseipennis

were observed (Chi-square=9.52,df=4, P<0.05).

Orius insidiosus

fed minimally (10% mortality) on the first nymphalstage and did not feed on larger nymphal or adult

S. festinus

stages. Values for

O. in-sidiosus

were not included in the Chi-square test because of the low frequency of mor-tality (<1) observed for all prey developmental stages. These results suggest that

Orius insidiosus

is probably not an important predator of

S. festinus

in nature. Thehighest

S. festinus

mortality (100%) was observed when first instars were exposed to

G. punctipes

(Table 1). This mortality was not significantly different (P=0.05, two-sample binomial test) from the mortality (90%) obtained when second and thirdnymphal stages were exposed to

G. punctipes

and N.

roseipennis

predators, respec-tively.

Nabis roseipennis

attacked all nymphal stages equally well (P=0.05, two-sam-

Medal et al.: Predation of

Spissistilus festinus 563

ple binomial test).

Nabis roseipennis

was the only predator that fed on adult

S.festinus

(10% killed).

Geocoris punctipes

caused the highest mortality of nymphal instars (first throughthird), which are probably the most susceptible to attack (Table 1). Crocker & Whit-comb (1980) found that the largest percentage (79%) of target prey captured undernatural conditions by

Geocoris spp

. are those that remain passive during physical con-tact with the predator. Early and intermediate nymphal stages are probably not ableto adequately defend themselves and their strategy of remaining motionless for cer-tain periods of time is not an effective behavior for avoiding predation. The lower pre-dation on fourth and fifth instars by

G. punctipes

can be attributed to the more activephysical movements of the prey during predator-prey encounters and to their morewell-developed spines. Further biological studies on prey-predator interactions underlaboratory and field conditions will provide basic information for developing predic-tive models on population dynamics of pests and natural enemies that can be used inpest management programs. These studies indicate that because

G. punctipes

and

N

.

roseipennis

fed on

S. festinus

nymphs in the laboratory they are potential predatorsfor this pest in nature.

A

CKNOWLEDGMENT

We thank D. T. Johnson, W. C. Yearian and S. Y. Young (Department of Entomology,University of Arkansas) for reviewing the manuscript. This research was supported inpart by an Arkansas Soybean Promotion Board grant. Article published with the ap-proval of the Director, Arkansas Agricultural Experiment Station, University of Ar-kansas, Fayetteville, manuscript No. 95002.

R

EFERENCES

C

ITED

B

ARRY

, R. M. 1973. A note on the species composition of predators in Missouri soy-beans. J. Georgia Entomol. Soc. 80: 284-286.

B

ELL

, K. O.,

AND

W. H. W

HITCOMB

. 1963. Field studies on egg predators of the bollworm,

Heliothis zea

. Florida Entomol. 47: 171-180.C

ROCKER

, K. O.,

AND

W. H. W

HITCOMB

. 1980. Feeding niches of the big-eyed bugs

Geo-coris bullatus

,

G. punctipes

and

G.

uliginosus

(Hemiptera: Lygaeidae). Environ.Entomol. 9: 508-513.

T

ABLE

1. P

ERCENT

M

ORTALITY

OF

N

YMPHAL

S

TAGES

OF

S

PISSISTILUS

FESTINUS

DUETO

P

REDATORS

.

Prey Developmental Stage

Predator N1 N2 N3 N4 N5 Adult

Geocoris

100 a

1

90 ab 60 b 10 cd 0 d 0 d

Nabis

60 b 60 b 90 ab 50 bc 50 bc 10 cd

Orius

2

10 0 0 0 0 0

1

Values followed by the same letter do not differ at the 0.05 probability level using a two-sample binomial testfor equal proportions. Comparisons were carried out between

Geocoris

and

Nabis

predators and prey stageswithin predator species indicated.

2

Values for

Orius

were not included in the Chi-square test because of the low frequency of mortality (<1) ob-served.

564 Florida Entomologist 78(4) December, 1995

HERTING, B., AND F. J. SIMMONDS. 1972. A catalogue of parasites and predators of ter-restrial arthropods. Section A. Host or prey/enemy. Vol. II. Homoptera. CIBC.210 p.

JORDAN, C. R. 1952. The biology and control of the threecornered alfalfa hopper, Spis-sistilus festinus (Say). Ph.D. dissertation, Texas A&M University, College Sta-tion.

LAWRENCE, R. K., AND T. F. WATSON. 1979. Predator-prey relationship of Geocorispunctipes and Heliothis virescens. Environ. Entomol. 2: 245-248.

LOPEZ, J. D., R. L. RIDGWAY, AND R. E. PINNELL. 1976. Comparative efficacy of four in-sect predators of the bollworm and tobacco budworm. Environ. Entomol. 5:1160-1164.

MUELLER, A. J., AND B. A. DUMAS. 1975. Effects of stem girdling by the threecorneredalfalfa hopper on soybean yields. J. Econ. Entomol. 4: 511-512.

OTT, L. 1984. An introduction to statistical methods and data analysis. DuxburyPress. Boston. 775 p.

RICHMAN, D. B., R. C. HEMENWAY, AND W. H. WHITCOMB. 1980. Field cage evaluationof predators of the soybean looper, Pseudoplusia includens (Lepidoptera: Noc-tuidae). Environ. Entomol. 3: 315-317.

ROACH, S. H. 1980. Arthropod predators on cotton, corn, tobacco, and soybeans inSouth Carolina. J. Georgia. Entomol. Soc. 15: 131-138.

SPARKS, A. N., AND D. J. BOETHEL. 1987. Late-season damage to soybean by threecor-nered alfalfa hopper (Homoptera: Membracidae) adults and nymphs. J. Econ.Entomol. 80: 471-477.

SPARKS, A. N., AND L. D. NEWSOM. 1984. Evaluation of the pest status of Spissistilusfestinus (Say) (Homoptera: Membracidae) on soybean in Louisiana. J. Econ.Entomol. 77: 1553-1558.

SPURGEON, D. W. 1992. Threecornered alfalfa hopper (Homoptera: Membracidae) onsoybean: Insect-plant interactions. Ph.D. dissertation, University of Arkansas,Fayetteville.

Osborne et al.: Ant Predation on Mites

565

PREDATION BY

TAPINOMA MELANOCEPHALUM

(HYMENOPTERA: FORMICIDAE) ON TWOSPOTTED SPIDER

MITES (ACARI: TETRANYCHIDAE) IN FLORIDA GREENHOUSES

L

ANCE

S. O

SBORNE

1

, J. E. P

EÑA

2

AND

D

AVID

H. O

I

3

1

Central Florida Research and Education Center,University of Florida, IFAS

2807 Binion RoadApopka, FL 32703

2

Tropical Research and Education Center,University of Florida, IFAS

18905 SW 280 Street,Homestead, FL 33031

3

Department of Entomology301 Funchess Hall

Auburn University, AL 36849

A

BSTRACT

Natural infestations of

Tapinoma melanocephalum,

(Fab.) found in central Flor-ida greenhouses were observed attacking

Tetranychus urticae

Koch in test evalua-tions of two chemicals. Subsequent laboratory tests using isolated leaf discs,greenhouse data, and whole plants demonstrated that

T. melanocephalum

is a signif-icant predator of

T. urticae

.

Key Words: Biological control, ants, spider mites.

R

ESUMEN

Durante la evaluación de dos productos químicios en invernaderos de la regióncentral de la Florida fueron encontradas infestaciones naturales de

Tapinoma mela-nocephalum

(Fab.) atacando

Tetranychus urticae

Koch.Las pruebas de laboratorio realizadas posteriormente usando discos de hojas, da-

tos de invernadero y plantas completas demostraron que

T. melanocephalum

es un de-

predador significativo de

T. urticae.

The first report of movement of beneficial insects to control a pest insect was byForskål (1775) who reported that date palms in the Middle East were protected frompests by ants. Annually, colonies of predatory ants were moved from the mountainsinto infested areas. Groff & Howard (1924) stated that chinese citrus growers ofKwangtung province would commonly use colonies of the cultured ant,

Oecophyllasmaragdina

Fab., as predators for citrus pests.Ants found in greenhouses are generally treated as pests because they tend

aphids, mealybugs or soft scales or they are of quarantine importance (i.e., red im-ported fire ants,

Solenopsis invicta

Buren). In almost all cases, we have traditionallyrecommended the use of a pesticide to kill the pest insect being tended by the ants or,

566



specifically, to kill the ants. Ants are not thought of as biological control agents ingreenhouses, rather, they are considered disruptive to biological control of various ho-mopterous pests.

One species of ant that can be found in greenhouses is

Tapinoma melanocephalum

(Fab.). This species is considered a nuisance ant and occasionally an important pest inhouses. Field populations are found in south Florida but are limited to greenhousesand buildings in the north (Nickerson & Bloomcamp 1988). This tropical species hasbeen so widely distributed by commerce that it is difficult to determine its origin, butit is believed to be African or Oriental (Smith 1965). The workers are monomorphicand approximately 1 mm long. The worker head and thorax are black, legs and abdo-men and gastor are clear or light yellow. Colonies of this highly adaptable species con-tain multiple queens (polygyny) and are often found in transient habitats, such asplant debris, under potted plants, rotting wood planks and plant stems (Nickerson &Bloomcamp 1988). Colonies may break into subunits that occupy different sites, butindividual ants will move between them (Oster & Wilson 1978).

Smith (1965) reported that

T. melanocephalum

fed on many different foods in thehouse, but seemed to prefer sweets. In the greenhouse, she reported that they fed onhoneydew and on live or dead insects. Nickerson & Bloomcamp (1988) noted that acolony of

T. melanocephalum

had established in the quarantine greenhouse of theFlorida Department of Agriculture in Gainesville, Florida, where it preyed on smallbeetle larvae and lepidopterous larvae from the insect cultures in quarantine. In Ven-ezuela,

T. melanocephalum

is the primary predator of eggs of

Rhodnius prolixus

Stål(Gomez-Nunez 1971). The only report of this ant interacting with Arachnida was byShepard & Gibson (1972) who reported that a symbiotic relationship had developed inCosta Rica between

T. melanocephalum

and jumping spiders (Araneae: Salticidae)which were found inhabiting the nests. It is believed that the spiders provided someprotection to the ants from natural enemies and the nest served as a foundation forweb construction.

In this paper, we report chemical evaluations conducted in 1993 for control oftwospotted spider mites,

Tetranychus urticae

Koch, in the University of Florida-Apo-pka greenhouses. The tests results led us to the conclusion that mite numbers de-clined significantly on both treated and untreated plants because of predation by

T.melanocephalum

. This paper describes this preliminary experiment and other tests todefine the interaction between

T. urticae

and

T. melanocephalum

.

M

ATERIALS

AND

M

ETHODS

Pesticide Trials

Salvia splendens

cv. Red Hot Sally seedlings were potted into 15.2-cm round plas-tic pots using Verlite Nursery Mix A (without superphosphate; Verlite Co. Tampa, FL)amended with 4.4 kg Osmocote (19:6:12 slow release fertilizer; Grace-Sierra ChemicalCo., Milpitas, CA), 4.2 kg dolomite, and 0.9 kg Micromax per m

3

(micronutrient source;Grace-Sierra Chemical Co.). The pots were placed on raised benches in a glass green-house. Forty plants were infested on September 16, 1993 with twospotted spidermites (TSM) by placing pieces of infested Henderson Bush lima bean (

Phaseolus li-mensis

Macfady) leaves on each plant. An initial count of all TSM stages on twomarked leaves per plant was conducted and five plants were assigned to each of fivetreatments. Additional counts were conducted five days later. The five treatmentswere: three with an experimental formulation containing neem oil supplied to us un-der a non-disclosure agreement (UK-1%, UK-1.5%, UK-2%), the labeled rate of a stan-dard acaricide (Pentac Aquaflow

®

- dienochlor) and an untreated control.


567

Disc Trials

Henderson bush lima bean seeds were planted into 12.7-cm square black plasticpots using the same soil described above. Five 20-mm diam discs were cut from ma-ture leaves and placed on the bottoms of 10 cm

2

plastic-petri dishes filled with moistcotton. The pattern of placement was one disc at each corner of a square for the firsttest; for the second and third tests one additional disc (total=5) was placed in the cen-ter of this pattern. Five adult female TSM were placed on each disc. Two dishes wereprepared for each experiment. Half the dishes were individually isolated by placingthem in a saucer on an inverted 10-cm square plastic pot sitting in a second saucerfilled with soapy water. This served as an efficient method to prevent ants from ob-taining access to mites on these discs. The remaining dishes were placed on a green-house bench on which worker ants were observed foraging. The number of live TSM(all stages) were counted on each leaf on days 1, 2, 3, and 6. This study was repeatedthree times. All data from each test were pooled and the median number of mites perdisc for each treatment was compared using Mann-Whitney Rank Sum Test (SigmaS-tat version 1.01; Jandel Scientific, San Rafael, CA, 1994).

Whole Plant Trials

Twenty Henderson bush lima bean seeds were planted into 12.7-cm square blackplastic pots using the same soil previously described. When the first true leaves werefully expanded (two-leaf stage), each plant was infested with 10 adult female TSM perleaf by hand with a camel-hair brush. Ten plants were individually isolated by placingeach pot in a saucer on an inverted 10-cm square plastic pot resting in a second saucerfilled with soapy water. This served as an efficient method to prevent ants from forag-ing on these test plants. The remaining 10 plants were placed on a greenhouse benchon which worker ants were observed foraging.

The numbers of live TSM (all stages) were counted on each leaf on day 7, 11, 14,18, and 22. This study was repeated three times. All data from each test were pooledand the median number of mites per leaf for each treatment was compared usingMann-Whitney Rank Sum Test (SigmaStat version 1.01; Jandel Scientific, SanRafael, CA, 1994).

T

ABLE

1. C

OMPARISON

OF

T

HREE

R

ATES

OF

N

EEM

O

IL

,

A

M

ITICIDE

S

TANDARD

AND

N

ON

-

TREATED

C

ONTROL

FOR

THE

C

ONTROL

OF

T

ETRANYCHUS

URTICAE

ON

S

ALIVA

SPLENDENS

CV

. R

ED

H

OT

S

ALLY

S

EEDLINGS

(M

EAN

±

SE

FOR

TSM/2L

EAVES

/P

LANT

).

Treatment Pre-count 7-Day Count 14-Day Count

UK-1.0%

1

51.4

±

13.0

2

32.2

±

28.7 1.6

±

1.4UK-1.5% 51.0

±

13.4 34.8

±

11.7 12.0

±

4.9UK-2.0% 51.2

±

12.9 47.8

±

16.1 34.2

±

14.7Dienochlor 51.0

±

12.6 15.0

±

6.9 0.0

±

0.0Control 43.8

±

19.1 11.2

±

6.9 0.0

±

0.0

1

This experiment consisted of five treatments, three with an experimental neem oil formulation of unknowncomposition and supplied to us under a non-disclosure agreement (UK-1%, UK-1.5%, UK-2%), the labeled rateof a acaricide standard (Pentac Aquaflow

®

-dienochlor) and an untreated control.

568



R

ESULTS

AND

D

ISCUSSION

Pesticide Trials

The results of the pesticide trials were contrary to those expected for a standardpesticide efficacy study (Table 1), because mite numbers on

all

treatments declinedcompared to the initial counts. In the three treatments where neem oil was applied, thenumber of mites increased with the concentration applied. These results prompted usto inspect all plants for the presence of predatory mites. No phytoseiid mites werefound on any treatments. We did notice a significant number of ants on many plants inthis study and on closer observation we found worker ants leaving plants with mites,adult whiteflies, thrips and immature aphids in their mandibles. This observationprompted us to conduct the disc and individual plant studies reported below.

Disc Trials

Results of the disc tests are presented in Fig. 1. Number of mites on each disc weresignificantly different (P<0.01; Mann-Whitney Rank Sum Test) on days 1, 2, 3, and 7.

Figure 1. A comparison of the number of mites (mean ± SE) per leaf disc when antswere allowed to forage versus when they were excluded; plotted against time (day 1,2, 3, and 7).


569

Worker ants were observed walking across the wet cotton substrate used to maintainthe disc and prevent mites from escaping. They were never observed carrying eggs;however, they were seen removing other stages of

T. urticae

from these discs. No antswere observed on the isolated treatments. It appeared that the ants were able to moveacross the moist cotton, find the mites, and remove them within 24 h from the time thedishes were placed in the infested greenhouse.

Whole Plant Trials

Results of the individual plant tests are presented in Fig. 2. Numbers of mites oneach leaf were significantly different (P<0.01; Mann-Whitney Rank Sum Test) on days7, 11, 14, 18, and 22. Ants were observed foraging on the exposed plants after 1 day ofexposure. Numbers of mites increased until day 11 after which the population de-clined to a very low level. The age distribution of surviving mites changed throughoutthe course of this study. Initially, the active stages were mainly adult females butmost of the mites counted after day 14 were nymphs or newly hatched larvae. We

Figure 2. A comparison of the number of mites (mean ± SE) per leaf when antswere allowed to forage versus when they were excluded; plotted against time (day 7,11, 14, 18, and 22).

570



never observed a reduction in the numbers of mite eggs nor did we observe ants re-moving eggs from the discs or whole plants.

T. melanocephalum

is usually considered to be a pest because of its impact on mitecolonies and its disruptive effect on experiments by feeding on the mites in controls.Results of these studies show that

T. melanocephalum

can be a significant predator oftwospotted spider mites; however, there are several important questions that must beaddressed before employing these ants as predators in a commercial setting. Exten-sive studies should be conducted to learn what foods they will feed on under green-house conditions. This would include extensive host range studies to determine if theypose any threat to ornamental plants. Because we have observed

T. melanocephalum

feeding on a number of other arthropod prey, we also must determine if they have apreference when given the option of feeding on a array of different prey. Secondly, wewould like to determine if

T. melanocephalum

only feed on twospotted spider miteswhen other food sources are scarce. We have noticed that they will feed on westernflower thrips and

Ecinothrips americanus

when no aphids or spider mites are present,but when these hosts are in sufficient numbers the ants seem not to attack thrips.

The final step would be to determine their sensitivity to pesticides so that theycould be eradicated from a greenhouse if necessary, or to prevent their movement inor on ornamental plants.

T. melanocephalum

is considered a “fugitive” or opportunis-tic ant (Hölldobler & Wilson 1990) and its status as an urban pest cannot be ignored.Because this ant can infest potted plant material, cardboard boxes, and other mate-rial commonly used to ship plants, it may be necessary to develop management pro-grams for control.

A

CKNOWLEDGMENTS

We wish to extend our appreciation to Drs. R. K. Yokomi, G. L. Leibee and F. L.Petitt for their critical review of this work. This is Florida Experiment Station JournalSeries No. R-04739.

R

EFERENCES

C

ITED

F

ORSKÅL

, P. 1775. Descriptiones animalium, avium, amphibiorum, piscium, insecto-rum, vermium: quae in itinere orientali observavit P. Forskål, post mortem auc-toris edidit Carsten Niebuhr. Hauniae, Moeller (Pt. 3).

G

OMEZ

-N

UNEZ

, J. C. 1971.


as an inhibitor of

Rhodniusprolixus

populations. J. Med. Entomol. 8: 735-737.G

ROFF

, G. W.,

AND

C. W. H

OWARD

. 1924. The cultured citrus of south China. LingnanAgr. Rev. 2: 108-14.

H

ÖLLDOBLER

, B.,

AND

E. O. W

ILSON

. 1990.

The Ants.

Belknap Press of Harvard Uni-versity Press, Cambridge, Mass. 732 pp.

N

ICKERSON

, J. C.,

AND

C. L. B

LOOMCAMP

. 1988.


(Fabri-cius) (Hymenoptera: Formicidae). Entomol. Cir. No. 307. Florida Dept. Agric. &Consumer Serv. Div. of Plant Industry. Gainesville, FL. 2 p.

O

STER

, G. F.,

AND

E. O. W

ILSON

. 1978. Caste and Ecology in the Social Insects. Prin-ceton Univ. Press, Princeton, New Jersey. 352 p.

S

HEPARD

, M.,

AND

F. G

IBSON

. 1972. Spider-ant symbiosis: Cotinusa spp. (Araneida:Salticidae) and


(Hymenoptera: Formicidae). Cana-dian Entomol. 104: 1951-1954.

S

MITH

, M. R. 1965. House-investing ants of the eastern United States; their recogni-tion, biology, and economic importance. USDA-ARS Tech. Bull. 1326. 105 p.

Robacker: Attractant for Mexican Fruit Fly

571

ATTRACTIVENESS OF A MIXTURE OF AMMONIA, METHYLAMINE AND PUTRESCINE TO MEXICAN FRUIT FLIES (DIPTERA: TEPHRITIDAE) IN A CITRUS ORCHARD

D

AVID

C. R

OBACKER

Crop Quality and Fruit Insects ResearchAgricultural Research Service, U.S. Department of Agriculture

2301 S. International Blvd.Weslaco, TX 78596

A

BSTRACT

A mixture of ammonium bicarbonate or ammonium carbonate, methylamine HCland putrescine (AMPu) was evaluated for attractiveness to gamma-irradiated Mexi-can fruit flies,

Anastrepha ludens

(Loew), in a citrus orchard in 1-day tests. AMPu(10:10:1 mixture of ammonium bicarbonate:methylamine HCl:putrescine) was testedboth in dilute aqueous solutions in the reservoir of McPhail traps and in more concen-trated form in polypropylene tubes suspended in McPhail traps or fastened to yellowsticky ball traps. The most attractive concentration of AMPu used in aqueous solutioncaptured only half as many flies as Torula yeast in McPhail traps. AMPu (6:10:1 mix-ture of ammonium carbonate:methylamine HCl:putrescine) formulated into agar andtested in tubes fastened to sticky ball traps captured as many male and female fliesas Torula yeast in McPhail traps.

Key Words:

Anastrepha ludens

, trapping, lures, amines.

R

ESUMEN

Fue evaluada la atractividad de una mezcla de bicarbonato de amonio o carbonatode amonio, metilamina HCl y putrescina (AMPu) sobre moscas mexicanas de la frutagamma-irradiadas,

Anastrepha ludens

(Loew), en un campo de cítricos en pruebas deun día de duración. La mezcla AMPu (mezcla de 10:10:1 de bicarbonato de amonio:me-tilamina HCl:putrescina) fue probada en soluciones acuosas diluídas en el reservoriode trampas de McPhail y en forma más concentrada en tubos de polipropileno suspen-didos en trampas de McPhail o atados a trampas pegajosas de bolas amarillas. La con-centración más atractiva de AMPu, usada en solución acuosa, capturó solamente lamitad de las moscas capturadas con levadura Torula en las trampas de McPhail. Lamezcla AMPu (mezcla de 6:10:1, de carbonato de amonio:metilamina HCl:putrescina)fromulada en agar y probada en tubos atados a trampas pegajosas de bola capturó

tantos machos y hembras como la levadura Torula en las trampas de McPhail.

Recently, I reported on development of a three-component attractant (AMPu) forthe Mexican fruit fly (

Anastrepha ludens

(Loew)) containing metabolites from biolog-ical degradation of amino acids (Robacker & Warfield 1993). AMPu was more attrac-tive than Torula yeast, the most commonly used bait for Mexican fruit fly, in flightchamber tests in a greenhouse. This research was analogous to work by Wakabayashi& Cunningham (1991) with the melon fly (

Bactrocera cucurbitae

(Coquillett)). Morerecently, Heath et al. (1995) have reported on a similar attractant for the Mediterra-nean fruit fly (

Ceratitis capitata

(Wiedemann)) and the Mexican fruit fly. The purpose of the current research was to evaluate the initial attractiveness of

AMPu compared to Torula yeast in a citrus orchard. Various concentrations of AMPu

572



were tested in McPhail traps and yellow sticky ball traps. The ultimate goal of this re-search is to develop an attractant that can be used with a dry trap to replace theMcPhail trap/Torula yeast trapping system.

M

ATERIALS

AND

M

ETHODS

Insects

The test flies originated from a culture from Morelos, Mexico, that had been main-tained on laboratory diet for about 400 generations with no wild-fly introductions. Arecent study has shown that the mating behavior of this culture has changed onlyslightly from that of wild flies (Robacker et al. 1991). Likewise, I presume that the re-sponse of laboratory-reared flies to food-based attractants does not differ markedlyfrom that of wild flies.

Flies were irradiated with 7000-9200 rads (Cobalt 60 source) 1-2 days before adulteclosion, to comply with quarantine laws for releasing

A. ludens

. Irradiated flies wereshown to be 20% less responsive than unirradiated flies to bacterial odor (Robacker &Garcia 1993), the attractant on which development of AMPu was partially based.

Mixed-sex groups of 180-200 flies were kept in 473 ml cardboard cartons withscreen tops until used in tests. Laboratory conditions for holding flies were 22

±

2

°

C,50

±

20% relative humidity and photophase from 0630 to 1930 hours provided by flu-orescent lights. Flies were fed sucrose and water up until the time of release.

Citrus Orchard and Test Procedures

A mixed citrus orchard located near the laboratory in Weslaco, Texas, was used forall experiments. The orchard contained several varieties of orange, lemon, grapefruitand tangerine trees of varying ages. One row of ruby red grapefruit (

Citrus paradisi

)and one row of Dancy tangerine (

C. reticulata

) were chosen for tests since they con-tained relatively large (2-3 m height) fruit-bearing trees. Two blocks of seven consec-utive trees were used in each row, for a total of four blocks in the orchard.

Flies were released into the test orchard when 2-10 days old during the late after-noon of the day before a test. Robacker & Garcia (1993) showed that, within this agerange, fly age had little effect on attraction to bacterial odor, an attractant similar toAMPu as discussed above. Approximately 2000 flies were distributed equally amongthe 28 test trees in the four blocks. Attractants were tested either in McPhail traps(Baker et al. 1944) or on sticky yellow ball traps (Robacker 1992) that were hung oneto a tree, north of center, at 1-2 m height. Traps were placed in the orchard during themorning and removed for fly counts and cleaning on the following morning. Positionsof treatments within each block of trees were randomized for the first 1-day test ofmost experiments. Positions of treatments in consecutive 1-day tests were not ran-domized but were moved sequentially within each block.

Experiments 1 and 2 were conducted to determine the most attractive concentra-tion of AMPu in aqueous solution in McPhail traps. The AMPu tested was an aqueoussolution of ammonium bicarbonate, methylamine HCl, and putrescine in the ratio10:10:1 at pH 8.8 (adjusted with NaOH). The three chemicals were obtained fromSigma Chemical Co. (St. Louis, MO) and were >98% pure.

Experiment 1 evaluated three concentrations of AMPu. AMPu 2000 was preparedwith the three chemicals at 2:2:0.2 mg/ml. AMPu 200 and AMPu 20 were 1:10 and1:100 dilutions of AMPu 2000. Each AMPu trap contained 200 ml of one of these so-lutions in the trap’s liquid reservoir. Traps baited with three Torula yeast/borax “bait


573

pellets” (Sit-Khem Corp., Michigan City, IN) and 200 ml of tap water were included inthis and in Experiments 2 & 5 as attractiveness standards. Traps containing only 200ml of water were used as blanks. All traps except Torula yeast contained amber color-ing from a combination of red, yellow and green food colors (McCormick & Co., Inc.,Baltimore, MD) to mimic the color of Torula yeast. These traps also contained 0.01%Triton

®

(Rohm and Haas Co., Philadelphia, PA) as a wetting agent. One each of thethree AMPu traps, one Torula yeast trap and one water-blank trap were included ineach of the four blocks of trees. Five 1-day tests were conducted for a total of 20 repli-cations of each bait treatment. Baits were discarded after each 1-day test.

Experiment 2 compared AMPu 20 and AMPu 200 to three additional concentra-tions: AMPu 400; AMPu 100; and AMPu 50. The additional concentrations were 1:5,1:20 and 1:40 dilutions, respectively, of AMPu 2000. Experiment 2 was identical to Ex-periment 1 except that each block contained five AMPu treatments instead of three.Seven 1-day tests were conducted for a total of 28 replications of each bait treatment.

Experiment 3 was conducted to develop a formulation of AMPu that could be usedon a dry sticky trap. For this purpose, 1.9 ml polypropylene microcentrifuge tubes (A.Daigger & Company, Inc., Wheeling, IL) were used to hold various AMPu prepara-tions. The objective was to determine how much AMPu was needed in the tubes tomake them competitive with the best concentration used in McPhail traps.

AMPu was prepared in water at the concentration of 20:20:2 mg/ml at pH 8.8.Amounts ranging from 1.0-1.6 ml of this solution or various dilutions of the solutionranging down to 2:2:0.2 mg/ml were put into microcentrifuge tubes. Concentrationsgreater than 20:20:2 mg/ml were not used because all indications at the time this ex-periment was conducted were that greater concentrations would be less attractive.Tubes were suspended inside McPhail traps just above the inner rim and traps werefilled with 200 ml of amber-colored water as described above. These traps were testedagainst McPhail traps containing 200 ml of AMPu 200 in a flight chamber in a green-house as described by Robacker & Warfield (1993). AMPu 200 was used as the stan-dard because of its great attractiveness in previous flight chamber tests (Robacker &Warfield 1993). Briefly, the procedure was as follows. For each test, a trap containingAMPu 200 and a trap containing an AMPu tube were suspended side by side in the

upwind end of the screened chamber (2.0 m long

×

0.7 m wide

×

1.3 m high) with anairflow of 0.1 to 1.0 m/sec. Traps were alternated between left and right sides of thechamber every 15 min for a 1-h test. Approximately 200 sugar-fed, protein-starvedflies were released into the downwind end of the chamber at the beginning of eachtest. Four to 15 replications were conducted for each of seven concentrations tested inthe microcentrifuge tubes.

Experiment 4 evaluated AMPu tubes

vs

AMPu 400 in McPhail traps in the field.The purpose of this experiment was to determine if the optimum formulation of AMPuin microcentrifuge tubes that was developed in the greenhouse flight chamber wouldbe equivalent to AMPu 400 in McPhail traps in the field. AMPu 400 was used as thestandard because this was the most attractive concentration in previous field tests(Experiment 2). AMPu tubes contained 1.6 ml of AMPu at the concentration of 20:20:2mg/ml at pH 8.8. Three traps of each type were placed alternately on six trees in eachof the four blocks of trees used in previous tests. Two 1-day tests were conducted fora total of 24 replications of each bait treatment.

Experiment 5 evaluated AMPu tubes on ball traps

vs

Torula yeast in McPhailtraps in the field. Initially, AMPu microcentrifuge tubes were prepared containing 1.6ml of AMPu at the concentration of 20:20:2 mg/ml at pH 8.8, the formulation thatproved equal in attractiveness to AMPu 200 in greenhouse tests (Experiment 3) andAMPu 400 in field tests (Experiment 4). Subsequently, AMPu solutions were mixed

574



with agar to increase durability of the AMPu tubes exposed to weather on tops ofsticky traps. Concentrations of AMPu used in agar preparations were higher than20:20:2 mg/ml because the initial tests with aqueous formulations indicated that20:20:2 mg/ml was too low. Final AMPu concentrations in agar tubes ranged from100:100:10 to 225:225:22.5 mg/ml of the three components at pH 8.5 to 8.8. Ammo-nium carbonate (A.C.S. Reagent quality; Aldrich Chemical Co. Inc., Milwaukee, WI)was substituted for ammonium bicarbonate in some preparations, keeping the molarconcentration of ammonia equivalent to previous ammonium bicarbonate prepara-tions. Agar (Bacto Agar, Difco Laboratories, Detroit, MI) concentrations ranged be-tween 1-3% in final preparations. The AMPu/agar tubes were prepared by mixing hotagar solution with aqueous AMPu solution in microcentrifuge tubes.

AMPu tubes were fastened, with their caps open, to the tops of yellow ball traps(13 cm diam) that were coated with Tangle-Trap (Tanglefoot Company, Grand Rapids,MI). These traps were described previously in tests without olfactory lures (Robacker1992). Ball traps with AMPu tubes, unbaited ball traps, and McPhail traps containingTorula yeast as described above were compared in 1-day tests. Two each of the threetreatments were used in each of the four blocks in the citrus orchard for a total of eighttraps of each treatment per 1-day test. Fourteen 1-day tests were conducted using var-ious combinations of AMPu concentrations and agar percentages.

Statistical Analyses

Analysis of variance (ANOVA) was conducted for both males and females for Ex-periments 1, 2 and 5. Means separations were done by Fisher’s protected least signif-icant difference (LSD) method. t-Tests were used to determine if the ratio of femalesto males captured by AMPu traps was different from the ratio of flies captured inTorula yeast traps and to compare specific pairs of treatments in Experiments 3, 4and 5.

R

ESULTS

Experiments 1 and 2: AMPu Dosage-Response

The results of Experiment 1 are shown in Fig. 1. AMPu treatments were generallymore attractive than water but significantly less attractive than Torula yeast to bothmales (

F

= 18.7; df = 4,91;

P

< 0.0001) and females (

F

= 15.8; df = 4,91;

P

< 0.001).AMPu 200 was significantly more attractive than AMPu 2000 but was not signifi-cantly more attractive than AMPu 20. These results suggested that the most attrac-tive concentration was probably between AMPu 20 and AMPu 2000.

The results of Experiment 2 are shown in Fig. 2. All AMPu treatments were sig-nificantly more attractive than water to both males (

F

= 10.9; df = 6,189;

P

< 0.01) andfemales (

F

= 12.0; df = 6,189;

P

< 0.01). Torula yeast was significantly more attractiveto both males and females than all AMPu concentrations except AMPu 400 for males.Among AMPu treatments, AMPu 400 captured the most flies although it was not sig-nificantly more attractive than most of the other AMPu treatments. In both Experi-ments 1 and 2, the ratio of females to males captured by AMPu traps did not differsignificantly from the ratio of flies captured by Torula yeast traps.

Experiment 3: Optimum Concentration of AMPu in Microcentrifuge Tubes

Only the microcentrifuge tube containing 1.6 ml of AMPu at the concentration of20:20:2 mg/ml was comparable in attractiveness to the McPhail trap containing


575

AMPu 200. Mean captures by traps containing these AMPu tubes (

n

= 12) were 23.8

±

2.2 (SE) flies. Mean captures by traps containing AMPu 200 (

n

= 12) were 21.6

±

1.7flies.

Experiment 4: Field Evaluation of AMPu Tubes

vs

AMPu 400 in McPhail Traps

Traps containing AMPu tubes at 20:20:2 mg/ml of the three components wereequal in attractiveness to traps containing AMPu 400. Mean captures by traps con-taining AMPu tubes (

n

= 24) were 19.4

±

3.1 (SE) flies. Mean captures by traps con-taining AMPu 400 (

n

= 24) were 17.2

±

2.2 flies.

Experiment 5. Field Evaluation of AMPu Tubes on Ball Traps

vs

Torula Yeast in McPhail Traps

Ball traps with AMPu tubes containing aqueous AMPu at 20:20:2 mg/ml weremuch less attractive than McPhail traps containing Torula yeast. Mean captures onballs with AMPu tubes (

n

= 16) were 12.9

±

1.7 (SE) flies compared with 28.9

±

4.4 fliescaptured by Torula yeast traps (

n

= 16). The difference was highly significant (

t

= 3.3;df = 30;

P

< 0.01). Ball traps with AMPu tubes were much more attractive than un-baited balls (

n

= 16) which captured only 1.5

±

0.4 flies per trap.Ball traps with AMPu tubes containing AMPu in agar were competitive with

McPhail traps containing Torula yeast. No consistent differences were observed forthe various AMPu and agar concentrations, so they were combined for analysis. Table1 shows captures of flies by the traps, summed over all AMPu and agar concentra-tions. Captures by unbaited ball traps were significantly lower than captures by the

Figure 1. Mean captures (± SE; n = 20 each trap bait) of adult A. ludens in McPhailtraps containing water, Torula yeast or three concentrations of AMPu (Experiment 1).Within each sex, bars with the same letter are not significantly different from eachother by Fisher’s protected LSD (P < 0.05).

576



other two traps for males (

F

= 22.0; df = 2,314;

P

< 0.0001), females (

F

= 43.2; df =2,314;

P

< 0.0001), and males + females (

F

= 39.6; df = 2,314;

P

< 0.0001). Captures ofmales, females and total flies by AMPu traps and Torula yeast traps were not signifi-cantly different at the 5% level.

D

ISCUSSION

Wakabayashi & Cunningham (1991) developed a chemically defined attractant forthe melon fly (

B. cucurbitae

) for use in McPhail traps. Their attractant was an aque-ous preparation of ammonium bicarbonate, linolenic acid, putrescine and pyrrolidinein which concentrations of ammonium bicarbonate and putrescine were similar tothose in AMPu 400. Wakabayashi & Cunningham’s attractant was more attractive

T

ABLE

1. M

EAN

C

APTURES

(

±

SE; N = 110 E

ACH

T

RAP

/B

AIT

)

OF

M

EXICAN

F

RUIT

F

LIESON

S

TICKY

B

ALL

T

RAPS

W

ITH

OR

W

ITHOUT

AMP

U

T

UBES

AND

IN

M

C

P

HAIL

T

RAPS

C

ONTAINING

T

ORULA

Y

EAST

(E

XPERIMENT

5).

Trap/Bait Males

1

Females

1

Males + Females

1

Ball 0.21

±

0.05 a 0.30

±

0.06 a 0.51

±

0.08 aBall/AMPu Tube 1.83

±

0.33 b 3.15

±

0.34 b 4.97

±

0.61 bMcPhail/Torula Yeast 2.16

±

0.25 b 3.21

±

0.37 b 5.37

±

0.56 b

1

Means in a column followed by the same letter are not significantly different by Fisher’s protected LSD.

Figure 2. Mean captures (± SE; n = 28 each trap bait) of adult A. ludens in McPhailtraps containing water, Torula yeast or five concentrations of AMPu (Experiment 2).Within each sex, bars with the same letter are not significantly different from eachother by Fisher’s protected LSD (P < 0.05).


577

than NuLure in 1-day orchard tests. They did not evaluate their attractant in testslasting longer than 1 day, nor did they attempt to develop a formulation that could beused in a dry trap. However, their results were very important in showing that chem-ically defined “food bait” attractants are at least competitive with standard proteina-ceous lures.

Heath et al. (1995) developed an attractant for Mediterranean and Mexican fruitflies for use with a newly designed dry trap. Their attractant contained ammonium ac-etate and putrescine in a formulation that released ammonia and acetic acid at stablerates for at least a month. Although putrescine emissions were not measured byHeath et al. (1995), their data indicate that the lures remained attractive to both spe-cies of flies for 6 weeks in the field in Guatemala. The lure was as attractive as Torulayeast to feral Mediterranean fruit flies, but despite its similarity to AMPu, it was lessthan 20% as attractive as Torula yeast to feral Mexican fruit flies. The explanation forthe low attractiveness of their lures to Mexican fruit flies compared with the AMPulures used here is unknown. It could be related to chemical differences between AMPuand their lure, laboratory flies

vs

feral flies, race differences between the Mexican andGuatemalan flies, or a combination of the three factors.

As in Wakabayashi & Cunningham (1991), all experiments conducted here withAMPu were 1-day tests. It would have been desirable to conduct tests for 1 week, thestandard period that McPhail traps with Torula yeast are used. However, liquid for-mulations used in this work were not sufficiently attractive to warrant longer tests(Figs. 1 and 2) and the longevity of the agar preparations is unknown but likely lessthan 1 week. The initial attractiveness of the AMPu/agar preparations on sticky trapswas sufficient to warrant longer tests with sticky traps if a longer-lasting AMPu for-mulation that can be used with the traps can be developed. The goal will be to developa formulation that emits the three components at constant rates for 2 weeks or more.This should be possible in light of the success of Heath et al. (1995). It certainly willbe necessary to develop such a formulation before AMPu lures will be practical fortrapping programs by regulatory agencies.

A

CKNOWLEDGMENTS

I thank Pravait Kaochoung (Office of Atomic Energy for Peace, Bangkhen,Bangkok, Thailand), Maura Rodriguez and Marco Gomez for technical assistance;Sammy Ingle for insects; and A. W. Guenthner (USDA-APHIS, Mission, Texas) for ir-radiation of pupae. I thank Dr. Peter Landolt and Dr. Nancy Epsky for reviewing themanuscript. Use of a product brand in this work does not constitute an endorsementby the USDA.

R

EFERENCES

C

ITED

B

AKER

, A. C., W. E. S

TONE

, C. C. P

LUMMER

,

AND

M. M

C

P

HAIL

. 1944. A review of stud-ies on the Mexican fruitfly and related Mexican species. U. S. Department ofAgriculture Misc. Publ. 531.

H

EATH

, R. R., N. D. E

PSKY

, A. G

UZMAN

, B. D. D

UEBEN

, A. M

ANUKIAN

,

AND

W. L.M

EYER

. 1995. Development of a “dry” plastic trap with food-based synthetic at-tractant for the Mediterranean and Mexican fruit flies (Diptera: Tephritidae).J. Econ. Entomol. (In press).

R

OBACKER

, D. C. 1992. Effects of shape and size of colored traps on attractiveness toirradiated, laboratory-strain Mexican fruit flies (Diptera: Tephritidae). FloridaEntomol. 75: 230-241.

R

OBACKER

, D. C., R. L. M

ANGAN

, D. S. M

ORENO

,

AND

A. M. T

ARSHIS

M

ORENO

. 1991.Mating behavior and male mating success in wild Anastrepha ludens (Diptera:Tephritidae) on a field-caged host tree. J. Insect Behav. 4: 471-487.


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., AND W. C. WARFIELD. 1993. Attraction of both sexes of Mexican fruitfly, Anastrepha ludens, to a mixture of ammonia, methylamine, and putrescine.J. Chem. Ecol. 19: 2999-3016.

WAKABAYASHI, N., AND R. T. CUNNINGHAM. 1991. Four-component synthetic food baitfor attracting both sexes of the melon fly (Diptera: Tephritidae). J. Econ. Ento-

♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦

mol. 84: 1672-1676.

578



SUPERPARASITISM AND INTRASPECIFIC COMPETITION BY THE SOLITARY LARVAL-PUPAL PARASITOID

ARCHYTAS MARMORATUS

(DIPTERA: TACHINIDAE)

S

TUART

R

EITZ

Department of EntomologyUniversity of California

Riverside, CA 92521USA

A

BSTRACT

Superparasitism and intrinsic larval competition by the solitary larval-pupal par-asitoid

Archytas marmoratus

(Townsend) were studied

in vivo

. In superparasitizedhosts, when two parasitoids entered a host pupa, only one parasitoid completed devel-opment. The surviving

A. marmoratus

maggot eliminated the conspecific competitorthrough physiological suppression during the second stadium of the supernumerarymaggot. Supernumerary parasitoids never survived beyond the second instar, regard-less of the time interval between initial parasitism and subsequent superparasitism.Physical combat was not evident because the parasitoid eliminated did not show signsof physical injuries. Scramble competition for host resources was not a probable mech-anism of elimination because puparial weights and adult eclosion rates from super-parasitized host pupae, and those from singly parasitized pupae, were not signif-icantly different.

Key Words: Parasitoid competition, intraspecific interactions.

R

ESUMEN

El parasistismo y la competencia larval intrínseca del parasitoide larvo-pupal

Ar-chytas marmoratus

(Townsend) fueron estudiados en vivo. En hospedantes superpa-rasitados, cuando dos parasitoides entraron en una pupa hospedante, solamente unocompletó el desarrolo. La larva sobreviviente de

A. marmoratus

eliminó el competidorconespecífico mediante supresión fisiológica durante el segundo estadio de la larva su-pernumeraria. Los parasitoides supernumerarios nunca sobrevivieron más allá delsegundo instar, independientemente del intervalo entre el parasistismo inicial y el su-perparasitismo subsecuente. El combate físico no fue evidente debido a que el parasi-toide eliminado no mostró señales de daño físico. La competencia por recursos de

Reitz: Larval Competition in

A. marmoratus 579

hospedante no fue un mecanismo probable de eliminación debido a que los pesos pu-pales y las tasas de eclosión de adultos de las pupas superparasitadas y de las para-

sitadas por una sola larva no fueron significativamente diferentes.

Archytas marmoratus

(Townsend) (Diptera: Tachinidae) is a solitary larval-pupalparasitoid of numerous species of Noctuidae (Lepidoptera). Included in its host rangeare many important pest species in the genera

Helicoverpa, Heliothis, Pseudaletia,

and

Spodoptera

(Arnaud 1978, Ravlin & Stehr 1984)

. A. marmoratus

has a complex life history that allows it to parasitize a wide rangeof host instars. Females do not oviposit directly on hosts; instead they deposit numer-ous eggs in the vicinity of potential host larvae. The eggs soon hatch into planidia-typelarvae (Wood 1987). Parasitism occurs when a host contacts a planidium which thenburrows between the host cuticle and epidermis where it resides (Bratti et al. 1993).The first instar of

A. marmoratus

begins feeding on the host larva, but it does not moltuntil after the host pupates. The first instar must reenter the host following each lar-val-larval molt of the host. After the host undergoes its larval-pupal molt, the first-in-star parasitoid penetrates the hemocoel under the host wing pad, where it induces theformation of a respiratory tunnel.

A. marmoratus

development within the host pupais rapid. The maggot molts to the second instar 1 - 2 days following host pupation; thesecond and third stadia last 2 - 4 days each, with pupariation occurring within thehost remains (Vickery 1929).

Because female

A. marmoratus

deposit multiple eggs at one time (Vickery 1929),and more than one female may oviposit in the same location, considerable potentialfor superparasitism exists. Despite this potential, only one

A. marmoratus

maggotcompletes development in a host (Vickery 1929, Hughes 1975). Among the possiblemechanisms for the elimination of supernumerary parasitoids are physical combat,scramble competition for host resources, or physiological suppression (Salt 1961,Fisher 1971, Vinson & Iwantsch 1980). In this study, I examine aspects of superpara-sitism and intrinsic larval competition, including parasitism rates, elimination of su-pernumerary parasitoids, and effects on parasitoid development and emergence.

M

ATERIALS

A

ND

M

ETHODS

All tests were conducted at the Istituto di Entomologia “Guido Grande”, Univer-sita degli Studi di Bologna, Bologna, Italy.

A. marmoratus

adults were reared in plexi-glass cages (40

×

40

×

40 cm) in an environmental chamber maintained at 27

±

2

°

C,60

±

10% R.H. and 14:10 (L:D) photoperiod (fluorescent light). To obtain

A. marmora-tus

planidia for parasitization, pieces of pleated filter paper were placed on the bottomof cages as oviposition substrate the day prior to parasitism. Thus, all planidia wereless than 24 h old at the time of parasitization. Larvae of the factitious host,

Galleriamellonella

L. (Lepidoptera: Galleriidae), were reared on artificial medium (Cam-padelli 1973) in plastic containers (23

×

11

×

8 cm) held at 30

±

2

°

C, 60

±

10% R.H.,and 0:24 (L:D) photoperiod.

Penultimate-instar larvae of

G. mellonella

in apolysis were isolated in containerswith fresh diet. The following morning, these groups were reexamined for newly-molted ultimate-instars. Each

G. mellonella

larva was infested by gripping it behindthe head capsule with a soft forceps and transferring

A. marmoratus

planidia to the

580



larval thorax with a fine camel hair brush. Each larva was held until the planidia bur-rowed into the cuticle. Then it was placed in a new plastic container with fresh diet.

Six parasitism treatments were used, with three groups of

G. mellonella

larvae be-ing superparasitized and three groups being singly parasitized. The three superpar-asitized groups were: (A) Newly molted (day 1) ultimate-instar

G. mellonella

larvaeparasitized with two

A. marmoratus

planidia (Superparasitized - Day 1), (B) Day 1larvae parasitized once and superparasitized two days later (Superparasitized - Day1, 3), and (C) Day 1 larvae parasitized and superparasitized four days later (Super-parasitized - Day 1, 5). Only larvae with visible planidia were superparasitized. Thethree corresponding singly parasitized control groups were parasitized on day 1 (Day1 Control), day 3 (Day 3 Control), or day 5 (Day 5 Control) of the ultimate stadium, re-spectively.

G. mellonella

were weighed upon pupation and individually isolated until

A. mar-moratus

pupariation, or

G. mellonella

eclosion or death.

A. marmoratus

puparia wereweighed one day after pupariation and held individually until eclosion. Host remainswere dissected to determine the number and status of

A. marmoratus

maggots. To ver-ify that all parasitoid remains had been recovered during the initial inspection, thehost remains were macerated in 10% KOH and reexamined. No additional

A. marm-oratus

were recovered by this procedure. All parasitoid remains (bodies or exuviae)were identified to larval instar (Ravlin & Stehr 1984), and bodies were carefully in-spected for signs of physical injury. The size and degree of sclerotization of the ceph-alopharyngeal skeletons of maggots from superparasitized hosts were compared atthe stage at which the first maggot died. The

A. marmoratus

in each superparasitizedhost were classified according the developmental stage to which they survived. If nei-ther parasitoid survived longer than the other, the competitive interaction was con-sidered a “tie”. True winners of competitive interactions were those that actuallysurvived to adult eclosion.

Chi square tests were used to examine differences in parasitism rates and parasi-toid survival among the different treatments. To determine if parasitoid size and de-velopment were affected by parasitism treatment, data were analyzed by analysis ofcovariance (ANCOVA) with host pupal weight serving as a covariate. Pairwise com-parisons between superparasitized treatments and their corresponding controls weremade by least squares means

t

-tests.

R

ESULTS

Because first-instar parasitoids had to reenter the host successfully after it pu-pated, not all

G. mellonella

pupae contained

A. marmoratus

(Table 1)

.

However, par-asitoid entries into host pupae were independent events because the proportion ofsuperparasitized hosts across superparasitism treatments (19.8%) was approxi-mately equal to the square of the proportion of the parasitized pupae in all controltreatments (44.5%, X

2

= 0.001, df = 1, P > 0.9). The first planidium that entered thehost pupa did not exclude the entry of the other planidium because superparasitismrates were not significantly less than the values expected had entries been indepen-dent events. Even though approximately 20% of host pupae were superparasitized(Table 1), a maximum of one

A. marmoratus

survived per host.Based on the condition of the parasitoid remains in host pupae, supernumerary

parasitoids were almost always eliminated during their second stadium (test for dif-ferences among

A. marmoratus

instars, X

2

= 133, df = 2, P < 0.001, Table 2); this dif-ference was consistent across superparasitism treatments (test for differences amongsuperparasitism treatments, X

2

= 3.4, df = 2, P = 0.18, Table 2). Three of the

A. mar-

Reitz: Larval Competition in

A. marmoratus 581

moratus

maggots that died as first instars (17%, n = 18) had failed to penetrate thehost cuticle following host pupation. The remainder that did enter their host pupagrew (when compared with newly hatched planidia), but did not become successfullyestablished in the host and molt. Only four (22%) of these first-instars showed signsof physical injury, such as melanized wounds. Few of those maggots that died as sec-ond instars had signs of physical injury (5%, n = 94), but they typically had smallerand/or less sclerotized cephalopharyngeal skeletons than those that survived to alater stage (75%, n = 94, X

2

= 17.7, df = 2, P < 0.001). In two superparasitized pupae(2%, n = 112), the supernumerary

A. marmoratus

died before completing their finallarval ecdysis.

Adult eclosion of

A. marmoratus

did not differ across treatments (X

2

= 10.1, df =5, P > 0.07, Table 2), or when considering superparasitism versus single parasitismtreatments (X

2

= 3.6, df = 1, P = 0.06, Table 2). Overall, development times of

A. mar-moratus

(from host pupation to

A. marmoratus

adult eclosion) from singly and super-parasitized host pupae were not significantly different (overall

x

±

SE = 13.4

±

0.2days, F = 0.1, df = 1, 128, P = 0.80). In pairwise comparisons between superparasitizedgroups and their respective control groups, the only significant difference was be-tween the Day 1, 3 superparasitized and Day 3 control groups; the controls emergedone day earlier (12.7

±

0.3 days) than the parasitoids from the superparasitized group(13.9

±

0.4 days) (

t

= 3.1, P = 0.0024).The size of

A. marmoratus

puparia increased significantly with host weight (pu-paria from superparasitized hosts: y = 0.3 + 0.46x, r

2

= 0.82; puparia from singly par-asitized hosts: y = 1.3 + 0.42x, r

2

= 0.73). However, puparia from singly parasitizedhosts were not significantly heavier (71.1

±

1.9 mg) than those from superparasitizedhosts (68.2

±

2.5 mg, F = 1.7, df = 1, 136, P = 0.19, test for homogeneity of intercepts).Host weight alone accounted for over 74% of the variation in

A. marmoratus

weights.

T

ABLE

1. P

ARASITISM

AND

S

UPERPARASITISM

OF

G.

MELLONELLA

P

UPAE

BY

A.

MARM-ORATUS

W

HEN

P

ARASITIZED

AT

D

IFFERENT

I

NTERVALS

D

URING

THE

U

LTI-MATE

L

ARVAL

S

TADIUM

.

Number of

A. marmoratus

Maggots per

G. mellonella

Pupa

Treatment

1

1 Maggot 2 MaggotsTotal Number of

Pupae Tested

SuperparasitizedDay 1, 1 93 (36%) 47 (18%) 261

Day 1 Control 48 (41%) — 118SuperparasitizedDay 1, 3

87 (44%)40 (20%) 196

Day 3 Control 56 (62%) — 91SuperparasitizedDay 1, 5

47 (44%)25 (23%) 108

Day 5 Control 44 (36%) — 123Total 375 112 897

1

See text for details of each treatment.

582



T

AB

LE

2.

D

EV

EL

OP

ME

NT

AL

S

TA

GE

OF

A.

MA

RM

OR

AT

US

IN

G.

ME

LL

ON

EL

LA

P

UP

AE

S

UP

ER

PA

RA

SIT

IZE

D

AT

D

IFF

ER

EN

T

T

IME

I

NT

ER

VA

LS

D

UR

ING

TH

E

U

LT

IMA

TE

L

AR

VA

L

S

TA

DIU

M

. T

AB

LE

V

AL

UE

S

R

EF

LE

CT

TH

E

F

INA

L

D

EV

EL

OP

ME

NT

AL

S

TA

GE

R

EA

CH

ED

BY

C

OM

PE

TIN

G

P

AR

AS

I-T

OID

S

. N

O

H

OS

TS

P

RO

DU

CE

D

P

AR

AS

ITO

IDS

TH

AT

S

UR

VIV

ED

TO

TH

E

SA

ME

ST

AG

E.

A. m

arm

orat

us

Sta

ge1

Nu

mbe

r an

d P

erce

nt

of O

utc

omes

for

Eac

h T

reat

men

t2

(A)

(B)

Su

perp

aras

itiz

edD

ay 1

, 1S

upe

rpar

asit

ized

Day

1, 3

Su

perp

aras

itiz

edD

ay 1

, 5T

otal

Adu

ltII

In

star

18 (

40%

)19

(42

%)

8 (1

8%)

45A

dult

I In

star

8 (5

7%)

3 (2

1%)

3 (2

1%)

14P

upa

eII

In

star

10 (

36%

)12

(43

%)

6 (2

1%)

28P

upa

eI

Inst

ar1

(50%

)0

(0%

)1

(50%

)2

III

Inst

arII

In

star

9 (4

1%)

6 (2

7%)

7 (3

2%)

22II

I In

star

I In

star

1 (1

00%

)0

(0%

)0

(0%

)1

Tot

al47

(42

%)

40 (

36%

)25

(22

%)

112

1 (A)

Sta

ge r

each

ed b

y pa

rasi

toid

su

rviv

ing

the

lon

gest

, (B

) S

tage

rea

ched

by

firs

t pa

rasi

toid

th

at d

ied.

2 See

tex

t fo

r de

tail

s of

eac

h t

reat

men

t.

Reitz: Larval Competition in A. marmoratus 583

DISCUSSION

A variety of mechanisms for the elimination of supernumerary larvae exist amongthe Tachinidae. Physical combat has been observed among first instars of Marquartiachalconota Meigen (Mellini & Baronio 1971). Anoxia is responsible for elimination ofolder supernumerary maggots of Lixophaga diatraeae (Townsend) (King et al. 1976).Superparasitism results in reduced body size for several potentially gregarious ta-chinids (Pschorn-Walcher 1971, Ziser et al. 1977, Reitz 1994). This variation in para-sitoid size is attributed to resource depletion in superparasitized hosts. However,these species have significantly different life histories from A. marmoratus. Becauseof the high potential of superparasitism occurring in the field, and the relationship be-tween parasitoid and host size (A. marmoratus puparia are > 50% of the weight ofhost pupae), A. marmoratus would be expected to have evolved an effective mecha-nism for eliminating conspecific competitors.

Given the consistent stage at which supernumerary maggots of A. marmoratusare eliminated and the lack of demonstrable physical injuries to these “losing” mag-gots, physiological suppression of conspecific competitors cannot be excluded as amechanism of intraspecific competition. If competition were based solely on physicalattacks, all “losing” maggots should show signs of injury (Mellini & Baronio 1971,Mellini 1990). Also, some encounters, especially in hosts superparasitized on the sameday, could be expected to be resolved when both parasitoids were third instars.

In fact, if direct physical combat was responsible, it should occur most often amongthird instars. Unlike many solitary hymenopteran parasitoids that have free-roaminglarvae adapted for fighting (Vinson 1985, Kfir & van Hamburg 1988, McBrien &Mackauer 1990), first and second instars of A. marmoratus reside in respiratory tun-nels (Mellini 1990) that form along the wing pad margins of host pupae. Only third in-stars become mobile (Hughes 1975, Bratti et al. 1992). However, no host pupaecontained two third instars. While second and third instars of A. marmoratus possesssickle-shaped mandibles that could inflict serious damage, any observed damagecould have occurred after a competitor had already died from other causes. In addi-tion, second instars are considerably smaller than G. mellonella pupae; therefore, un-less parasitoid respiratory attachments are in close proximity, second instars wouldnot encounter one another, further increasing the occurrence of encounters amongthird instars.

The possibility that supernumerary maggots are eliminated through scramblecompetition for host resources is also not supported by the present data. If scramblecompetition was operating, greater variation in the stage at which competitors areeliminated would be expected. In particular, larger hosts should more frequently sup-port multiple third instars. Additionally, if scramble competition was responsible forelimination of supernumerary maggots, the size of A. marmoratus should vary withthe number of maggots present in a host pupa. However, the relationship between A.marmoratus weights and host pupal weights did not vary with respect to whether ahost was singly or superparasitized. Also, adult eclosion rates did not differ signifi-cantly as might be expected as a result of scramble competition.

A possible scenario for physiological suppression of supernumerary A. marmora-tus is that older maggots (i.e., those parasitizing the host larva first) are more devel-opmentally advanced, and initially have faster development rates in the host pupa,thus molting to the second and third instar sooner than subsequent maggots (Brattiet al. 1992, 1993). Because the host pupa dies by the time an A. marmoratus maggotmolts to the third instar (Allen 1926), the maggot that molts to its final instar firstcould make the host environment unsuitable for younger maggots to continue theirdevelopment. Therefore, maggots reaching their final instar first could suppress com-


petitors by production of proteolytic enzymes (Mellini 1990) or degradation of thehost. Further in vitro studies of intrinsic competition should elucidate the specificmeans of physiological suppression used by A. marmoratus.

ACKNOWLEDGMENTS

A. Bratti, M. Mariani and the Staff of the Istituto di Entomologia “Guido Grande”,Universita degli Studi di Bologna provided valuable technical assistance. I appreciatethe assistance of P. H. Adler, L. Correlli-Grappadelli, K. A. Luhring, and J. T. Trumblein making this study possible, and the comments of two anonymous reviewers whichhave improved this manuscript. This study was made possible with financial supportfrom a W. C. Nettles Memorial Grant, a Sigma Xi Grant-in-Aid of Research, and aFlorida Entomological Society Scholarship.

REFERENCES CITED

ALLEN, W. H. 1926. Life history of the variegated cutworm tachini fly, Archytas ana-lis. J. Agric. Res. 32: 417-435.

ARNAUD, P. H., JR. 1978. A host-parasite catalog of North American Tachinidae(Diptera). United States Dept. Agric. SEA Misc. Publ. No. 1319, 860 pp.

BRATTI, A., G. GARDENGHI, AND G. MIGLIOLI. 1993. Behavior and growth rate of Ar-chytas marmoratus (Town.) (Diptera: Tachinidae) planidia in larvae of Galleriamellonella L. (Lepidoptera Galleriidae). Boll. Ist. Entomol. Univ. Bologna 47:141-149.

BRATTI, A., W. C. NETTLES, JR., AND P. FANTI. 1992. Influence of Helicoverpa zea (Lep-idoptera: Noctuidae) age during the last instar on rates of parasitization by thelarval-pupal parasitoid, Archytas marmoratus (Diptera: Tachinidae). Environ.Entomol. 21: 1196-1201.

CAMPADELLI, G. 1973. Allevemento di Galleria mellonella L. con dieta semiartificiale.Boll. Ist. Entomol. Univ. Bologna 32: 2-25.

FISHER, R. C. 1971. Aspects of the physiology of endoparasitic Hymenoptera. Biol.Rev. Cambridge Philos. Soc. 46: 243-278.

HUGHES, P. S. 1975. The biology of Archytas marmoratus (Townsend). Ann. Entomol.Soc. America 68: 759-767.

KFIR, R., AND H. VAN HAMBURG. 1988. Interspecific competition between Telenomusullyetti (Hymenoptera: Scelionidae) and Trichogrammatoidea lutea (Hy-menoptera: Trichogrammatidae) parasitizing eggs of the cotton bollworm He-liothis armiger in the laboratory. Environ. Entomol. 17: 664-670.

KING, E. G., L. R. MILES, AND D. F. MARTIN. 1976. Some effects of superparasitism byLixophaga diatraeae of sugarcane borer larvae in the laboratory. Entomol. Exp.Appl. 20: 261-269.

MCBRIEN, H., AND M. MACKAUER. 1990. Heterospecific larval competition and hostdiscrimination in two species of aphid parasitoids: Aphidius ervi and Aphidiussmithi. Entomol. Exp. Appl. 56: 145-153.

MELLINI, E. 1990. Sinossi di biologia dei Ditteri Larvevoridae. Boll. Ist. Entomol.Univ. Bologna. 45: 1-38.

MELLINI, E., AND P. BARONIO. 1971. Superparasitismo sperimentale e competizionilarvali del parassitoide solitario Marquartia chalconota Meig. Boll. Ist. Ento-mol. Univ. Bologna 30: 133-152.

PSCHORN-WALCHER, H. 1971. Experiments on inter-specific competition betweenthree species of tachinids attacking the sugar cane moth borer, Diatraea sac-charalis (F.). Entomophaga 16: 125-131.

RAVLIN, F. W., AND F. W. STEHR. 1984. Revision of the genus Archytas (Diptera: Ta-chinidae) for America north of Mexico. Entomol. Soc. America Misc. Pub. 58, 58pp.

Scheffrahn & Roisin: Antillean Parvitermes 585

REITZ, S. R. 1994. Reproductive biology of Eucelatoria bryani and Eucelatoria ruben-tis (Diptera: Tachinidae), larval parasitoids of Helicoverpa zea (Lepidoptera:Noctuidae). Ph. D. Thesis, Clemson University.

SALT, G. 1961. Competition among insect parasitoids. Symp. Soc. Exp. Biol. 15: 96-119.

VICKERY, R. A. 1929. Studies on the fall army worm in the Gulf coast district of Texas.United States Dept. Agriculture Tech. Bull. 138, 64 pp.

VINSON, S. B. 1985. The behavior of parasitoids, pp. 417-469 in G. A. Kerkut and L. I.Gilbert [eds.], Comprehensive insect physiology, biochemistry and pharmacol-ogy, vol. 9. New York, Pergamon Press.

VINSON, S. B., AND G. F. IWANTSCH. 1980. Host suitability for insect parasitoids.Annu. Rev. Entomol. 25: 397-419.

WOOD, D. M. 1987. Tachinidae, pp. 1193-1269 in J. F. McAlpine [ed.], Manual of Ne-arctic Diptera. Ottawa, Agriculture Canada.

ZISER, S. W., J. A. WOJTOWICZ, AND W. C. NETTLES, JR. 1977. The effects of the num-ber of maggots per host on length of development, puparial weight, and adult

♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦

emergence of Eucelatoria sp. Ann. Entomol. Soc. America 70: 733-736.

Scheffrahn & Roisin: Antillean

Parvitermes 585

ANTILLEAN NASUTITERMITINAE (ISOPTERA: TERMITIDAE):

PARVITERMES COLLINSAE

, A NEW SUBTERRANEAN TERMITE FROM HISPANIOLA AND REDESCRIPTION OF

P. PALLIDICEPS

AND

P. WOLCOTTI

R

UDOLF

H. S

CHEFFRAHN

1

AND

Y

VES

R

OISIN

2

1

Fort Lauderdale Research and Education CenterUniversity of Florida, Institute of Food and Agricultural Sciences

3205 College Avenue, Ft. Lauderdale, FL 33314

2

Research Associate, National Fund for Scientific Research, Belgium; Université Libre de Bruxelles, CP 160/12

Laboratoire de Biologie Animale et Cellulaire Avenue F.D. Roosevelt 50, B-1050 Brussels, Belgium

A

BSTRACT

Three

Parvitermes

species are described from recent Antillean collections. All ex-hibit a dimorphic soldier caste characterized by rare major soldiers, reported from

Parvitermes

for the first time, and minor soldiers with constricted heads. Workersshare similarities in digestive tube morphology and enteric valve armature. Soldiersand workers of a new species,

Parvitermes collinsae

, are described and the descrip-tions of

Parvitermes wolcotti

(Snyder, 1924) from Puerto Rico and

P. pallidiceps

(Banks, 1919) from Hispaniola are revised.

Key Words: Taxonomy, new species, castes, West Indies.

R

ESUMEN

Tres especies de

Parvitermes

son descritas de colecciones antillanas recientes. To-das exhiben una casta dimórfica de soldados caracterizada por soldados mayores, re-

586



portados de

Parvitermes

por primera vez, y soldados menores con cabezasconstringidas. Las obreras tienen similitudes en la morfología del tubo digestivo y enla armadura de la válvuala entérica. Son descritos los soldados y obreras de la nuevaespecie,


, y son revisadas las descripciones de

Parvitermes wol-

cotti

(Snyder, 1924) de Puero Rico y

P. pallidiceps

(Banks, 1919) de La Española.

The genus

Parvitermes

was established by Emerson (in Snyder 1949) for an assem-blage of small nasute termite species from the Neotropical Region. The type species,

P. brooksi

(Snyder), and five of the other seven species currently placed in

Parvitermes

are known only from the West Indies (Araujo 1977, Scheffrahn & Krecek 1993). A re-cent morphological study of the worker digestive tube, mandibles, and enteric valvearmature indicates that

Parvitermes

is endemic to the Greater Antilles and that thisand other Antillean nasute genera, as well as the mainland species of

Parvitermes

, re-quire a reevaluation of their generic status (Roisin et al. unpubl.).

An ongoing survey of the termites of the West Indies has uncovered a number ofnew species, species records (Scheffrahn et al. 1994), and undescribed castes. In-cluded among these findings are a new

Parvitermes

from the Dominican Republic andthe discovery of a major soldier caste in

P. pallidiceps

(Banks) and

P. wolcotti

(Snyder).In addition to a major soldier, minor soldiers of all three species exhibit a well-markedhead constriction. We include herein the description of the soldier and worker castesof


n. sp. and a redescription of

P. pallidiceps

from Hispaniolaand

P. wolcotti

from Puerto Rico to supplement the earlier descriptions by Banks(1919) and Snyder (1924), respectively.

M

ATERIALS

AND

M

ETHODS

Measurements of specimens preserved in 85:15 ethanol:water were made with acalibrated ocular micrometer and follow those defined by Sands (1965) and Roonwal(1970). Terms used to describe soldier morphology and color follow those of Sands(1965). Left mandible index of workers equals the distance between the apical andfirst marginal tooth divided by distance between first and third marginals (Emerson1960). In

Parvitermes

, the second marginal tooth of the left worker mandible is re-duced to a long, rather straight, cutting edge. Head height was measured withoutpostmentum to the highest point of the head capsule. Scanning electron micrographsof soldiers dehydrated by the method of Nation (1983) were made with a Hitachi S-4000 field emission microscope at 10kV.

The digestive tube of large workers was observed after removal of the abdominalwall and fat tissues under a dissecting microscope. The digestive tube of

P. pallidiceps

was drawn with the aid of a camera lucida at 50X and described using the terminologyof Noirot & Noirot-Timothée (1969) and Kovoor (1969). Enteric valves were longitudi-nally split with a fine scalpel. Mandibles and split enteric valves were dehydrated andmounted

in toto

for microphotography. The holotype minor soldier and morphotype major soldier and worker of

P. collin-sae

will be deposited in the collection of the National Museum of Natural History,Washington, D.C. Paratype specimens will be deposited in the Florida State Collec-tion of Arthropods, Fla. Dept. Agric. Cons. Serv., Division of Plant Industries, Gaines-ville, Florida, at the institutions of the first and second authors (in Ft. Lauderdale andBrussels, respectively), and at the Universidad de Santo Domingo, Dominican Repub-lic.


Parvitermes 587


Scheffrahn and Roisin, new species

IMAGO.

Unknown.

MINOR SOLDIER

(Figs. 1-2, Table 1). Head capsule, postmentum (gula), and firstantennal article orange, nasus chestnut brown; antennal articles three and beyond se-

T

ABLE

1. M

EASUREMENTS

OF

P

ARVITERMES

COLLINSAE

M

INOR

S

OLDIER

.

Measurement in mm (n = 46) Range Mean

±

SD Holotype

Head length with nasus 0.95 - 1.16 1.06

±

0.056 1.06Head length without nasus 0.58 - 0.71 0.66

±

0.036 0.66Head width, maximum 0.45 - 0.64 0.55

±

0.056 0.55Head width, anterior lobe 0.43 - 0.54 0.49

±

0.029 0.49Nasus width at base 0.11 - 0.14 0.13

±

0.0094 0.13Nasus width at middle 0.059 - 0.081 0.069

±

0.0056 0.063Head height, maximum 0.33 - 0.44 0.38

±

0.035 0.38Pronotum width 0.33 - 0.39 0.36

±

0.014 0.35Pronotum length, maximum 0.14

±

0.19 0.17

±

0.012 0.18Hind tibia length 0.59 - 0.83 0.73

±

0.059 0.74Total length 2.06 - 3.10 2.53

±

0.25 2.93

Figures 1-4. Scanning electron micrographs of dorsal and lateral views of Parvit-ermes collinsae n. sp. minor (1, 2) and major (3, 4) soldiers.

588



pia brown; thoracic nota and abdominal tergites pale brown; and abdominal sternites,coxae, and femora very pale brown.

Head capsule in dorsal view slightly constricted near middle, maximum width ofanterior lobe usually less than that of posterior lobe; in lateral view, anterior and pos-terior lobes raised equally and rounded in front of and behind constriction. Head cap-sule covered with dozens of short and medium length setae tilted at various angles.

Antennae with 13 articles; second less than or as long as third, third usuallylonger than fourth, fourth shorter or as long as fifth. Mandibles usually with distinctpoints. Nasus very weakly conical, projecting almost straight forward, i.e., parallel todorsal plane of head.

MAJOR SOLDIER

(Figs. 3-4, Table 2). Head capsule, postmentum, and first anten-nal article ferruginous orange, nasus chestnut brown; distal antennal articles sepiabrown; thoracic nota and abdominal tergites pale brown; and abdominal sternites,coxae, and femora very pale brown.

Head capsule in dorsal view roundly constricted near middle, maximum width ofanterior lobe greater than that of posterior lobe; in lateral view, anterior and posteriorlobes raised equally and rounded in front of and behind shallow constriction. Headcapsule covered with dozens of randomly tilted medium and long setae.

T

ABLE

2. M

EASUREMENTS

OF

M

AJOR

S

OLDIER

.


±

SD Morphotype

Head length with nasus 1.09 - 1.13 1.12

±

0.020 1.13Head length without nasus 0.69 - 0.74 0.72

±

0.024 0.74Head width, maximum 0.60 - 0.62 0.61

±

0.0088 0.62Head width, anterior lobe 0.58 - 0.60 0.59

±

0.0094 0.60Nasus width at base 0.18 - 0.19 0.18

±

0.0063 0.18Nasus width at middle 0.088

±

0 0.088Head height, maximum 0.43 - 0.46 0.44

±

0.020 0.43Pronotum width 0.41 - 0.43 0.42

±

0.0088 0.43Pronotum length, maximum 0.18 - 0.19 0.18

±


±

0.026 0.88Total length 2.60 - 3.16 2.84

±

0.26 3.16

T

ABLE

3. M

EASUREMENTS

OF

P

ARVITERMES

COLLINSAE

L

ARGE

W

ORKER

.


±

SD Morphotype

Head width, maximum 0.85 - 1.11 0.96

±

0.070 0.96Head length to postclypeus

anteclypeus suture 0.78 - 1.03 0.90

±

0.059 0.90Postclypeus width 0.40 - 0.54 0.47

±

0.032 0.48Postclypeus length 0.15 - 0.24 0.20

±


±

0.056 0.83Total length 2.85 - 4.15 3.51

±

0.33 3.95


Parvitermes 589

Antennae with 14 articles; second shorter than third, third longer than fourth, andfourth equal to fifth. Mandibles with points. Nasus stout, slightly conical; tiltingabout 15

°

above dorsal plane of head.

WORKER

(Figs. 13,17; Table 3). Head capsule pale brown except for unpigmentedepicranial suture and genae; nota and tergites very pale brown; antennal articlesbrown; no pigmentation on remainder of body. Dozens of variable setae covering head.

Antennae with 14 or 15 articles; relative lengths somewhat variable but usually if14, second longer than third, third equal or longer than fourth, and fourth shorterthan fifth; if 15, second equal to or longer than third, third shorter than fourth, andfourth as long as fifth.

Mandibles with posterior edge of apical tooth slightly shorter or equal in length toanterior edge of first marginal tooth, left mandible index 0.24-0.35; right molar plateabruptly notched near base, 5-6 ridges total, 4 well-developed ridges distal to notch(Fig. 13).

Digestive tube consisting of moderate-sized crop, well-armed gizzard, and me-senteron followed by very long mixed segment (as in

P. pallidiceps

, Fig. 15). Mesen-teric part of mixed segment on internal/dorsal side, attached to remainder ofmesenteron by thin peduncle. Malpighian tubules inserted on external/ventral side ofmesentero-proctodeal junction. P1 extremely elongated, forming a long loop on ven-tral side of paunch. Enteric valve latero-dorsal, comprising diffuse areas with manysmall spines, followed by a ring of six spiny swellings, three major ones bearing 12-20long, curved spines (Fig. 17), alternating with minor ones with small spines. P3 to rec-tum without remarkable features.

Figures 5-8. Scanning electron micrographs of dorsal and lateral views of Parvit-ermes pallidiceps (Banks) minor (5, 6) and major (7, 8) soldiers.

590



Comparisons

. Although allopatric in distribution, minor soldiers and workers of

P.collinsae

are closest to

P. wolcotti

. Minor soldiers of

P. wolcotti

can be distinguishedby their much darker, more brown pigmentation, and proportionally thicker nasus.Minor soldiers of

P. collinsae

from Pedernales Province are proportionally larger thanthose from Barahona and Azua Provinces.

Major soldiers can be distinguished by the shape of their head capsule which lacksconstriction in

P. wolcotti

, while that of

P. collinsae

is constricted and has an anteriorlobe wider than the posterior lobe.

Workers of

P. wolcotti

have no exoskeletal pigmentation and have antennae withonly 14 articles, whereas

P. collinsae

worker bodies are dorsally pigmented and havea nearly equal proportion of individuals with 14 and 15 antennal articles. The molarplate of the right mandible of

P. wolcotti

workers has 5 well-developed ridges distal tothe basal notch, whereas

P. collinsae

has four such ridges (Figs. 13-14).Soldiers and workers of

P. collinsae

can be readily separated from those of the par-tially sympatric

P. pallidiceps

on the basis of simple characters. Minor soldiers of theformer have 13 antennal articles and distinct mandibular points while the latter have12 articles and points are either lacking or vestigial. Likewise, major soldiers of

P. col-linsae

have 14 antennal articles and points while

P. pallidiceps

major soldiers have14-15 articles but no points. Large workers of

P. collinsae

have 14-15 antennal articlesand head width ranging between 0.85-1.11 mm while large workers of

P. pallidiceps

have only 15 articles and greater head widths of 1.05-1.36 mm.

Material Examined

. Specimens from 25 foraging groups of

P. collinsae

n. sp. weremeasured from eleven localities in the Dominican Republic. HOLOTYPE minor sol-dier and MORPHOTYPE worker: Barahona Province, 2 km W Fondo Negro (18

°

25'N,

Figures 9-12. Scanning electron micrographs of dorsal and lateral views of Parvi-termes wolcotti (Snyder) minor (9, 10) and major (11, 12) soldiers.


Parvitermes 591

Figures 13-14. Scanning electron micrographs of P. collinsae (13) and P. wolcotti(14) right molar plates of worker mandibles.

592



71

°

05'W), 30-III-1993, J. Chase and J. de la Rosa Guzman, nest series reference no.DR801 and DR802. MORPHOTYPE major soldier: Azua Province, Barahona/SanJuan highway intersection (18

°

28'N, 70

°52'W), 3-V-1992, J. Chase, J. de la Rosa Guz-man, and R. Scheffrahn, nest series reference no. DR350. PARATYPES: Azua Prov-ince, 9 km E Quita Coraza (18°28'N, 71°58'W), 3-V-1992, Caracoles (18°25'N,70°37'W), 27-III-1993; Baoruco Province, Vijia de Mena (18°23'N, 71°11'W), 21-VI-1991: Barahona Province, La Canoa 1 km W Vincente Noble (18°23'N, 71°11'W), 27-II-1992, 2 km N Canoa (18°22'N, 71°09'W) 3-V-1992; Pedernales Province, 12 km WOviedo (17°52'N, 71°29'W), 29-III-1993, 15 km E Cabo Rojo (17°56'N, 71°32'W), 29-III-1993, 3 km E Pedernales (18°00'N, 71°41'W), 29-III-1993, Pedernales (18°03'N,71°44'W), 28-III-1993, all collected variously by J. Chase, J. de la Rosa Guzman, J.Mangold, and R. Scheffrahn.

Etymology. This species is named in honor of Dr. Margaret S. Collins, isopterist atthe Smithsonian Institution and retired Professor of Zoology, Howard University, forher lifelong dedication to the study of termites.

Parvitermes pallidiceps (Banks, 1919)

IMAGO. Unknown.

MINOR SOLDIER (Figs. 5-6, Table 4). Head capsule and first several antennal arti-cles orange-yellow, nasus darker, grading to chestnut brown in distal region and be-coming lighter at tip to give banded appearance, postmentum lighter than headcapsule; distal antennal articles pale brown; thoracic nota and abdominal tergitesvery pale brown; abdominal sternites, coxae, femurs and tibiae paler than tergites.

Head capsule in dorsal view slightly constricted near middle, maximum width ofanterior lobe always less than that of posterior lobe; in lateral view, posterior loberaised and in line with tip of nasus, anterior lobe raised slightly between constrictionand base of nasus. Head capsule scattered with medium and long setae.

Antennae with 12 articles; the second shorter than the third, and the third equalto the fourth. Mandibles without points or only one point vestigial. Nasus slender, cy-lindrical except near base, tilting about 20° above plane of head.

TABLE 4. MEASUREMENTS OF PARVITERMES PALLIDICEPS MINOR SOLDIER.

Measurement in mm (n = 48) Range Mean ± SD

Head length with nasus 1.03 - 1.26 1.14 ± 0.051Head length without nasus 0.65 - 0.80 0.71 ± 0.030Head width, maximum 0.51 - 0.67 0.57 ± 0.033Head width, anterior lobe 0.44 - 0.55 0.47 ± 0.023Nasus width at base 0.094 - 0.13 0.11 ± 0.0090Nasus width at middle 0.059 - 0.075 0.065 ± 0.0040Head height, maximum 0.36 - 0.51 0.42 ± 0.033Pronotum width 0.33 - 0.40 0.35 ± 0.016Pronotum length, maximum 0.15 - 0.20 0.17 ± 0.010Hind tibia length 0.74 - 0.95 0.83 ± 0.047Total length 2.23 - 3.26 2.82 ± 0.21


MAJOR SOLDIER (Figs. 7-8, Table 5). Head capsule and first several antennal ar-ticles ferruginous orange, nasus darker, grading to dark chestnut brown in distal re-gion and becoming lighter at tip to give banded appearance, postmentum lighter thanhead capsule; distal antennal articles brown; thoracic nota and abdominal tergites or-ange-yellow; abdominal sternites, coxae, femurs and tibiae paler than tergites.

TABLE 5. MEASUREMENTS OF PARVITERMES PALLIDICEPS MAJOR SOLDIER.



Figure 15. Dorsal (D), right (R), ventral (V), and left (L) configurations of the di-gestive tube in situ of P. pallidiceps worker. CP, crop; M, mesenteron (stippled) includ-ing mesenteric part of MS, mixed segment; O, oesophagus; P1, first proctodealsegment; P2, enteric valve; P3, paunch; P4, colon; R, rectum; T, Malpighian tubules(darkly stippled). Scale bar = 0.5 mm.


Head capsule in dorsal view roundly constricted near middle, maximum width ofanterior lobe always less than that of posterior lobe; in lateral view, posterior loberaised and in line with base of nasus, anterior lobe raised beyond constriction and con-tinues to rise with upward tilt of nasus. Head capsule scattered with dozens of me-dium and long, randomly tilted setae.

Antennae with 14-15 articles; the second equal or longer than the third, the thirdshorter than the fourth, and the forth equal to the fifth. Mandibles without points. Na-sus conical, especially near base, tilting about 25° above plane of head.

WORKER (Figs. 15-16, Table 6). Head capsule pale brown except for unpigmentedepicranial suture and genae; nota and tergites very pale brown; antennal articleslight brown; no pigmentation on remainder of body. Dozens of variable setae coveringhead.

Antennae with 15 articles; second longer than third, third shorter than fourth, andfourth equal to fifth.

Mandibles similar to P. collinsae with the exception that molar plate of right man-dible has 6-7 ridges total, including 5 well-developed ridges distal to basal notch. Di-gestive tube (Fig. 15) and enteric valve armature also similar to P. collinsae.

TABLE 6. MEASUREMENTS OF PARVITERMES PALLIDICEPS LARGE WORKER.


Head width, maximum 1.05 - 1.36 1.21 ± 0.064Head length to postclypeus anteclypeus

suture 0.96 - 1.26 1.13 ± 0.079Postclypeus width 0.48 - 0.60 0.55 ± 0.029Postclypeus length 0.19 - 0.25 0.22 ± 0.017Hind tibia length 0.95 -1.26 1.14 ± 0.063Total length 3.25 - 4.85 4.03 ± 0.45

TABLE 7. MEASUREMENTS OF PARVITERMES WOLCOTTI MINOR SOLDIER.




Material Examined. Specimens compared favorably with paratype minor soldiersfrom type colony, Diquini, Haiti, XI-1912, W.M. Mann. Specimens from 48 foraginggroups of P. pallidiceps were measured from 12 localities in the Dominican Republic:Peravia Province, 2 km E Las Calderas (18°13'N, 70°29'W), 3-V-1992, J. Chase, J. dela Rosa Guzman, and R. Scheffrahn; Azua Province, 12 km N Yayas de Viajama(18°39'N, 70°56'W), 3-V-1992, J. Chase, J. de la Rosa Guzman, and R. Scheffrahn;Azua Province, 9 km E Quita Coraza (18°28'N, 70°58'W), 3-V-1992, J. Chase, J. de laRosa Guzman, and R. Scheffrahn; Azua Province, Barahona/San Juan highway inter-section (18°28'N, 70°52'W), 3-V-1992; Barahona Province, La Cienega (18°02'N,71°08'W), 4-VIII-1992, 2 km W Fondo Negro (18°25'N, 71°05'W), 4-VIII-1992, 30-III-1993; Distrito Nacional, Santo Domingo (18°29'N, 69°54'W), 4-V-1992; La RomanaProvince, La Romana (18°27'N, 68°58'W), 12-VI-1992; La Vega Province, El Piño de LaVega (19°09'N, 70°29'W), 8-VI-1992; Peravia Province, 8 km W Bani (18°19'N,70°24'W), 26-II-1992; Samana Province, 15 km S Las Galeras (19°12'W, 69°13'N), 6-VI-1992; San Pedro de Macoris Province, Juan Dolio (18°25'N, 69°25'W), 4-VIII-1992,all collected variously by J. Chase, J. de la Rosa Guzman, J. Mangold, and R. Schef-frahn.

Parvitermes wolcotti (Snyder, 1924)

IMAGO. Not described; suspected collections from light traps.

MINOR SOLDIER (Figs. 9-10, Table 7). Head capsule brown, nasus darker, gradingto very dark sepia brown in distal region, slightly lighter at tip; antennal articlesslightly lighter than head capsule; margins of thoracic nota and abdominal tergitespale brown; and abdominal sternites, legs, and interior areas of nota very pale yellow-brown.

Head capsule in dorsal view slightly constricted near middle, maximum width ofanterior lobe usually less than that of posterior lobe; in lateral view, posterior and an-terior lobes equally raised and rounded in front of and behind constriction. Head cap-sule covered with dozens of short and medium length setae tilted at various angles.

Antennae with 13 articles; second as long as third, third longer than fourth, fourthshorter than fifth. Mandibles with points. Nasus very weakly conical, projecting al-most straight forward.

MAJOR SOLDIER (Figs. 11-12, Table 8). Head capsule brown, nasus darker, grad-ing to very dark sepia brown in distal region, slightly lighter at tip; antennal articlesslightly lighter than head capsule; thoracic nota and abdominal tergites pale brown;and abdominal sternites, legs, and interior areas of nota very pale yellow-brown.

Head capsule in dorsal view ellipsoidal, not constricted near middle; in lateralview, head indented near middle raised and rounded in front of and behind indenta-tion. Head capsule covered with dozens of short and medium length setae randomlytilted.

Antennae with 14 articles; second as long as third, third shorter than fourth,fourth shorter than fifth. Mandibles with points. Nasus conical, projecting almoststraight forward.

WORKER (Fig. 14, Table 9). Head capsule yellow brown except for unpigmented ep-icranial suture and genae; nota and tergites light yellow or unpigmented; antennalarticles pale yellow brown; no pigmentation on remainder of body. Dozens of variablesetae covering head.

Antennae with 14 articles; second longer than third, third equal to or longer thanfourth, fourth shorter than fifth..


Mandibles with posterior edge of apical tooth slightly shorter than anterior edgeof first marginal tooth, left mandible index 0.45; right molar plate abruptly indented(notched) near base, 6-7 ridges total, 5 well-developed ridges distal to indentation(Fig. 14). Digestive tube also similar to P. collinsae.

Material Examined. Available type material of P. wolcotti was badly damaged andunusable, however, Snyder’s (1924) description of the minor soldier was sufficient foridentification. Specimens from 18 foraging groups of P. wolcotti were measured from6 localities in Puerto Rico: Guanica State Forest Reserve. (17°58'N, 66°52'W), 13-I-1993, S. Jones; NE Salinas, Rancho Guama Rd @ 706/713 (18°01'N, 66°13'W), 15-V-1992, S. Jones; Baños de Coamo (18°02'N, 66°22'W), 30-V-1993, J. Chase, J. de la RosaGuzman, J. Mangold, and R. Scheffrahn; Baños de Coamo, 29-V-1993; highway 1 & 52intersection, 9 km NE Salinas (18°01'N, 66°15'W), 29-V-1993; 5 km W Coamo on high-way 14 (18°03'N, 66°29'W), 30-V-1993; Yauco (18°02'N, 66°49'W), 30-V-1993, GuanicaReserve, 30-V-1993, J. Chase, J. de la Rosa Guzman, J. Mangold, and R. Scheffrahn;Guanica Reserve, 15-I-1993, 6-V-1992, 24-25-V-1993, S. Jones.

TABLE 8. MEASUREMENTS OF PARVITERMES WOLCOTTI MAJOR SOLDIER.

Measurement in mm (n = 1)1

Head length with nasus 1.11Head length without nasus 0.76Head width, maximum 0.65Head width, anterior lobe —Nasus width at base 0.15Nasus width at middle 0.088Head height, maximum 0.38Pronotum width 0.41Pronotum length, maximum 0.21Hind tibia length 0.80Total length 2.66

1Dehydrated and sputter-coated with gold for SEM photography.

TABLE 9. MEASUREMENTS OF PARVITERMES WOLCOTTI LARGE WORKER.


Head width, maximum 0.88 - 1.08 0.95 ± 0.042Head length to postclypeus anteclypeus

suture 0.80 - 0.98 0.88 ± 0.045Postclypeus width 0.41 - 0.50 0.45 ± 0.020Postclypeus length 0.19 - 0.24 0.21 ± 0.012Hind tibia length 0.71 - 0.84 0.77 ± 0.030Total length 2.95 - 4.00 3.59 ± 0.29


Fig

ure

16.

Dor

sal v

iew

of

left

an

d ri

ght

wor

ker

man

dibl

es o

f P. p

alli

dic

eps.

Sca

le b

ar =

0.1

mm

.


DISCUSSION

Originally described from minor soldiers collected in Haiti (Banks 1919), Parviter-mes pallidiceps is widely distributed throughout the Dominican Republic, whereas P.

Figure 17. Longitudinal section of enteric valve of P. collinsae worker, showing twoof three major spine-bearing swellings.


collinsae is restricted to the more arid southwestern Dominican Provinces. Arid local-ities in southeastern Haiti will likely also yield P. collinsae. In the Dominican Repub-lic, both species occur sympatrically in the southwestern Province of Azua andadjacent areas of Barahona Province. Parvitermes wolcotti is known from the south-western and southern dry forest lowlands of Puerto Rico (Jones et al. 1995) and theVirgin Islands (Scheffrahn et al. 1994 and unpublished).

Parvitermes pallidiceps and P. collinsae foragers have been collected in and underdried ruminant dung on soil, and in or on various cellulosic materials. Parvitermespallidiceps is reported to attack sugarcane seed in Haiti (Araujo 1970). Although thenest center with royal pair has not been observed for either species, early instars,workers, soldiers, and brachypterous nymphs of both species have been collected fromsimilar nesting structures. Their subterranean excavations consist of a diffuse systemof chambers interconnected by narrow tunnels and are usually found under largerocks, stones, or heavy surface debris. Nest chambers of P. pallidiceps often containbits of dried grass which suggests they forage in the open at night as this species hasnot been collected under protective sheeting. In contrast, P. collinsae and P. wolcottiwill cover dried twigs and grass stems with thin soil sheeting when foraging aboveground. Parvitermes wolcotti has been collected from beneath dung pats, soil sheeting,and foraging tubes covering wood, or from buried cardboard traps. Snyder’s (1924)types for P. wolcotti were collected from beneath soil sheeting covering rotten wood.

Although minor soldiers are common, major soldiers are extremely rare for allthree species, constituting much less than 1% of total foraging populations thus farcollected. Unexpectedly, major soldiers have been collected more often with small for-aging groups containing fewer than 100 individuals than with large groups consistingof more than 1,000 members. Their role in colony defense remains obscure.

Brachypterous nymphs have been collected in foraging groups in May and Augustfor P. pallidiceps and in October for P. collinsae suggesting dispersal flights in latesummer or fall. Although not collected with foragers, alates believed to be P. wolcottiwere collected at night in October 1992 from light traps on Guana Island, British Vir-gin Is. during rain (J. Krecek, unpubl.). No additional information is available on theswarming habits of these three Parvitermes species.

ACKNOWLEDGMENT

We are indebted to J. A. Chase, J. de la Rosa G., and J. R. Mangold for their relent-less dedication to collecting termites throughout the West Indies and elsewhere; S.C.Jones for her diligent collecting efforts in Puerto Rico; D. S. Williams of the ICBR Elec-tron Microscope Core Facility at the University of Florida, Gainesville, for assistingwith scanning electron microscopy; Dr. Sule Oygur of the American Museum of Nat-ural History for the loan of P. pallidiceps paratypes and J. Krecek, J. Tsai, and N.-Y.Su for critically reviewing and improving this contribution no. R-04475 of the Univer-sity of Florida Experiment Station Series.

REFERENCES CITED

ARAUJO, R. L. 1970. Termites of the Neotropical Region. Chapter 12 in K.Krishna andF. M. Weesner [eds.], Biology of Termites, Vol. 2. Academic Press, New York.

ARAUJO, R. L. 1977. Catálogo dos Isoptera do Novo Mundo. Acad. Brasileira de Ciên-cias, Rio de Janeiro, RJ. 92 pp.

BANKS, N. 1919. Antillean Isoptera. Bull. Mus. Comp. Zool. 62: 474-489 + 2 plates.EMERSON, A. E. 1960. New genera of termites related to Subulitermes from the Ori-

ental, Malagasy, and Australian Regions (Isoptera, Termitidae, Nasutitermiti-nae). American Mus. Nov. 1986: 1-28.


JONES, S. C., J. A. CHASE, J. R. MANGOLD, J. DE LA ROSA GUZMAN, AND R. H. SCHEF-FRAHN. 1995. Survey of the termites of Puerto Rico. Florida Entomol. (submit-ted).

KOVOOR, J. 1969. Anatomie comparée du tube digestif des termites II. Sous-Familledes Nasutitermitinae. Insectes Soc. 16: 195-233.

NATION, J. A. 1983. A new method using hexamethyldisilazane for the preparation ofsoft insect tissue for scanning electron microscopy. Stain Technol. 55: 347-352.

NOIROT, C., AND C. NOIROT-TIMOTHÉE. 1969. The digestive system. Chapter 3 in K.Krishna and F. M. Weesner [eds.], Biology of Termites, Vol. 1. Academic Press,New York.

ROONWAL, M. L. 1970. Measurements of termites (Isoptera) for taxonomic purposes.J. Zool. Soc. India 21: 9-66.

SANDS, W. A. 1965. A revision of the termite subfamily Nasutitermitinae (Isoptera,Termitidae) from the Ethiopian Region. Bull. British Mus. Nat. Hist., Entomol.Suppl. 4: 1-172.

SCHEFFRAHN, R. H., AND J. KRECEK. 1993. Parvitermes subtilis, a new subterraneantermite (Isoptera: Termitidae) from Cuba and the Dominican Republic. FloridaEntomol. 76: 603-607.

SCHEFFRAHN, R. H., J. P. E. C. DARLINGTON, M. S. COLLINS, J. KRECEK, AND N. -Y. SU.1994. Termites (Isoptera: Kalotermitidae, Rhinotermitidae, Termitidae) of theWest Indies. Sociobiology 24: 213-238.

SNYDER, T. E. 1924. Description of a new termite from Puerto Rico. Proc. Entomol.Soc. Washington 26: 131-132.

SNYDER, T. E. 1949. Catalog of the termites (Isoptera) of the world. Smithson. Misc.

♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦

Collect. 112: 1-490.

600



REARING METHODS FOR

AGENIASPIS CITRICOLA

(HYMENOPTERA: ENCYRTIDAE) AND

CIRROSPILUS QUADRISTRIATUS

(HYMENOPTERA: EULOPHIDAE) RELEASED IN A CLASSICAL BIOLOGICAL CONTROL

PROGRAM FOR THE CITRUS LEAFMINER

PHYLLOCNISTIS CITRELLA

(LEPIDOPTERA: GRACILLARIIDAE)

J

ANEL

M. S

MITH

AND

M

ARJORIE

A. H

OY

Department of Entomology and NematologyP.O. Box 110620, University of Florida

Gainesville, FL 32611-0629

A

BSTRACT

Rearing techniques for

Ageniaspis citricola

and

Cirrospilus quadristriatus

andtheir host, the citrus leafminer,

Phyllocnistis citrella

, are discussed as related to aclassical biological control program. Methods for rearing the three trophic levels (cit-rus plants, leafminers, and parasitoids) are described in detail. An average of 1,155adult citrus leafminers were produced in a cage filled with 60-72 young citrus trees.Between April and October 1994, a total of 15,230

A. citricola

were produced, with anaverage of 750 adults per cage. Between late July and October 1994, a total of 1,328

C. quadristriatus

were produced, with an average of 144 adults per cage. The two par-asitoids were released into leafminer-infested citrus groves throughout Florida in aclassical biological control project.

Smith & Hoy: Rearing CLM and Two Parasitoids

601

Key Words: Citrus leafminer,

Phyllocnistis citrella, Ageniaspis citricola, Cirrospilusquadristriatus

, biological control, rearing methods.

R

ESUMEN

Se discuten las técnicas para la cría del minador de los cítricos

Phyllocnistis citre-lla

y dos de sus parasitoides,


y


, en re-lación a un programa de control biológico clásico. Son descritos en detalle los métodospara criar los tres niveles tróficos (plantas de cítricos, minadores y parasitoides). Seprodujeron un promedio de 1,155 adultos del minador en una jaula provista con 60-72plantas jóvenes. De abril a octubre de 1994 se produjeron un total de 15,230

A. citri-cola

, con un promedio de 750 por jaula. De fines de julio a octubre de 1994 se produ-jeron un total de 1,328

C. quadristriatus

, con un promedio de 144 adultos por jaula.Como parte de un proyecto de control biológico clásico, se liberaron los dos parasitoi-des en huertas de cítricos infestadas por el minador, en varios sitios del estado de Flo-

rida.

The citrus leafminer (CLM),


Stainton, (Lepidoptera: Gracil-lariidae) is an important pest of citrus. It affects production and can augment the se-verity of citrus canker (

Pseudomonas citri

Hasses) on damaged plants (Sohi & Sandhu1968). The CLM originates from southeast Asia (Heppner 1993). Perhaps due to nat-ural dispersal patterns and shipment of infested citrus, it has become established inother citrus production areas throughout the world.

The adult CLM is a minute moth, 2.5 mm long with folded wings and with a 4.5mm wingspan. Adults emerge from their pupal chambers early in the morning (Beat-tie & Smith 1993). Mating, which lasts an average of 22 minutes (Pandey & Pandey1964), occurs at dusk and early evening, 9 to 12 hours after emergence. Egg-laying be-gins 1 to 8 days later (Badawy 1967; Ba-Angood 1977; Beattie & Smith 1993). A singlefemale can lay up to 20 eggs per night, for a total of more than 50 in her 5- to 20-daylifetime (Beattie & Smith 1993). The translucent oval eggs are typically laid near themidrib of young leaves on the under side of the leaf (Badawy 1967; Ba-Angood 1977;Beattie & Smith 1993). Egg eclosion occurs 1 to 10 days later (Pandey & Pandey 1964;Beattie & Smith 1993) with the young larva immediately burrowing under the waxycuticle of the leaf (Sohi & Verma 1965). The larva feeds on the cells of the epidermis,creating silvery, serpentine mines along the leaf (Sohi & Verma 1965) often causingthe leaf to curl (Heppner 1993). During warm weather, the small larva progressesthrough three feeding instars in 5 to 6 days and enters a fourth, non-feeding stage(prepupa) for one day before forming a pupal chamber by folding over a leaf edge. Thepupal stage can last 6 to 22 days, depending on the time of year (Pandey & Pandey1964). A generation is thus completed in 14 to 17 days during warm summer months(Beattie & Smith 1993), but can be as long as 52 days in winter (Pandey & Pandey1964).

The CLM was first recorded from Florida in May 1993 and has since dispersedthroughout the state (Heppner 1993). It is now also recorded in Alabama, Louisiana,and Texas. The use of pesticides to control CLM is inefficient due to several reasons:price requirements for multiple applications, CLM larval stages are protected withintheir mines from topical applications, and the CLM may develop resistance to pesti-cides. Research to develop an integrated pest management program in citrus groveswas initiated shortly after the CLM arrived. Classical biological control was identifiedas a high priority component of the IPM program. As part of the classical biological

602



control project for CLM in Florida, two parasitic wasps were imported from Australia:


Logvinovskaya (Hymenoptera: Encyrtidae) and

Cirrospilusquadristriatus

Subba Rao & Ramamani (Hymenoptera: Eulophidae) in April 1994(Hoy & Nguyen 1994a, b, c). These parasitoids are native to Asia and reported to behost specific to the CLM (Beattie 1992).

Synchronized rearing methods were developed in order to produce large numbersof the CLM and its parasitoids so inoculative releases could be made in Florida. Thebenefits of synchronized rearing for each species include: 1) the developmental stageand age of the colony is known; 2) the purity of the colony is easier to maintain; and3) the likelihood of introducing pests and diseases into the colony is reduced. The pur-pose of this paper is to describe rearing methods for: 1) producing large numbers of cit-rus trees in flush suitable for rearing CLM in the greenhouse; 2) the CLM; and 3) theparasitoids

A. citricola

and

C. quadristriatus

.

M

ATERIALS

AND

M

ETHODS

Citrus

Citrus was either grown from seed or obtained as seedlings or grafted trees fromlocal nurseries. Rough lemon (

Citrus jambhiri

Lushington) seeds were planted in a1:1 mixture of potting soil and vermiculite in a cavity seedling tray (Hummert Inter-national, Earth City, MO) containing 96 2.5

×

2.5

×

7.5 cm cavities. Three 7- to 10-cmtall seedlings were transferred to each 3.8 liter plastic pot or 3.9 liter black plasticnursery bag (Poly-Cel, Hummert International, Earth City, MO). Two weeks after be-ing transplanted, the seedlings were fertilized with a long-acting, slow-release fertil-izer (19-10-10 plus iron, Once, Grace-Sierra, Horticultural Products Company,Milpitas, CA). Fertilizer was reapplied after 6 months. Seedlings were ready to use ashosts for the CLM when the stems were approximately 5 mm in diam and 30 to 50 cmtall. The time required to achieve this size depended upon the time of year the seedswere planted, ranging from 7 months if planted in fall/winter to 4 months if plantedin spring/summer.

Grapefruit (

Citrus

×

paradisi

Macf.) and sour orange grafted on trifoliate orange(

Citrus trifoliata

(L.) Raf.) rootstock also are suitable as hosts for CLM. Both producea large amount of flush from the nodes after pruning (1/4 to 1/2 of each branch re-moved) and leaf stripping. Grafted trees were obtained from nurseries when theywere approximately 60 cm tall. Grafted trees were treated to reduce pest infestationsby pruning and spraying them with oil (15 ml 97% petroleum oil, Ortho Volck OilSpray, Chevron Chemical Company, CA in 3.8 liter water). The pruned plants pro-duced sufficient flush for use after approximately 2 weeks at 30

°

C and 80% relativehumidity. Other citrus varieties, including rough lemon, lime, trifoliate orange, andswingle, also were donated as seedlings and reared as above. All proved suitable forrearing the CLM.

Citrus plants were maintained either in a greenhouse or a shadehouse. Seedlingswere grown in a 6.6

×

9.1 m greenhouse covered with a shadecloth that provided 35%shade. The average temperature in this greenhouse was 30

°

C (temperatures occasion-ally reached a maximum of 37.8

°

C and a minimum of 23.3

°

C) and the average relativehumidity was 80% (90-100% for approximately 14 h per day, as low as 50% for a shorttime during the heat of the afternoon). Trees, including those recently pruned, do-nated material, and other extras, were also housed in a 6.1

×

24.4 m shadehouse con-structed of 50% shadecloth. Recently-pruned plants were placed in the shadehousewithin 61

×

61

×

61 cm mesh cages (BioQuip, Gardena, CA) until they had produced


603

new flush with no CLM. All trees were watered when needed, usually 2 to 3 times perweek.

Pest Problems

. A variety of pests had to be managed in the greenhouse where treeswere reared, including citrus whitefly (

Dialeurodes citri

Ashmead), broad mite(

Polyphagotarsonemus latus

Banks), and citrus red mite (

Panonychus citri

McGre-gor). Trees in the greenhouse and shadehouse were monitored at least weekly forpests. Broad mites were controlled by lightly hand dusting only the new flush withsulfur (90% sulfur, Southern Agricultural Insecticide, Inc., Hendersonville, NC) semi-weekly or when needed. Citrus whiteflies and citrus red mite were controlled byspraying with 5% insecticidal soap solution (Safer, Inc. Eden Prairie, MN) semi-weekly. The sulfur and insecticidal soap were applied on alternate weeks.

Citrus mealybug (

Planococcus citri

Risso) was an occasional pest in the shade-house. Mealybugs were physically removed from plants when detected. Some treesalso became infested with scale insects, primarily Caribbean black scale (

Saissetia ne-glecta

DeLotta) and cottony cushion scale (

Icerya purchasi

Mask.). When scales of anytype were discovered, the adult scales were removed by hand and the plant wassprayed with insecticidal soap, or the plant was discarded if the infestation was se-vere.

Citrus Leafminer

CLM-infested foliage was initially obtained from citrus groves around Lake Alfred,Florida in February 1994. Infested foliage was also obtained occasionally from treesin Gainesville to supplement the colony. Occasionally, mines were found with deadlarvae (<5%), but no bacterial, fungal, or viral diseases were observed in CLM larvaeor pupae although detailed observations were not made.

Initially, isolation of adult moths from the infested foliage was difficult. Severalstandard methods produced few adults or were very labor-intensive. Placing infestedleaves on a water-soaked cotton pad in glass petri dishes was attempted; moth emer-gence rates were high, but collection was slow and it was a space- and labor-consum-ing procedure. Infested foliage was placed in several dark containers of different sizesfitted with one or more glass emergence tubes at the top, streaked with honey. Themoths preferred to rest on the leaves and did not fly toward the light unless disturbed.The few that flew into the tubes often did not stay for a long period of time but re-turned to the foliage to rest.

The most efficient emergence method tested involved placing infested leaves withpupal chambers in clear plastic bags. Approximately 120 leaves were placed in each30.4

×

25.2 cm bag. If only a few leaves were placed in a bag, a pad of moistened cottonwas added to prevent the leaves from drying out. The bags were then inflated by blow-ing into them, and the end of the bag was twisted and secured. The bags were placedunder a fluorescent light in the laboratory. A high rate (averaging 81%) of adult CLMemerged, usually early in the morning. Adult moths could be removed from the bagsevery other day in late morning or early afternoon using a vacuum aspirator. The vac-uum pump aspirated the moths through 5 mm plastic tubing into a 29.6-ml plasticcup. Mouth aspiration is unsafe because the moth scales are allergenic. The bags werewiped with paper towels after each aspiration to reduce condensation, although theCLM adults did not seem to be adversely affected by free moisture.

After the moths were aspirated into a cup, they were fed honey by adding a honey-soaked tissue (Kimwipe, Kimberly-Clark, Roswell, GA) or by streaking thin lines ofhoney on the lid or sides of the cup. Adult CLM were allowed to feed for 1 to 2 h beforebeing placed in a large cage to mate and to oviposit on potted citrus trees in flush.

604



Citrus trees suitable for oviposition by CLM were those with young flush 1 to 2 cmlong. We placed 20 to 24 pots into a 76.2

×

114.3

×

91.4 cm screened cage. Honey wasstreaked in fine lines on two 5

×

8 cm clear plastic sheets which were taped to the in-side top of the cage frame as a food source for CLM adults. We added 175 to 250 adultmoths (sex ratio unknown) to each cage by placing the opened plastic cups on the floorof the cage.

Fresh honey was streaked on the plastic sheets after 2 days. The trees were wa-tered as needed, typically every three days. Cages were maintained in a 2.8

×

6 mgreenhouse covered with shadecloth which provided 35% shade. The greenhouse forrearing CLM averaged 30

°

C (but occasionally reached a maximum of 37.8

°

C for abrief duration and a minimum of 23

°

C) and 80% relative humidity (with a minimumof 50% for approximately 1 h during the middle of the day). Because CLM adults sur-vive best in >85% RH (J. Villanueva-Jiménez, unpublished), we attempted to main-tain high humidity (around 80-90%) by flooding the floor of the greenhouse once ortwice a day and/or by running portable humidifiers.

Young mines (1-3 mm long) were observed on the foliage after 4 to 6 days. Plantswere then used to rear the 2 parasitoid colonies or for maintaining the CLM colony(Fig. 1). If the infested foliage was used for colony maintenance, leaves with pupalchambers, which developed 9 to 12 days after adding adults to the cage, were removedfrom the trees and placed in plastic bags in the laboratory for adult emergence as de-scribed above. Adults emerged in bags 4 to 21 days after the first pupal chambersformed.

To estimate productivity of the rearing, 3 large cages were selected at random be-tween June and July and the number of CLM produced from 20 to 24 pots (containing57 to 70 trees) per cage was recorded.

Pest Problems in the Citrus Greenhouse

. To manage ants in the greenhouse, stickybarriers (The Tanglefoot Company, Grands Rapid, MI) were applied to the legs of thegreenhouse benches. Additionally, commercial ant baits (Combat Insect Control Sys-tems, Oakland, CA) were placed on the benches and in the cages. One species,

Tapi-noma melanocephalum

, was especially difficult to control because they were notcontrolled with commercial baits. To reduce infestation by

T. melanocephalum

, plantswere thoroughly watered in an attempt to flush any ant colonies from the pots beforethey were placed in cages with the CLM and again before the CLM-infested trees weretransferred to cages containing the parasitoids.


A. citricola

is an endoparasitoid, parasitizing eggs and early instar larvae (Logvi-novskaya 1983; Hoy & Nguyen 1994b; O. R. Edwards, personal communication) andproducing 1 to 10 individuals per single host. Both males and females are found, con-trary to previous reports of thelytoky (Evans 1995). Unmated females produce onlymale progeny, suggesting that this species is arrhenotokous (O. Edwards, personalcommunication). When first instar CLM larvae were visible on foliage, typically 4 to6 days after CLM adults were introduced, the trees were ready to be used for

A. citri-cola

colonies. At this stage, foliage will have both eggs and mines containing first in-star larvae. Prior to placing the trees in cages with

A. citricola

, they were thoroughlywatered to reduce ant densities.

Parasitoid cages were maintained in the same greenhouse where citrus plantswere housed. Fifteen to twenty pots, usually containing three infested citrus treeseach, were added to each cage and 50 to 75

A. citricola

adults were then introduced.The sex ratio of the introduced adults was unknown, although the average sex ratio


605

was 1 male:1.8 females based on 204 individuals sexed from random samples from 7different cages between October and November. Honey was streaked on several piecesof plastic suspended from the top of the cage to provide food for parasitoid adults.Honey was reapplied after 48 hours and the plants were watered as needed.

Between April and October, new

A. citricola

adults emerged 16 to 18 days afteradults were introduced into the cages. The parasitoids were collected by pruning foli-age containing CLM pupal chambers from the trees after 15 to 17 days. The exact timewas judged by opening a few pupal chambers to determine if the majority of

A. citri-cola

pupae were dark brown. The leaves were then placed in inflated plastic bags with

Figure 1. A flow diagram indicating the steps and approximate time involved inrearing citrus, the CLM and the two parasitoids. See text for more detail.

606



paper towels, and the bags were checked daily to collect wasps and to eliminate con-densation on the bags. Adult parasitoids were collected once a day via mouth aspira-tion into a 50 ml vial containing tissues in the bottom to provide a soft surface. Ahoney-soaked strip of tissue was placed in the vial to provide food for the adult para-sitoids.

If the parasitoids were to be released into citrus groves, the vials were placed in agrowth chamber at 19

°

C until they were shipped. Parasitoids were delivered by auto-mobile or shipped via overnight mail in styrofoam containers with blue ice packs tomaintain temperatures at approximately 17

°

C. If the parasitoids were used to main-tain the colony, they were allowed to feed and then were introduced into a new cagewith trees infested with CLM eggs and early instar larvae. Adult

A. citricola

only livefor 2 to 5 days, so they must be used for colonies or shipped to growers as soon as theyare collected.

Problems Encountered

. We encountered several problems in rearing

A. citricola

.Initial attempts to rear the parasitoids in a rearing room or in a shaded alcove failedto produce progeny, possibly because light intensity was low. Cages were then heldwithin a greenhouse with a relative humidity below 60%. In an attempt to increaserelative humidity, plastic sheeting was placed over the cages and a humidifier wasplaced under the greenhouse bench. These cages also did not produce wasps, possiblydue to the high temperatures (>38

°

C) that were reached under the plastic.Adult

A. citricola

are small (<2 mm) and difficult to collect from the cages becausethey tend to rest on the foliage and do not go to the top of the cage. High rates of adult

A. citricola

emergence were achieved by placing leaves with parasitized CLM pupaeinto inflated plastic bags, in a manner similar to that used to obtain adult CLM emer-gence. Adult parasitoids could easily be aspirated from the bags. One problem withplastic bags is the amount of condensation that develops on the inside.

A. citricola

areeasily trapped and die in free moisture, so the bags must be wiped dry at least once aday.


C. quadristriatus

is an ectoparasitoid of late instar larvae of the CLM (Beattie1992; Hoy & Nguyen 1994c) producing a single individual per host. Both males andfemales are produced. Under our conditions, foliage inoculated with CLM reached thesuitable host stage in 7 to 10 days. Trees with third and fourth instar larvae were wa-tered and transferred into a new cage. Because adults live for almost 2 weeks, a mixedage class of trees was added to the cages (same size as used with the CLM). One thirdof the cage was filled with trees that had been infested with CLM for 7 to 10 days. Wethen added 50 to 75 adult wasps (unknown sex ratio, extremely difficult to sex) to thecage. After 2 days, another third of the cage was filled with new trees that were 7 to10 days old. The last third was filled after another 2 days. Honey was streaked everyother day on plastic sheets suspended in the cages and the plants were watered whenneeded. These cages were held in the citrus greenhouse.

Adult

C. quadristriatus

began emerging 11 to 13 days after they were introducedinto the cages. Adults were aspirated from the cage every afternoon, when the waspswere most active.

C. quadristriatus

are easy to locate in cages due to their large size,orange color, and because they typically rest on the top of the leaves. After allowingthe wasps to emerge in the cage for approximately one week, leaves with intact pupalchambers were pruned off each plant and placed in plastic bags to allow additional

C.quadristriatus

adults to emerge. This procedure was adopted to allow early wasps toemerge while allowing later larvae to continue to develop. Adult parasitoids were fedwith a honey-soaked piece of tissue or by streaking thin lines of honey in the vial.


607

Adult

C. quadristriatus

can be held longer before being supplied to growers or usedin colony maintenance because they live for approximately 2 weeks. The adults wereplaced in a growth chamber held at 19

°

C until they were used or shipped in the samemanner as

A. citricola

. If held for a longer period of time, the adults were suppliedwith fresh honey every 48 hours.

R

ESULTS

AND

D

ISCUSSION

Citrus Leafminer

A mean of 1426

±

168 (

±

SD) intact pupal chambers were produced in each cage.The average number of leaves infested per tree was 10.2

±

7.9, with a range from 0 to35 leaves. The average number of CLM pupae produced per leaf was 2.8

±

1.8. Themaximum number of pupal chambers on one leaf was 13. Approximately the samenumber of pupal chambers were located on the lower surface of the leaf (1.8

±

1.1) ascompared to the upper surface (1.1

±

1.0).


Between April and October, the productivity of cages (n=21) used to rear

A. citri-cola

was evaluated. An average of 750 adults (

±

410) was produced from 18 to 24 potscontaining an average number of 60 trees in each cage. The maximum number ofadults from a single cage was 1491, while the minimum was 109. One to ten

A. citri-cola

develop from a single CLM pupa; the average number of

A. citricola

individualsemerging per CLM pupal chamber in our greenhouse cages was 2.8

±

1.1.


Since their release from quarantine in late July, an average of 144 (

±

25.8) parasi-toids have been reared from each of 9 cages, each containing approximately 60 trees.The maximum number of adults obtained from a single cage was 171 while the mini-mum was 101. Reasons for low rate of production of these parasitoids are unknown.We do not know how many eggs are laid by each female or the preferred relative hu-midity. Also, as already stated, only one

C. quadristriatus

is produced per host.

C

ONCLUSIONS

The methods described provide parasitoids for inoculative releases, but do not al-low large scale augmentative releases. Rearing is time consuming and expensive be-cause 3 trophic levels must be maintained. A total of 15,230

A. citricola

were rearedbetween April and October 1994, and 1328

C. quadristriatus

were reared between late

July and October 1994. This required 225.7 m

2

in greenhouse and shadehouse space,approximately 2,500 citrus trees, and one full-time employee devoted solely to thisproject (plus some hours performed by other employees). The potential for augmenta-tive releases would be improved if an artificial diet was available either for the CLMor the parasitoids.

A

CKNOWLEDGMENTS

We thank Ru Nguyen for his advice on rearing and his efforts in rearing the para-sitoids in the quarantine facilities. We thank Owain Edwards for advice and assis-

608



tance and Juan Villanueva-Jiménez for the spanish translation of the abstract.Ayyamperumal Jeyaprakash, Denise Johanowicz, Mark Pomerinke, Jim Presnail,Shawn Rogers, and three anonymous reviewers provided advice on the manuscript.This work was funded in part by the Citrus Production Research Advisory Council.This is journal series number R-04482.

R

EFERENCES

C

ITED

B

A

-A

NGOOD

, S. A. S. 1977. A contribution to the biology and occurrence of the citrusleafminer,


Staint., in the Sudan. Zeit. Angew. Entomol. 83:106-111.

B

ADAWY

, A. 1967. The morphology and biology of


Staint., a citrusleaf-miner in the Sudan. Bull. Soc. Entomol. Egypte LI: 95-103.

B

EATTIE

, G. A. C. 1992. Biological control of citrus leaf miner - introduction and re-lease of natural enemies. Final Report Project C/0031, NSW Agriculture.

B

EATTIE

, G. A. C.,

AND

D. S

MITH

. 1993. Citrus leafminer. Agfact H2.AE.4, second edi-tion. NSW Agriculture.

E

VANS

, G. A. 1995. Discovery of the male of


(Hymenoptera: En-crytidae) parasitoid of the citrus leafminer

Phyllocnistis citrella (Lepidoptera:Gracillaridae). Florida Entomol. 78: 134-136.

HEPPNER, J. B. 1993. Citrus leafminer (CLM) Phyllocnistis citrella Stainton. FloridaState Collection of Arthropods, DPI/FDACS.

HOY, M. A., AND R. NGUYEN. 1994a. Classical biological control of the citrus leafminerin Florida. Citrus Industry, April: 22, 25.

HOY, M. A., AND R. NGUYEN. 1994b. Classical biological control of the citrus leafminerin Florda: a progress report. Citrus Industry, June: 61-62.

HOY, M. A., AND R. NGUYEN. 1994c. Classical biological control of the CLM: release ofCirrospilus quadistriatus. Citrus Industry, November: 14.

LOGVINOVSKAYA, T. V. 1983. A new species of Ageniaspis Dahlbom 1857 (Hy-menoptera, Encryrtidae) from Vietnam. Entomol. Rev. 62: 150-152.

PANDEY, N. D., AND Y. D. PANDEY. 1964. Bionomics of Phyllocnistis citrella Stt. (Lep-idoptera: Gracillariidae). Indian J. Entomol. 26: 417-422.

SOHI, G. A. S., AND M. S. SANDHU. 1968. Relationship between Citrus leaf-miner(Phyllocnistis citrella Stainton) injury and citrus canker (Xanthomonas citri(Hasse) Dowson) incidence on Citrus leaves. J. Res. Punjab Agric. Univ. 5: 66-69.

SOHI, G. A. S., AND G. C. VERMA. 1965. Feeding habits of Phyllocnistis citrella Stain-ton in relation to the anatomical structure of the leaf. Indian J. Entomol. 27:483-485.

Scientific Notes

609

OBSERVATIONS OF PREDATION ON ALATE QUEENS OF THE RED IMPORTED FIRE ANT (HYMENOPTERA: FORMICIDAE) BY THE BLACK AND YELLOW GARDEN SPIDER (ARANEAE:

ARANEIDAE)

T

IMOTHY

C. L

OCKLEY

USDA-APHIS-PPQ-IFA, 3505-25th Avenue, Gulfport, MS 39501

There are a number of published records of predation on the newly mated queensof the red imported fire ant,

Solenopsis invicta

Buren, including attacks on foundingqueens by numerous insectivorous predators (Edwards et al. 1974, Glancey 1981, Lu-cas & Brockman 1981, Nichols & Sites 1991). Whitcomb et al. (1973) listed 22 verte-brate and invertebrate predators. Among these, only one spider

Lycosa timuga

Wallace was observed feeding on founding queens. Nyfeller et al. (1988) collected theremains of 34

S. invicta

queens from the webs of 100

Latrodectus mactans

(F.) spidersin cotton fields. Red imported fire ant queens made up over 15% of the total prey of

L.mactans

. In the same study, 16 additional spiders from eight families were listed aspredators of red imported fire ants. Of these, only two (

Neoantistea

sp. and

Phidippusaudax

) were observed with

S. invicta

queens as prey.Beginning at 1015 hours on 23 August 1990, a single black and yellow garden spi-

der,

Argiope aurantia

Lucas, was observed capturing alate red imported fire ant fe-males in flight. The spider, a penultimate female, had established her vertical webapproximately 1.0 m (at its center) above and 1.0 m to the northeast of an active

S. in-victa

mound [category 9 on the Lofgren & Williams (1982) scale]. The spiraled area ofthe web covered an area of approximately 0.8 m. Prevailing winds placed the spider’sweb directly downwind of the mound. Alate females were seen emerging from the col-ony, ascending adjacent plants (primarily wild grasses and a wild sparkelberry bush

Vaccinium arboreum

Marsh.) before launching themselves into the air. During a pe-riod of 30 min, 275 alate females were observed leaving the mound by flight. Duringthis same period, the garden spider snared 37 ants. For the first twelve min of this ac-tivity, the spider reacted to the arrival of the alate females by rushing to the point ofweb contact and quickly subduing the prey by swathing it with silk. Twenty-four ofthe alates were handled in this manner. Nine of these were first envenomated by thespider before swathing. The remaining 15 were either bitten after swathing or, as wasthe case for the last 5 taken, merely swathed without a bite. The final 13 alates to con-tact the web were handled differently from the first twenty-four. The spider reacted byjerking the web to dislodge the prey (n=5). Failing to dislodge the prey, the spiderwould cautiously approach the captured queen and carefully sever the lines to whichthe ant was attached to the web allowing it to drop from the web to the ground strata(n=8). Ants that were shaken from the web climbed an adjacent plant and again tookflight (one of which was again caught in the web). Those alates severed from the webwere unable to regain flight and, upon closer examination, were found to have web-bing attached to their wings and body.

Research into biological control of imported fire ants has concentrated on patho-gens and parasitoids almost to the exclusion of generalist predators (Allen 1980, Jou-venaz 1983, Jouvenaz et al. 1980, Williams 1980, Williams & Whitcomb 1974).Although only a single observance, a 15% reduction by a spider in alate females re-ported here may represent a more widespread and frequent phenomena. Furtherstudy of the potential of such generalist predators as biocontrol agents of

S. invicta

should be encouraged.

610



S

UMMARY

The serendipitous placement of an

Argiope aurantia

web in the direct flight pathof emerging alate fire ants succeeded in disrupting the mating flight of approximately15% of the observed queens, either through direct predation or indirectly by hamper-ing their ability to fly (capture and release).

R

EFERENCES

C

ITED

A

LLEN

, G. E.,

AND

J. D. K

NELL

. 1980. Pathogens associated with the

Solenopsis sae-vissima

complex in South America. Proc. Tall Timbers Conf. Ecol. Anim. Con-trol Habitat Manag. 7: 87-94.

E

DWARDS

, G. B., J. F. C

ARROLL

,

AND

W. H. W

HITCOMB

. 1974.

Stoidis aurata

, a spiderpredator of ants. Florida Entomol. 57: 337-346.

G

LANCEY

, B. M. 1981. Two additional dragonfly predators of queens of the red im-ported fire ant,

Solenopsis invicta

Buren. Florida Entomol. 64: 194-195.J

OUVENAZ

, D. P. 1983. Natural enemies of fire ants. Florida Entomol. 66: 111-121.J

OUVENAZ

, D. P., W. A. B

ANKS

,

AND

J. D. A

TWOOD

. 1980. Incidence of pathogens in fireants,

Solenopsis

spp., in Brazil. Florida Entomol. 63: 345-346.L

OFGREN

, C. S.,

AND

D. F. W

ILLIAMS

. 1982. Avermectin B1a: a highly potent inhibitorof reproduction by queens of the red imported fire ant (Hymenoptera: Formi-cidae). J. Econ. Entomol. 75: 798-803.

L

UCAS

, J. R.,

AND

H. J. B

ROCKMAN

. 1981. Predatory interactions between ants andantlions. J. Kansas Entomol. Soc. 54: 228-232.

N

ICHOLS

, B. J.,

AND

R. W. S

ITES

. 1991. Ant predators of founder queens of

Solenopsisinvicta

(Hymenoptera: Formicidae) in Central Texas. Environ. Entomol. 20:1024-1029.

N

YFELLER

, M., D. A. D

EAN

,

AND

W. L. S

TERLING

. 1988. The southern black widow spi-der,

Latrodectus mactans

(Araneae: Theridiidae), as a predator of the red im-ported fire ant,

Solenopsis invicta

(Hymenoptera: Formicidae), in Texas cottonfields. J. Appl. Entomol. 106: 52-57.

W

HITCOMB

, W. H., A. B

HATKAR

,

AND

J. C. N

ICKERSON

. 1973. Predators of

Solenopsisinvicta

queens prior to successful colony establishment. Environ. Entomol. 2:1101-1103.

W

ILLIAMS

, R. N. 1980. Insect natural enemies of fire ants in South America. Proc. TallTimbers Conf. Ecol. Anim. Control Habitat Manag. 5: 123-124.

W

ILLIAMS

, R. N.,

AND

W. H. W

HITCOMB

. 1974. Parasites of fire ants in South America.Proc. Tall Timbers Conf. Anim. Control Habitat Manag. 5:49-59.

Scientific Notes

611

RANGE EXTENSION OF

DIADITUS TEJANUS

(HETEROPTERA: REDUVIIDAE)

J. E. M

C

P

HERSON

1

, R. C. F

ROESCHNER

2

A

ND

R. W. S

ITES

3

1

Department of Zoology, Southern Illinois University, Carbondale, IL 62901

2

Department of Entomology, National Museum of Natural History, Washington, D.C. 20560

3

Wilbur R. Enns Entomology Museum, Department of Entomology, University of Missouri, Columbia, MO 65211

Diaditus tejanus

was described in 1980 by Giacchi, who listed it from Mexico (Te-hauantepec, Oaxaca; Chuminopolis, Yucatan) and Texas (Alvin, Brownsville, Mer-cedes). This species represented only the second of the genus reported from Americanorth of Mexico.

D. pictipes

, described by Champion in 1898, is known from Guate-mala, Mexico, and Texas (Giacchi 1982). Nothing else has been published on the biol-ogy of either species.

Recently, while examining material from the entomology collections at the Univer-sities of Missouri and Mississippi, we discovered 25 specimens of

D. tejanus

that hadbeen collected in Florida and Mississippi. These collection records represent an east-ward range extension from Alvin to Highlands Co., Florida (see below), of approxi-mately 1,300 km, and a northeastern extension from Yucatan to Highlands Co. ofapproximately 1,100 km. These distribution records, along with those of Giacchi(1980, 1982), suggest that the range of this species may be restricted by coastal fac-tors, because all records are from Florida to Mexico along the Gulf Coast and acrossthe isthmus of Mexico at Tehuantepec.

The label information and repositories for these specimens are given below; collec-tion abbreviations include: University of Missouri-Columbia, UMC; University ofMississippi, UMISS; Southern Illinois University at Carbondale, SIUC; and NationalMuseum of Natural History, NMNH:

MISSISSIPPI: Hancock Co., Pt. Clear Island, 12-VIII-1986, Paul K. Lago (Coll.) (5

??

), Sam Testa (Coll.) (4

??

); same label information other than date, 15-VIII-1986,Paul K. Lago (Coll.) (6

??

), Sam Testa (Coll.) (3

??

); Hancock Co., 1.5 mi SW lake-shore, 12-VIII-1986, Sam Testa (1

?

) (all specimens, UMISS).FLORIDA: Highlands Co., Highlands Hammock St. Pk., black light, 30-III-1979,

E. Riley & D. LeDoux (Coll.) (1

?

, UMC); Gadsden Co., 15 mi SW Quincy, 21-VIII-1992, R. Beiriger (Coll.) (1

?

, 1

/

, NMNH; 1

?

, SIUC; 2

??

, UMC).We thank Paul K. Lago, Department of Biology, University of Mississippi, Univer-

sity, for the loan of the Mississippi specimens mentioned above.

S

UMMARY

The geographic range of

Diaditus tejanus

Giacchi, based on 25 specimens, is ex-tended eastward in the United States from Texas through Mississippi to Florida.

R

EFERENCES

C

ITED

C

HAMPION

, G. C. 1897-1901. Insecta: Rhynchota (Hemiptera-Heteroptera). Vol. II,

in

Goodwin and Salvin [eds.]. Biologica Centrali-Americana. London. 1898: 33-192.

612



G

IACCHI

, J. C. 1980. Una nueva especie para el genero

Diaditus

Stal, 1859 (Stenopo-dainae-Reduviidae). Revista Sociedad Entomologia Argentina 39 (1-2): 1-4.

G

IACCHI

, J. C. 1982. Revision de los stenopodainos americanos. V. El genero

Diaditus

Stal, 1859 (Heteroptera, Reduviidae). Physis (Buenos Aires), Secc. C., 41(100):

♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦

9-27.

Scientific Notes

615

PARASITISM OF

ORCHELIMUM

KATYDIDS (ORTHOPTERA: TETTIGONIIDAE) BY

ORMIA

LINEIFRONS

(DIPTERA: TACHINIDAE)

L

EO

S

HAPIRO

Dept. of Ecology and EvolutionState University of New YorkStony Brook, NY 11794-5245

In the course of keeping

Orchelimum

katydids (Tettigoniidae: Conocephalinae)collected as nymphs and adults from the southeastern U.S. and Washington, D.C., Ihave obtained a small number of puparia of a parasitic tachinid fly, as follows: two pu-paria from a single adult male

O

.

agile

from Gainesville, FL; one puparium from anearly instar female

O

.

pulchellum

from Appling, Columbia Co., GA; one pupariumfrom an adult male

O

.

silvaticum

and one puparium from an adult male

O

.

pulchellum

from Montgomery, AL; one puparium from an adult male

O

.

pulchellum

from Gautier,MS; one puparium from an adult male

O

.

nigripes

from Fairview-Riverside StatePark, LA; and one puparium from an early instar female

O

.

pulchellum

from Wash-ington, D.C. The host exhibits a characteristic syndrome in response to the parasite:the katydid (nymph or adult) becomes sluggish and a distinct bulge develops in theabdomen. Within a few days, a puparium appears outside of the katydid and the ka-tydid dies.

Three of the pupae were reared in the laboratory (from Louisiana

O. nigripes

, Mis-sissippi

O. pulchellum

, and Alabama

O. pulchellum

) and a representative adult (fromthe Louisiana

O. nigripes

) was identified as

Ormia

lineifrons

. The identified fly hasbeen deposited in the collection of the U.S. National Museum. Since an adult fly wasactually reared and identified only from a single

O

.

nigripes

, the association of

Ormialineifrons

with the other parasitized

Orchelimum

species (

O. pulchellum, O. silvati-cum,

and

O. agile

) must remain tentative, although all the puparia and reared adultsappeared to be the same. The only hosts previously known for this fly are

Neocono-cephalus

katydids, especially

N

.

triops

(T. J. Walker 1994

in litt

., Burk 1982). Accord-ing to Burk (1982),

O. lineifrons

is attracted to tape recordings of the calling song of

N

.

triops

; Walker reports (

in litt.

) that each year

O. lineifrons

is attracted in smallnumbers to mole cricket (

Scapteriscus

vicinus

) sound trapping stations, although itdoes not parasitize mole crickets. (A Brazilian

Ormia

species is currently being usedas a biocontrol agent for this introduced cricket in Florida.)

While some acoustically orienting tachinids apparently depend almost entirely onhost calling song to locate hosts (e.g., Lakes-Harlan & Heller 1992), this reliance oncalling song to locate individual hosts is not always so complete (e.g., Walker & Win-eriter 1991). Given that two of seven parasitized

Orchelimum

were nymphs (andhence silent),

O. lineifrons

apparently does not depend strongly (perhaps does not de-pend at all) on song to find individual

Orchelimum

hosts, although it could be that fe-male flies are attracted to the general area around calling males. In the absence ofplayback experiments using

Orchelimum

songs and gravid

O. lineifrons

females, it isimpossible to assess precisely the role of calling song in

O. lineifrons

host searchingbehavior. It may be that

O. lineifrons

orients acoustically to

Neoconocephalus

(Burk1982), the

primary host, while other katydids are attacked opportunistically. Ob-served rates of tachinid parasitism of

Orchelimum

are very low.Tachinid parasitism of

Orchelimum

katydids has been reported previously onlyvery briefly and generally by Feaver (1983), who observed in her Michigan study pop-

616



ulation two

O. nigripes

individuals that had been parasitized by an undetermined ta-chinid. In this note I report the first specific identification of a tachinid parasite of

Orchelimum

.I thank Dr. N. Woodley of the Systematic Entomology Laboratory of the U.S.D.A.

for identifying the fly and Dr. T. J. Walker for providing information on flies, katydids,and crickets. I thank D. J. Funk, M. C. Keese, T. J. Walker, and an anonymous reviewerfor their valuable comments on this manuscript. My

Orchelimum

work has been sup-ported by the National Science Foundation, the Washington Biologists’ Field Club, theExplorers’ Club, the Theodore Roosevelt Fund of the American Museum of NaturalHistory, the Sigma Xi Scientific Society, and the Florida Entomological Society.

S

UMMARY

Ormia lineifrons

was identified as a parasite of

Orchelimum nigripes

(and, tenta-tively, of several other species of

Orchelimum

katydids), inhabiting both nymphs andadults. These observations document both a new host genus for

O. lineifrons

and thefirst specific identification of a tachinid from

Orchelimum

.

R

EFERENCES

C

ITED

B

URK

, T. 1982. Evolutionary significance of predation on sexually signalling males.Florida Entomol. 65: 90-104.

F

EAVER

, M. 1983. Pair formation in the katydid

Orchelimum nigripes

(Orthoptera:Tettigoniidae), pp. 205-239

in

D. T. Gwynne and G. K. Morris [eds.], Ortho-pteran Mating Systems: Sexual Competition in a Diverse Group of Insects.Westview Press, Boulder, CO.

L

AKES

-H

ARLAN

, R.,

AND

K.-G. H

ELLER

. 1992. Ultrasound-sensitive ears in a parasi-toid fly. Naturwissenschaften 79: 224-226.

W

ALKER

, T. J.,

AND

S. A. W

INERITER

. 1991. Hosts of a phonotactic parasitoid and lev-els of parasitism (Diptera: Tachinidae:

Ormia ochracea)

. Florida Entomol. 74:554-559.

Scientific Notes

617

THE SUGARCANE DELPHACID (HOMOPTERA: DELPHACIDAE) EXTENDS ITS NORTH AMERICAN RANGE

INTO LOUISIANA

W. H. W

HITE

1

, T. E. R

EAGAN

2

A

ND

O. S

OSA

, J

R

.

3

1

USDA-ARS, Sugarcane Research UnitP.O. Box 470, Houma, LA 70361-0470

2

Department of EntomologyLouisiana State University

Life Science Bldg., Baton Rouge, LA 70803-1710

3

USDA-ARS, Sugarcane Production ResearchStar Rte. Box 8, Canal Point, FL 33438

The sugarcane delphacid,

Perkinsiella saccharicida

Kirkaldy, an insect pest of sug-arcane, was first discovered in Louisiana on October 19, 1994, in a sugarcane field ap-proximately 58 km southeast of Lafayette. Identification was provided by F. W. Mead,Florida Department of Agriculture, Division of Plant Industry, P.O. Box 1269, Gaines-ville, FL 32614.

The sugarcane delphacid is a recent introduction to North America having beenfirst reported in Florida in 1982 (Sosa 1985), Georgia in 1983 (Nguyen 1984), Texas in1989 and Mexico in 1991 (Meagher et al. 1991). The sugarcane delphacid is probablynative to Papua, New Guinea, but with the movement of sugarcane, it is widespreadin Java, Taiwan, southern China, Malaysia, and eastern Australia. It is also estab-lished in the Hawaiian Islands, Mauritius, Reunion, Madagascar, and South Africa(Fennah 1969). In the Western Hemisphere, Risco (1969) reported the sugarcane del-phacid in Ecuador in 1966 and in Peru in 1967. Feeding by nymphs and adult ovipo-sition cause some plant damage (Allsopp & Bull 1990), but of principal concern is theinsect’s ability to vector

Fijivirus

sp., the causal agent of Fiji disease (Francki & Griv-ell 1972).

After the initial discovery of the pest in Louisiana, the sugarcane producing par-ishes (counties) of Louisiana were sampled during November 1994 to determine sug-arcane delphacid population densities and geographic distribution within the state.One to four fields were sampled per parish in each of 20 sugarcane producing par-ishes. These 20 parishes comprised about 159,296 ha of cultivated sugarcane. Fieldsof harvestable cane (about 3.8 m tall), uniformly spaced within each parish (about 8km apart), were selected for survey. Visual counts of nymphs and adults were madeon 4 sugarcane stalks at 10 sites about 3 m apart along one or two field edges. Addi-tionally, one leaf (3-5 down from the whorl) was examined for oviposition.

The sugarcane delphacid was found in 22 of the 60 fields sampled and in 13 of the20 parishes sampled. The sugarcane in these 13 parishes comprises 79% (about125,821 ha) of the total sugarcane cultivated in Louisiana. Numbers of individuals(adults + nymphs) per locations ranged from 0 to 12. The highest density was 0.3 perstalk in a field in St. Mary Parish. When the sugarcane delphacid was initially foundin Florida, densities ranged from 0.5 per stalk to 35.7 per stalk (Sosa 1985). No ovipo-sition was detected; oviposition was obviously occurring but apparently at such lowlevels that it was not detected.

Although the sugarcane delphacid was found in very low numbers, our survey de-tected an infestation gradient with the highest populations found in the coastal par-ishes and decreasing density in the inland parishes (Fig. 1). Immatures were, ingeneral, found in parishes with high adult numbers.

618



Densities of the sugarcane delphacid remained low in Louisiana sugarcane fieldsthrough the winter. Sweep net samples taken from 100 fields in late May and earlyJune of 1995 did not detect any adults or nymphs. Because of potential of the sugar-cane delphacid to become an economic pest, we will continue monitoring field densi-ties and geographic distribution of this insect in Louisiana.

Thanks are extended to Lance Rodriguez, Louisiana State University AgriculturalCenter, Baton Rouge, LA and Griffin Bell, USDA-ARS, Canal Point, FL for technicalsupport. Voucher specimens were deposited in the Louisiana State University InsectCollection and the Florida Department of Agriculture, Division of Plant Industry,Gainesville, FL.

S

UMMARY

The sugarcane delphacid,


Kirkaldy, was discovered inLouisiana, 19 October 1994. This insect is a new record for Louisiana and was foundin 13 of 20 sugarcane producing parishes surveyed.

R

EFERENCES

C

ITED

A

LLSOPP

, P. G.,

AND

R. M. B

ULL

. 1990. Sampling distributions and sequential sam-pling plans for


Kirkaldy (Hemiptera: Delphacidae)and

Tytthus

(Hemiptera: Miridae) on sugarcane. J. Econ. Entomol. 83: 2284-2289.

Figure 1. Distribution of the sugarcane delphacid in Louisiana sugarcane. Group-ings in legend are based on the mean total number of adults and nymphs per locationwithin a parish.

Scientific Notes

619

F

ENNAH

, R. G. 1969. Damage of sugarcane by fulgoridea and related insets in relationto the metabolic state of the host plant, pp. 367-389

in

J. R. Williams, J. R. Met-calfe, R. W. Mungomery and R. Mathes [eds.] Pests of sugar cane Elsevier Pub.Co., Amsterdam.

F

RANCKI

, R. I. B.,

AND

C. J. G

RIVELL

. 1972. Occurrence of similar particles in Fiji dis-ease virus-infected sugar cane and insect vector cells. Virol. 48: 305-307.

M

EAGHER

, J

R

., R

OBERT

, S

TEPHEN

W. W

ILSON

, R. S. P

FANNENSTIEL

,

AND

R. G.B

REENE

. 1991. Documentation of two potential insect pests of south Texas sug-arcane. Southwestern Entomol. 16: 365-366.

N

GUYEN

, R

U

, O. S

OSA

, J

R

.,

AND

F. W. M

EAD

. 1984. Sugarcane delphacid,

Perkinsiellasaccharicida

Kirkaldy 1903 (Homoptera: Delphacidae). Florida Dept. Agric. &Consumer. Serv. Entomology Circular 265.

R

ISCO

, S. H. 1969. Notas adicionales sobre el “saltahoja” de la caña de azucar

Perkin-siella saccharicida

K. Revista Peruana de Entomol. 9: 181-187.S

OSA

, J

R

., O. 1985. The sugarcane delphacid,


(Homoptera:Delphacidae), a sugarcane pest new to North America detected in Florida. Flor-

♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦

ida Entomol. 68: 357-360.

Scientific Notes

619

LARRA BICOLOR

(HYMENOPTERA: SPHECIDAE), A BIOLOGICAL CONTROL AGENT OF

SCAPTERISCUS

MOLE CRICKETS (ORTHOPTERA: GRYLLOTALPIDAE),

ESTABLISHED IN NORTHERN FLORIDA

J. H. F

RANK

, J. P. P

ARKMAN

AND

F. D. B

ENNETT

1

Entomology & Nematology Department, University of Florida,Gainesville, FL 32611-0620, USA

1

Current address: Crofton, Baldhoon Road, Laxey,Isle of Man IM4 7NA, United Kingdom

Larra

is a largely tropical genus of digger wasps (Sphecidae) with atypical behav-ior. Typical sphecid females sting and paralyze other arthropods which then are takento cells where they serve as food for larvae.

Larra

females attack and sting mole crick-ets (Gryllotalpidae), which suffer paralysis for only a few minutes. The

Larra

femalesoviposit on the mole crickets that they have paralyzed, and the neonate larvae developas external parasitoids on active hosts (Bohart & Menke 1976). The only known hostsof

Larra

are mole crickets.

Larra analis

F. is the only species native to coastal southeastern USA, and its hostis

Neocurtilla hexadactyla

(Perty), the only mole cricket native to this region. Threeimmigrant species of mole crickets of the genus

Scapteriscus

arrived in the southeast-ern USA about 1900. Tens of thousands of these

Scapteriscus

mole crickets have beenexamined by personnel of the University of Florida’s mole cricket research programsince 1978, but none was found with an egg or larva of

L. analis

. This is strong evi-dence that

L. analis

does not attack

Scapteriscus

spp. in nature.Some mole cricket species are pests of agriculture and horticulture. Notable exam-

ples are

Gryllotalpa orientalis

Burmeister in Hawaii,

Scapteriscus didactylus

(La-treille) in Puerto Rico and some other West Indian Islands, and

Scapteriscus vicinus

Scudder,

S. abbreviatus

Scudder, and

S. borellii

Giglio-Tos in the southern USA

620



(Frank 1994). These five species are immigrants in these areas and have been subjectto classical biological control, i.e., the attempted introduction of natural enemies fromtheir homelands into the areas where they are immigrants.

The earliest attempts at classical biological control of mole crickets used species of

Larra

.

Larra amplipennis

(F. Smith) introduced in 1921 from the Philippines and

L.bicolor

F. introduced in 1924 from Brazil did not become established in Hawaii, but

L.polita

(F. Smith) subspecies

luzonensis

Rohwer, introduced in 1925 from the Philip-pines, did become established (Williams 1928, Bohart & Menke 1976).

Larra bicolor

,introduced from Belem, Pará, Brazil, became established in Puerto Rico by 1941 (Wol-cott 1938, 1941). We have discovered no assessment of the effectiveness of these waspsin suppressing mole cricket populations in Hawaii and Puerto Rico.

An attempt was made in the 1940s to introduce

L. bicolor

into Florida, summa-rized by Frank (1990). Plantings were made of

Spermacoce verticillata

L. and

Hyptisatrorubens

Poit. (nectar-bearing plants favored by

L. bicolor

) at Gainesville, and flow-ers of the latter attracted

L. analis

. Unfortunately,

L. bicolor

adults and larvaeshipped from Brazil were dead on arrival in Florida and the attempt was not repeatedin that decade.

A renewed effort was made to import

L. bicolor

into Florida beginning in 1979 un-der the leadership of R. I. Sailer, as part of the University of Florida’s mole cricket re-search program. J. L. Castner, H. G. Fowler, W. G. Hudson, and J. R. Reinert(University of Florida) and E. Abreu (University of Puerto Rico) participated. PuertoRican populations were surveyed and five sites for release were identified in Florida;these sites were prepared with plantings of


. In 1981, scores offemale wasps were released at Ft. Lauderdale, Gainesville, and Tampa, in 1982 atBradenton and Ft. Lauderdale, and in 1983 near Lakeland. However, a population of

L. bicolor

became established only at Ft. Lauderdale (Sailer 1985, Frank 1990).By late 1984, the Ft. Lauderdale

L. bicolor

population occupied two sites: a golfcourse, and the University of Florida’s Agricultural Research Station, about 1 km dis-tant. Attempts to expand the population to additional sites were unsuccessful (Cast-ner 1988a). Mole crickets were trapped to assess the proportion infected with eggs orlarvae of

L. bicolor

. Only

S. abbreviatus

were found infected; however, the combinednumber of trapped

S. borellii

and

S. vicinus

accounted for only 15% of the total (n =677) collected in pitfall traps (Castner 1988a). Only 1% of mole crickets examinedwere infected with eggs or larvae (Castner 1988a). Establishment of

L. bicolor

only atFt. Lauderdale and not at the four more northerly sites in Florida suggested that thiswasp, of tropical origin, could not withstand colder or longer winters farther north inFlorida. This theory was supported by poor survival of wasp pupae overwintered out-doors experimentally at Gainesville (Castner 1988a).

F. D. Bennett joined the mole cricket research program in 1985. He shared J. L.Castner’s view that “Puerto Rican”

L. bicolor

had not become established in northernFlorida because of the equatorial origin of this biotype at low altitude in Belem. Hethought that a

Larra

stock from southern South America, or from high altitude else-where in South America, might be better adapted to survive in northern Florida. Al-though

Larra

females of other species had been observed to attack

Scapteriscus

molecrickets in South America (i. e., Uruguay and southern Brazil), only small numbers ofthese other

Larra

had been observed, and their identity was tenuous due to incom-plete systematic treatment (Frank 1990). Bennett began studies on

Larra

with C. J.Pruett at Santa Cruz de la Sierra, Bolivia, where species attributed to

L. bicolor

and

L. braunsii

Kohl (and perhaps a third species) occurred (Frank 1990). By this time, A.S. Menke was revising Neotropical

Larra

. His identifications convinced Bennett andPruett that they were dealing with

L. bicolor

and

L. praedatrix

(Strand), on which

Scientific Notes

621

they published behavioral notes (Bennett & Pruett 1991, Pruett & Bennett 1991).Live

Larra

were brought to Florida for release in Alachua County in 1988-1989. It islikely that specimens of three species,

L. bicolor

,

L. praedatrix

, and

L. godmani

Cam-eron (senior synonym of

L. braunsii

Kohl), were imported and released, but in un-known proportions. Female

L. praedatrix

and

L. bicolor

are not distinguishable withcertainty (Menke 1992).

The release sites were as follows: Micanopy, about 10 km south of Gainesville (Oc-tober 1988) where 175

/

wasps, 35

?

wasps, and 80 mole crickets bearing

Larra

eggswere released; the North Florida Regional Medical Center, Gainesville (March andMay 1989) where 86

/

wasps, 24

?

wasps, and 29 mole crickets bearing

Larra

eggswere released; and the University of Florida Honey Plant, Gainesville (June 1989)where 13

/

wasps and 23

?

wasps were released. The Honey Plant site was the samelocation where

L. bicolor

had been released by R. I. Sailer in 1981. This site containedthe original plot of


planted by Sailer.


plants were brought from Miami to Gainesville in 1987 byJ. H. Frank and maintained in pots. These plants were established in 1991 at thesoutheast corner of the new Entomology/Nematology building of the University, about2 km northwest of the Honey Plant. In 1992, A. S. Menke published his major revisionof Neotropical

Larra

, allowing reliable identification for the first time. No

Larra

wereobserved in Gainesville before the retirement of F. D. Bennett in July 1993 and his de-parture from Florida.

In October 1993, Entomology/Nematology Dept. technician J. A. Gillmore reportedobserving a wasp attack a mole cricket outside the departmental building.

Larra

adults were then observed feeding on flowers of


in the plot atthe southeast corner of the building. Dissection and microscopic examination revealedthat these were

L. bicolor

(not

L. analis

or

L. godmani

or

L. praedatrix

). Microscopicexamination further revealed a dense punctation of the vertex of the head typical ofspecimens from Santa Cruz, Bolivia, and not a sparse punctation typical of specimensfrom Puerto Rico (Menke 1992).

Larra

adults with the same morphological character-istics were found at the Honey Plant release site. We concluded that the wasps foundwere progeny of those released by F. D. Bennett in 1988-1989, originating from Bo-livia.

Wasps were seen at the

Spermacoce

plot at the Entomology/Nematology buildingalmost daily through the autumn of 1993. The last observation was on 9 December1993, whereafter freezing temperatures occurred and the foliage was killed by frost.The plants regenerated in spring 1994, and the first

Larra bicolor

was seen on 9 May1994. Wasps were seen occasionally in the plot during subsequent weeks to Septem-ber 1994, but at a lower density than in the autumn of 1993. Peak wasp abundance atFt. Lauderdale occurs in autumn (Castner 1988a), therefore, relatively low numbersin spring and summer are not surprising. In August 1994, a

Larra bicolor

female wasobserved by P. G. Koehler 2 km northeast of the Entomology/Nematology building atthe University of Florida track and field complex. Adult wasps have been observed atthe Entomology/Nematology building from October 1993 to September 1994. The pop-ulation has spread a distance of at least 4 km, which is greater than ever observed atFt. Lauderdale.

Life histories and behavior of

Larra analis

and of

Larra bicolor

are described bySmith (1935) and Castner (1988b), respectively. Under laboratory conditions

Larra bi-color

will sometimes attack

Neocurtilla hexadactyla

but is thwarted by the defensivesecretion of this mole cricket (Castner 1984) or the inability of the larvae to developon the host (Pruett & Bennett 1991).

Larra analis

has not been found to infect

Scap-teriscus

mole crickets under field conditions. The native wasp is specialized to the na-

622



tive mole cricket, and the introduced wasp is specialized to immigrant (pest) molecrickets of the genus

Scapteriscus

.

Larra bicolor

joins

Steinernema scapterisci

Nguyen & Smart (Rhabditida: Stein-ernematidae) and

Ormia depleta

(Wiedemann) (Diptera: Tachinidae) as South Amer-ican biological control agents established in Alachua County, Florida as naturalenemies of

Scapteriscus

mole crickets.We are grateful to L. Nong for help in handling and rearing

Larra

wasps, inducingthem to parasitize mole crickets in the laboratory, and releasing them in 1988-1989.We also thank C. J. H. Pruett and his colleagues at CIMCA, Santa Cruz, Bolivia, forhelp in collecting

Larra

, and to D. H. Habeck and T. J. Walker for critical commentson an earlier version of this text. This is Florida Agricultural Experiment Stationjournal series no. R-04082.

S

UMMARY

Larra bicolor

, a biological control agent of

Scapteriscus

mole crickets, has estab-lished a population in Gainesville, northern Florida. This population results fromspecimens collected in Santa Cruz de la Sierra, Bolivia, and released by F. D. Bennettin 1989. Previously, a Florida population of this wasp had been established only at Ft.Lauderdale in southern Florida; it resulted from releases made in the early 1980s byR. I. Sailer. The proximal origin of the Ft. Lauderdale population of

L. bicolor

is Pu-erto Rico, but its initial home of origin is Belem, Pará, Brazil.

R

EFERENCES

C

ITED

B

ENNETT

, F. D.,

AND

C. J. P

RUETT

. 1991. Observations on copulation in Florida andon the behavior of male and female wasps of the genus

Larra

in Santa Cruz, Bo-livia. Sphecos 21: 16-17.

B

OHART

, R. M.,

AND

A. S. M

ENKE

. 1976. Sphecid wasps of the world. A generic revi-sion. Univ. California Press; Berkeley.

C

ASTNER

, J. L. 1984. Suitability of

Scapteriscus

spp. mole crickets as hosts of

Larrabicolor

(Hymenoptera: Sphecidae). Entomophaga 29: 323-329. C

ASTNER

, J. L. 1988a. Evaluation of

Larra bicolor

as a biological control agent of molecrickets. PhD dissertation, Univ. Florida.

C

ASTNER

, J. L. 1988b. Biology of the mole cricket parasitoid

Larra bicolor

(Hy-menoptera: Sphecidae), pp. 423-432

in

V. K. Gupta [ed.], Advances in ParasiticHymenoptera Research. Brill; Leiden.

F

RANK

, J. H. 1990. Mole crickets and other arthropod pests of turf and pastures, pp.131-139

in

D. H. Habeck, F. D. Bennett, and J. H. Frank [eds.], Classical Bio-logical Control in the Southern United States. Southern Coop. Series Bull. 355:1-viii, 1-197.

F

RANK

, J. H. 1994. Inoculative biological control of mole crickets, pp. 467-475

in

A. R.Leslie [ed.], Integrated Pest Management for Turf and Ornamentals. LewisPublishers; Boca Raton.

M

ENKE

, A. S. 1992. Mole cricket hunters of the genus

Larra

in the New World (Hy-menoptera: Sphecidae, Larrinae). J. Hym. Res. 1: 175-234.

P

RUETT

, C. J.,

AND

F. D. B

ENNETT

. 1991. Behavior of two species of

Larra

in SantaCruz, Bolivia. Sphecos 21: 15-16.

S

AILER

, R. I. 1985. Natural enemies, pp. 23-32

in

T. J. Walker [ed.], Mole crickets inFlorida. Florida Agric. Exp. Stn. Bull. 846 (1984), 54 p.

S

MITH

, C. E. 1935.

Larra analis

Fabricius, a parasite of the mole cricket Gryllotalpahexadactyla Perty. Proc. Entomol. Soc. Washington 37: 65-82.

WILLIAMS, F. X. 1928. Studies in tropical wasps - their hosts and associates (with de-scriptions of new species). Hawaii. Sug. Plrs’ Assoc. Exp. Stn. Entomol. Ser.Bull. 19: 1-179.

Scientific Notes 623

WOLCOTT, G. N. 1938. The introduction into Puerto Rico of Larra americana Saus-sure, a specific parasite of the “changa” or Puerto Rican mole cricket, Scap-teriscus vicinus [sic]. J. Agric. Univ. Puerto Rico 22: 193-218.

WOLCOTT, G. N. 1941. The establishment in Puerto Rico of Larra americana Saus-

♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦

sure. J. Econ. Entomol. 34: 53-56.

Scientific Notes

623

A NEW SUBTERRANEAN TERMITE INTRODUCED TO FLORIDA:

HETEROTERMES

FROGGATT (RHINOTERMITIDAE: HETEROTERMITINAE)

ESTABLISHED IN MIAMI

R

UDOLF

H. S

CHEFFRAHN

AND

N

AN

-Y

AO

S

U

Ft. Lauderdale Research and Education CenterUniversity of Florida, Institute of Food & Agricultural Sciences

3205 College Avenue, Ft. Lauderdale, FL 33314

On 3 January 1995, we were asked to identify termites collected on 30 December1994 from a house in Miami. The sample, a termite-infested board and attached nestmaterial (carton) contained thousands of workers and hundreds of soldiers and youngbrachypterous nymphs. We were struck by their small size and recognized the soldiersas

Heterotermes

which are characterized by their slender and straight mandibles incontrast to the relatively thick, curved mandibles of the native

Reticulitermes

spp.[Fig. 1; also see Mathews (1977) for character diagnosis of

Heterotermes

]. The speci-mens more or less fit the brief description of

H. convexinotatus

(Snyder 1924), a widelyreported northern Neotropical species (Araujo 1977). However, the taxonomic statusof

Heterotermes

in this region is vague and in need of revision, therefore, we have notas yet assigned a species name to this find.

On 12 January 1995, we inspected the infested property, a small, older single-fam-ily house located 0.6 km east of Interstate Highway 95 and 0.3 km north of InterstateHighway 195 in the “Little Haiti” district of Miami. The

Heterotermes

infestation wascentered in a room addition which was under construction on the north side of thehouse. The addition consisted of concrete-block walls opening without a ceiling to acovered wood-truss roof. We observed extensive drywood termite damage to the roofrafters of the original house. The floor area of the addition was unfinished, consistingof fill sand on bare soil. The sand completely or partially buried numerous plywoodand solid lumber scraps. Additional scraps were scattered or stacked near the formernorth wall of the original house. Although conditions were dry, nearly all wood scrapswere under some degree of

Heterotermes

attack. Foraging tubes criss-crossed the sur-faces of some of the wood. Fist-size pieces of carton were attached to the older dam-aged wood. No foraging tubes were observed on any of the structure itself. Thecondition of the infestation and large numbers of brachypterous nymphs indicatedthat it had been active for years and had likely undergone one or more annual repro-ductive dispersal cycles.

Our suspicion that additional colonies were established in the neighborhood wereconfirmed on 30 March 1995 when several soldiers and workers were collected by apest control operator from a warehouse located about 300 m ENE from the originalsite. Unlike the original site, the warehouse showed many signs of above-ground for-

624



aging activity and damage to the structure itself. As in the original site, however, noneof the activity was associated with wet conditions or moisture sources. Foraging tubes,originating from the foundation slab, extended several meters up concrete walls. Thesmall size of the

Heterotermes

foragers may have contributed to their ability to pene-trate narrow cracks, fissures, or joints in the building’s foundation. Destruction ofwood was observed in framing, molding, and doors. Indoor workings of

Heterotermes

were spread over a 50 m distance suggesting an infestation by either one massive orseveral smaller colonies. The only damage observed outside the building was to awooden exterior door. As of this writing, dispersal flights have not been observed, noralates collected from either site. Based on our observations of

Heterotermes

in theWest Indies, fully formed alates do not appear in colonies until the beginning of therainy season (May-June).

This second infestation is important because it confirms that

Heterotermes

is well-established and thriving in a relatively large urban location and demonstrates the de-structive potential of this species. The infestation also underscores the significance of

Heterotermes

’ small size and ability to forage under dry conditions allowing it to oc-cupy a niche currently not exploited by other subterranean termite species in Florida.Our long-term expectations are that

Heterotermes

will expand its distribution well be-yond current bounds and rival the pest status of preexisting subterranean termitespecies in Dade and adjacent counties of subtropical Florida.

This is the first known successful exotic introduction of

Heterotermes

into theUnited States. These termites almost certainly originated from the West Indies or theNeotropical mainland. The only U.S. species, the native

H. aureus

(Snyder), is found

Figure 1. Soldiers of Coptotermes formosanus Shiraki (left), Heterotermes sp. (cen-ter), and Reticulitermes flavipes (Kollar) (right), all known from Dade County, Florida.

Scientific Notes

625

T

AB

LE

1.

S

IMIL

AR

ITIE

S

AN

D

D

IFF

ER

EN

CE

S

B

ET

WE

EN

N

EW

W

OR

LD

R

ET

ICU

LIT

ER

ME

S

AN

D

H

ET

ER

OT

ER

ME

S

.

Dif

fere

nce

s

Sim

ilar

itie

s

Het

erot

erm

esR

etic

uli

term

es

1.

Su

bter

ran

ean

ter

mit

es i

n t

he

Su

bfam

ily

Het

erot

erm

itin

ae1.

All

bu

t on

e sp

ecie

s N

eotr

opic

al1.

All

sp

ecie

s te

mpe

rate

or

su

btro

pica

lN

earc

tic

2.

Dif

fuse

an

d ar

chit

ectu

rall

y u

nst

ruct

ure

dsu

bter

ran

ean

nes

ts2.

For

agin

g tu

bes

and

feca

l sp

ots

ofte

ncr

eam

col

ored

2.F

orag

ing

tube

s an

d fe

cal s

pots

oft

en m

ore

brow

n.

3.

Sev

ere

stru

ctu

ral

dam

age

pote

nti

al d

ue

to la

rge

colo

nie

s an

d lo

ng-

ran

ge f

orag

ing

3.F

orag

ing

tube

s n

arro

w, s

moo

th, a

nd

mor

eci

rcu

lar

3.F

orag

ing

tube

s br

oad,

rou

gh, a

nd

flat

ter

4.

Su

perfi

cial

mor

phol

ogic

al l

iken

ess

of s

ol-

dier

an

d w

orke

r ca

stes

4.W

ell a

dapt

ed t

o dr

ier

hab

itat

s4.

Poo

rly

adap

ted

to d

rier

hab

itat

s

5.

Nes

t ca

rton

wea

k, e

asil

y br

oken

by

han

d5.

Ala

te

body

, w

ings

go

lden

br

own

; w

ing

mar

gin

s ci

liat

e; w

ing

mem

bran

e sm

ooth

,op

aqu

e

5.A

late

bod

y u

sual

ly d

ark;

win

g m

argi

ns

lack

ing

cili

a; w

ing

mem

bran

e re

ticu

late

,m

ore

clea

r6.

Dis

pers

al fl

igh

ts a

t du

sk o

r n

igh

t du

rin

gra

iny

seas

on in

late

spr

ing

or s

um

mer

6.D

ispe

rsal

flig

hts

in

su

nsh

ine

foll

owin

gra

in in

ear

ly s

prin

g7.

Sol

dier

s u

sual

ly s

mal

ler,

mor

e n

um

erou

s,an

d ag

gres

sive

7.S

oldi

ers

usu

ally

larg

er, l

ess

com

mon

, an

dap

t to

ret

reat

8.S

oldi

er m

andi

bles

str

aigh

t, s

len

der

wit

hn

arro

w b

ases

; abl

e to

cro

ss in

to “

X”

8.S

oldi

er

man

dibl

es

mor

e cu

rved

, th

ick

wit

h m

assi

ve b

ases

; u

nab

le t

o cr

oss

into

“X”

9.F

irst

mar

gin

al t

ooth

of

wor

ker/

imag

o le

ftm

andi

ble

shor

ter

than

api

cal t

ooth

9.F

irst

mar

gin

al t

ooth

of

wor

ker/

imag

o le

ftm

andi

ble

as lo

ng

as a

pica

l too

th10

.P

ostc

lype

us

of w

orke

r u

sual

ly in

flat

ed10

.P

ostc

lype

us

of w

orke

r n

ot b

ulg

ing

626



in the Sonoran and Colorado deserts of Arizona, southern California, and adjacent ar-eas of northern Mexico (Snyder 1954). Soldiers and workers of

H. aureus

are propor-tionally larger than those from the Miami discovery and are not conspecific. Like

Reticulitermes

,

Heterotermes

spp. are generally serious structural pests where theyare found. In Table 1 are listed general similarities and differences between NewWorld species of these two genera.

From a worldwide perspective,

Heterotermes

Froggatt is primarily a tropical genus(Emerson 1971) with the exception of several species in southern Australia (Hill 1942)and the aforementioned

H. aureus

. Eight species are described from throughout theNeotropical region, including three from the West Indies (Araujo 1977). Recently, ex-tensive collecting in the West Indies has cast some doubt on the validity of one or twoof the

Heterotermes

species which were described from there (Scheffrahn et al. 1994).Although occurring in drier habitats in the northern Neotropics,

Heterotermes

spp.are found in a wide range of pantropical habitats. Emerson (1971) suggests that indi-vidual species of

Heterotermes

are confined to their respective climatic zones by thelimits of soil moisture and temperature.

It is unclear why West Indian

Heterotermes

spp. have not previously become estab-lished in southern Florida or the Florida Keys, or why

Reticulitermes

spp. do not occurin the West Indies or, at least, on nearby offshore islands of the Bahamas. Since cli-matic differences between these land groups are minimal, we suspect that allopatryhas been maintained because these genera are poor candidates for introduction acrossocean barriers by natural means. Introduction of

Heteotermes

to new localities by hu-man activity is rare. Gay (1967) reports only two known cases of established human-aided introductions of

Heterotermes

;

H. perfidus

(Silvestri) from unknown origin to St.Helena about 1840, and

H. philippinensis

(Light) from the Philippines to Madagascarand Mauritius early in the 1900s. Emerson (1971) speculates that

H. convexinotatus

was introduced to the Galapagos Islands by man.In light of their broad distribution and structure-infesting potential,

Heterotermes

,along with

Coptotermes

, represent the two principle rhinotermitid subterranean pestgenera of the tropical world. In addition to

Heterotermes

, three other pestiferous ter-mite species have been introduced into Florida. These include:

Coptotermes formosa-nus

Shiraki (Fig. 1), the Formosan subterranean termite, which has saturated orappeared in numerous urban and suburban sites throughout the state; and two kalo-termitid species,

Cryptotermes brevis

(Walker), the West-Indian powderpost drywoodtermite, a widely distributed species; and

Incisitermes minor

(Hagen), the westerndrywood termite, which is occasionally encountered in Florida (Scheffrahn & Su1994).

We acknowledge the alert attention of Norm Sage and Burt Silver (InspectionGroup, Pompano Beach) who first collected

Heterotermes

in Miami, Tom Lostetter (Ac-tive Pest Control, North Miami) who collected

Heterotermes

at the second site, andMike Petrozzino and Frank Valdes (Florida State Bureau of Entomology, Miami), whoinspected both sites. We thank Jan Krecek, Phil Busey, and Robin Giblin-Davis fortheir critical reviews. Florida Agricultural Experiment Station Journal Series No. R-04368.

S

UMMARY

Two well-established structural infestations of the subterranean termite genus

Heterotermes

Froggatt were discovered in Miami, Florida, in 1995. This is the firstrecord of an exotic

Heterotermes

sp. in the United States and constitutes the fourth ex-otic termite species living in Florida.

Scientific Notes

627

R

EFERENCES

C

ITED

A

RAUJO

, R. L. 1977. Catálogo dos Isoptera do Novo Mundo. Acad. Brasileira de Ciên-cias, Rio de Janeiro, RJ. 92 pp.

E

MERSON

, A. E. 1971. Tertiary fossil species of the Rhinotermitidae (Isoptera), phy-logeny of genera, and reciprocal phylogeny of associated Flagellata (Protozoa)and the Staphylinidae (Coleoptera). Bull. American Mus. Nat. Hist. 146 (3):243-304.

G

AY

, F. J. 1967. A world review of introduced species of termites. CSIRO Melbourne,Australia, Bull. 286:1-88.

H

ILL

, G. F. 1942. Termites (Isoptera) of the Australian Region. CSIRO Melbourne,Australia. 479 Pp.

M

ATHEWS

, A. G. A. 1977. Studies on termites from the Mato Grosso State, Brazil. 267pp. Academia Bras. de Ciencias, Rio de Janeiro.

S

CHEFFRAHN

, R. H.,

AND

N.-Y. S

U

. 1994. Keys to soldier and winged adult termites(Isoptera) of Florida. Florida Entomol. 77: 460-474.

S

CHEFFRAHN

, R. H., J. P. E. C. D

ARLINGTON

, M. S. C

OLLINS

, J. K

RECEK

,

AND

N.-Y. S

U

.1994. Termites (Isoptera: Kalotermitidae, Rhinotermitidae, Termitidae) of theWest Indies. Sociobiology 24: 213-238.

S

NYDER

, T. E. 1924. Descriptions of new species and hitherto unknown castes of ter-mites from America and Hawaii. Proc. U.S. Natl. Mus. 64: 1-40.

S

NYDER

, T. E. 1954. Order Isoptera. The termites of the United States and Canada.

♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦♦

Natl. Pest Control Assn., New York. 64 Pp.

Scientific Notes

627

A MODIFIED CARROT WEEVIL (COLEOPTERA: CURCULIONIDAE) MONITORING TRAP

G

ERALD

M. G

HIDIU

AND

R

ICHARD

W. V

AN

V

RANKEN

1

Rutgers Research Center, 121 Northville Road, Bridgeton, NJ 08302

1

Atlantic County Extension Office, 1200 W. Harding Highway,Mays Landing, NJ 08330-1533

The carrot weevil,

Listronotus oregonensis

(LeConte), is an important pest of car-rots, parsley and celery in the northeastern United States (Simonet & Davenport1981) and can also be a pest of parsnips (Ryser 1975). Adults overwinter in or nearfields where carrots or celery were grown the previous year, emerging in late April toearly May. They feed directly on the roots, and females oviposit from the beginning ofMay until late June in carrot and parsley roots. Larvae tunnel extensively throughoutthe upper third of the roots. Carrot weevils may damage up to 40% of the crop in un-treated fields (Boivin 1985). Pepper (1942) reported two full broods with a partialthird in northern New Jersey, and three full broods with a partial fourth in southernNew Jersey.

Until recently, growers generally used in-furrow granular insecticides or multiplesoil-directed sprays of insecticides, such as azinphosmethyl, for control of carrot wee-vils. These materials killed the adults and larvae before they tunnelled into the roots.However, azinphosmethyl and parathion registrations on carrots were discontinued,and the management of carrot weevils is now obtained by repeated foliar applicationsof the pyrethroid esfenvalerate directed at the overwintered adults before they ovi-posit. However, the pyrethroids have a short residual period when exposed to the en-

628



vironment, and an accurate population monitoring system is necessary to determineadult activity. In New Jersey, it is recommended that growers begin insecticide sprayswhen adult activity begins (Anonymous 1995). A monitoring system for the weevils,then, must provide reliable and timely captures of adults.

The traps currently used to monitor the adult carrot weevil activity include Ma-son

R

jars fitted with a funnel and baited with carrots or carrot baby food (Ryser 1975),raw carrots placed in the soil to observe oviposition scars (Stevenson 1981), and a trapconsisting of wooden plates with a carrot as bait (Boivin 1985). Of these, the latter wasmore effective as a monitoring device for adult carrot weevils than either the Mason

R

jar type or the carrot in the soil (Boivin 1985). The Boivin trap, however, consisted ofmany small wooden plates, a wooden top and bottom, two long bolts with nuts, andseveral dozen washers. Even after assembly, the trap consisted of three major parts:the body, a top and a bottom plate.

In this note, we describe a modified Boivin trap constructed from a block of wood.The design is inexpensive, easy to construct, durable, and can be made from a singlepiece of pressure-treated post. In field comparisons, this trap was as effective as stan-dard Boivin traps in catching carrot weevil adults in a parsley field in New Jersey.

Trap Construction.

The materials needed to construct the trap are listed below.All measurements are reported in both metric and english units because the lumbersupply companies of the United States sell their materials based on english units:

1 - Pressure-treated pine post, 10.2

×

15.3 cm (4

×

6 in)1 - 5.1 cm diam drill (2 in)1 - Table saw, 25.4 cm diam (10-in saw)Cut the pressure-treated post into 22.9-cm (9 in) long sections. Drill a 5.1-cm diam

hole through the center of each post section (Fig. 1). With the table saw, cut the postsection lengthwise through the center to yield two 10.2

×

7.6 cm (4

×

3 in) pieces (Fig.1). Then cut 0.7 cm (1/4 in) grooves 4 mm apart and 5 cm deep from the face of the postthat was cut down the center (the face with the semicircular cut) for the length of theblock (Fig. 2). Although not necessary for trap function, a bottom plate of 0.7 mm thick

Figure 1. Schematic diagram of holes and cuts necessary to make two modifiedBoivin carrot weevil traps from one piece of pressure-treated post. English units arein ( ).

Scientific Notes

629

plywood can be made for each trap to allow the trap to sit flat in the soil (Fig. 2) andto provide a surface to bang the trap against to shake free the weevils hiding withinthe slats.

Trap Effectiveness.

Traps were compared for trapping effectiveness in a parsleyfield in Buena, NJ from 31 May through 30 June 1994. A total of three Boivin (1985)traps and two modified Boivin traps were randomly placed approximately 3 m apartwithin the edge rows of the parsley field. The edge rows bordered a 1.5-m wide row ofprivet (

Ligustrum ovalifolium

L.), commonly used as a windbreak in vegetable fieldsthroughout NJ. The weevils overwinter in hedgerows, such as privet (Ryser 1975),and migrate into the field from these hedgerows. A fresh, whole carrot was placed ineach trap when set out. The traps were emptied twice weekly by banging the trap ona wood board to shake loose the weevils. Adult carrot weevils were counted, collected,and removed from the field, and the old carrot was replaced with a fresh carrot in eachtrap. Traps in the field were maintained until 30 June 1995.

The standard Boivin trap caught an average of 6.3 weevils per trap, and the mod-ified Boivin trap caught an average of 11.0 weevils per trap (Table 1) during the 4 wktrial.

T

ABLE

1. A

VERAGE

W

EEKLY

T

RAP

C

ATCH

OF

A

DULT

L.

OREGONENSIS

PER

T

RAP

IN

B

OIVIN

AND

S

LOTTED

W

OOD

(M

ODIFIED

B

OIVIN

) T

RAPS

IN

P

ARSLEY

, B

UENA

,NJ 1994.

Trap Type31 May-

7 Jun 8-13 Jun 14-21 Jun 22-28 JunTotal per

Trap

Boivin 0.9 2.5 0.3 2.6 6.3Modified Boivin 1.0 4.5 0.0 5.5 11.0

Figure 2. Completed trap, with a bottom plate.

630



We thank D. Collins for monitoring and identifying the weevils from the traps.This work was funded by the Campbell’s Soup Company, the New Jersey AgriculturalExperiment Station publication No. D-08130-10-95, and by the United States HatchAct.

S

UMMARY

An inexpensive and simple method is described for constructing a modified Boivin(1985) carrot weevil trap. It is constructed from a single piece of pressure-treated post22.9 cm in length. The trap is as effective as the Boivin trap in catching adult carrotweevils.

R

EFERENCES

C

ITED

A

NONYMOUS

. 1994. Commercial vegetable production recommendations for New Jer-sey. Rutgers Coop. Ext. Bull. EO-001J. 144 pp.

B

OIVIN

, G. 1985. Evaluation of monitoring techniques for the carrot weevil,

Listrono-tus oregonensis

(Coleoptera: curculionidae). Canadian Entomol. 117: 927-933.P

EPPER

, B. B. 1942. The carrot weevil,

Listronotus latiusculus

(Bohe.) in New Jerseyand its control. New Jersey Agric. Expt. Sta. Bull. 693. 20 pp.

R

YSER

, B. W. 1975. Investigations regarding the biology and control of the carrot wee-vil,

Listronotus oregonesis

(LeConte) in New Jersey. M.Sc. thesis, RutgersUniv., New Brunswick, NJ.

S

IMONET

, D. E.,

AND

B. L. D

AVENPORT

. 1981. Temperature requirements for develop-ment and oviposition of the carrot weevil. Ann. Entomol. Soc. America. 74: 312-315.

S

TEVENSON

, A. B. 1981. Carrot insects. Min. Agric. Food, Ontario, Fact Sheet 81-007.Agdex 258/605. 4 pp.

Book Review

631

BOOK REVIEW

G

OLDSMITH

, M. R.

AND

A. S. W

ILKINS

. (eds.) Molecular Model Systems in the Lep-idoptera. Cambridge University Press, New York, xii + 542 p. ISBN 0-521-40249-2.Hardback. $125.00.

Yes, molecular genetics research

is

conducted on insects other than

Drosophilamelanogaster

! The stated aim of this book is to provide readers with a review of mo-lecular research in Lepidoptera and to convince readers that Lepidoptera can serve asimportant model systems. The chapters cover topics as diverse as silkworm genetics;transposable elements of Lepidoptera; lepidopteran molecular phylogeny, embryogen-esis, and development; chorion gene regulation and evolution; silk protein gene regu-lation in the silk gland; hormone action on the central nervous system; the moleculargenetics of moth olfaction and the immune response; and, the use of baculoviruses forinsect pest control. This book contains a wonderfully rich body of fundamental infor-mation and provides an entre to an extensive literature. As such, it is a welcome ad-dition to the growing list of books providing information on insect molecular geneticsand molecular biology.

The editors and authors are experts and have produced a well-written and illus-trated volume of value to entomologists looking for molecular arthropod models otherthan the ubiquitous fruit fly,

Drosophila melanogaster

. Ninety-three pages of refer-ences provide access to much of the relevant literature. This book is an excellent re-view of lepidopteran molecular genetics and could serve as supplementary reading incourses on insect molecular genetics. It was not intended, and is not suitable, for anintroductory text on insect molecular genetics. This book reminds us that

D. melano-gaster

is a very specialized insect, and a full understanding of insect genetics and evo-lution requires comparative studies using other species.

The Lepidoptera contain species of great economic importance and esthetic value,as well as providing species sufficiently large to be particularly amenable to physio-logical, behavioral, genetic, and ecological studies. Using

Bombyx mori

,

Ephestia

,

Manduca sexta

,

Antheraea pernyi

, and

Hyalophora cecropia

, fundamental advanceshave been made in insect genetics, endocrinology, and biochemistry. The 16 chaptersprovide: a history of Lepidoptera as model systems (J. H. Willis, A. S. Wilkins and M.R. Goldsmith), an overview of silkworm genetics (M. R. Goldsmith), a review of mobileelements of Lepidoptera (T. H. Eickbush), a review of phylogeny and comparative de-velopment (J. C. Regier, T. Friedlander, R. F. Leclerc, C. Mitter and B. M. Wiegmann),a summary of embryogenesis and experimental embryology (L. M. Nagy), a discussionof homeotic genes in

Bombyx

development (K. Ueno, T. Nagata and Y. Suzuki), anoverview of structure, function, and regulation of chorion genes (F. C. Kafatos, G.Tzertzinis, N. A. Spoerel and H. T. Nguyen), molecular models of chorion gene evolu-tion (T. H. Eickbush and J. A. Izzo), a review of silk protein gene regulation and ho-meobox genes in silk gland development (C. Hui and Y. Suzuki), an analysis of thecontrol of transcription of

B. mori

RNA polymerase III (K. U. Sprague), a review ofhormonal regulation of gene expression during development (L. M. Riddiford), a re-view of the impact of hormones on the central nervous system (J. W. Truman), an over-view of the molecular genetics of moth olfaction (R. G. Vogt), an analysis of themolecular biology of the immune response (A. B. Mulnix and P. E. Dunn), a discussionof engineered baculoviruses as tools for understanding development and physiologyand as potential agents for pest control (K. Iatrou), and an epilogue containing a sum-mary of the unresolved issues and prospects for Lepidoptera as model systems (A. S.Wilkins and M. R. Goldsmith).

632



Wilkins and Goldsmith point out that the Lepidoptera have several nearly uniquefeatures and phenomena that make them novel and intrinsically interesting (e. g.,elaborate wing patterns; silk production with its specialized translational apparatus;and pheromone production and response, with the possibility of integrating behavior,molecular, neurological and evolutionary aspects of moth pheromone utilization).Furthermore, certain lepidopteran species are exceptional models for more generalphenomena, especially hormonal changes associated with metamorphosis and theconstruction of the insect chorion. Hemolymph and cuticular proteins, and endocrinol-ogy can be studied easily in Lepidoptera because the model insects are relatively largeand comparatively slow in their developmental rate, thereby facilitating experimen-tation.

The Lepidoptera are also important in comparative analyses of important devel-opmental processes.

B. mori

has been shown to have an unusual development whichis distinctly different from the classic long germ band mode of development found in

D. melanogaster

. The homeotic genes and segmentation of

B. mori

are organized andexpressed differently, and their chorion genes are regulated differently. Thus, the Lep-idoptera are valuable in comparative studies of insect genome structure and evolu-tion. Novel families of proteins are involved in immune responses in the Lepidoptera,and these may even have relevance to understanding vertebrate immune systems.The editors conclude that the limitations to further progress in molecular biology ofthe Lepidoptera include the lack of conventional genetics and molecular maps, as wellas a reliable and efficient genetic transformation system for genetic manipulation.

This book should stimulate a new generation of molecular entomologists to con-sider the virtues and limitations of lepidopteran species as model systems for analysisof the molecular biology and genetics of insects.

Marjorie A. HoyDepartment of Entomology and NematologyUniversity of Florida, Gainesville 32611

Erratum

633

ERRATUM

L. S. Bauer—

Resistance: A Threat to the Insecticidal Crystal Proteins of

Bacillus thu-ringiensis.

Change first sentence in conclusions (p. 434) to read: The genetic capacity of insect

populations to evolve resistance to

Bt

δ

-endotoxins is now well documented in many

species within

three

different insect orders.

medal et al.: predation of spissistilus festinus 561...

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