Jansson et al.: Novel Formulation for Emamectin Benzoate ...

Jansson et al.: Novel Formulation for Emamectin Benzoate

425

DEVELOPMENT OF A NOVEL SOLUBLE GRANULE FORMULATION OF EMAMECTIN BENZOATE FOR CONTROL

OF LEPIDOPTEROUS PESTS

R

ICHARD

K. J

ANSSON

,

1

R

OBERT

F. P

ETERSON

,

2

P

RADIP

K. M

OOKERJEE

,

2

W. R

OSS

H

ALLIDAY

,

3

J

OSEPH

A. A

RGENTINE

3

AND

R

ICHARD

A. D

YBAS

2

Merck Research Laboratories, P.O. Box 450, Hillsborough RoadThree Bridges, NJ 08887-0450

1

Current Address: Rohm and Hass Co. Research Laboratories, 727 Norristown RoadSpring House, PA 19477

2

Current Address: Lonza, Inc., Lonza Research and Development, 79 Route 22 EastAnnandale, NJ 08801

3

Ricerca, Inc., 7528 Auburn Road, P.O. Box 1000, Painesville, OH 44077

A

BSTRACT

Six solid formulations of emamectin benzoate (one wettable powder (WP) blend,one wettable dispersible granule (WG), and four soluble granules (SG)) were com-pared with an emulsifiable concentrate (EC) formulation for their residual effective-ness at controlling tobacco budworm,

Heliothis virescens

(F.), beet armyworm,

Spodoptera exigua

(Hübner), and cabbage looper,

Trichoplusia ni

(Hübner), in threeglasshouse tests. Emamectin benzoate was applied to plants at two rates in each trial(8.4 and 0.084 g ai/ha). Results from the glasshouse studies showed that most formu-lations were comparable at controlling all lepidopterous pests tested. Four field trialsconducted in Florida confirmed that all formulations were comparable in their effec-tiveness at controlling populations of lepidopterous pests on vegetables, including di-amondback moth,

Plutella xylostella

(L.), on cabbage, southern armyworm,

Spodoptera eridania

(Cramer), on pepper, and

T. ni

and

S. exigua

on celery. Thesestudies identified a novel SG formulation of emamectin benzoate that was comparableto the EC formulation in its effectiveness at controlling lepidopterous pests, but supe-rior to the EC in terms of safety to man and the environment. This novel SG formula-tion is currently being developed for control of lepidopterous pests on a variety ofcrops.

Key Words: Avermectin, emamectin benzoate, formulation, residual efficacy

R

ESUMEN

El efecto residual de seis formulaciones sólidas de benzoato de emamectina (unamezcla de polvo humedecible, gránulos humedecibles dispersables, y cuatro gránulossolubles) fue comparado con el de un concentrado emulsificable en el control de

Helio-this virescens

(F.),

Spodoptera exigua

(Hübner) y

Trichoplusia ni

(Hübner) en trespruebas, en tres invernaderos. El benzoato de emamectina fue aplicado a las plantasa dos concentraciones en cada prueba (8.4 y 0.084 g ia/ha). Los resultados de los estu-dios de invernadero mostraron que la mayoría de las formulaciones fueron compara-bles con en el control de todos los lepidópteros probados. Cuatro pruebas de campoconducidas en la Florida confirmaron que todas las formulaciones fueron comparablesen su efectividad al controlar poblaciones de lepidópteros plagas de vegetales, inclu-yendo

Plutella xylostella

(L.), en col,

Spodoptera eridania

(Cramer) en pimiento, y

T.ni

y

S. exigua

en apio. Los estudios identificaron una nueva fórmula de gránulos solu-

426

Florida Entomologist

80(4) December, 1997

bles de benzoato de emamectina que fue comparable con el concentrado emulsionableen cuanto a su efectividad al controlar lepidópteros plagas pero es superior al concen-trado emusionable en términos de seguridad al hombre y el ambiente. Esta nueva for-mulación de gránulos soluble es actualmente desarrollada para el control de

lepidópteros plagas de varios cultivos.

Avermectins, a family of 16-membered macrocyclic lactones produced by the soil mi-croorganism,

Streptomyces avermitilis

MA-4680 (NRRL 8165), are an important tool inanimal health, human health and crop protection (Jansson & Dybas 1997). The majorcomponent of the fermentation, avermectin B

1

(= abamectin), is a mixture of B

1a

(

≥

80%)and B

1b

(

≤

20%) (Dybas et al. 1989). The discovery, spectrum of activity, safety, and ap-plications of avermectins for control of arthropods have been reviewed extensively(Campbell et al. 1984, Dybas 1989, Lasota & Dybas 1991, Jansson & Dybas 1997).

Emamectin benzoate (MK-0244; PROCLAIM™) is a semisynthetic derivative ofabamectin and is currently being developed for control of lepidopterous pests on a va-riety of vegetable crops worldwide (Dybas et al. 1989, Jansson & Dybas 1997, Janssonet al. 1997). Impressive, broad spectrum control of lepidopterous pests on a variety ofvegetable crops in the field has been demonstrated at low use rates (8.4-16.8 g ai/ha)(Jansson & Lecrone 1992, Leibee et al. 1995, Jansson et al. 1996, 1997, Jansson & Dy-bas 1997).

Earlier attempts to develop solid formulations of avermectin insecticides faileddue to their low water solubility and selection of unsuitable delivery systems. Thiswas especially difficult with abamectin, which is about 3-fold less soluble in waterthan emamectin benzoate (Merck, unpublished data). Recently, Jansson et al. (1996)found that wettable powder (WP) formulations of emamectin benzoate had potentialfor controlling lepidopterous pests on vegetables under glasshouse and field condi-tions. It is well known that changes in the constituents of formulations may havemarked effects on the behavior of arthropods and concomitant product efficacy (Hart-ley & Graham-Bryce 1980, Edwards et al. 1994). Additionally, changes in formulationcomposition can significantly affect the overall safety of pesticide products to man andthe environment (Hudson & Tarwater 1988). The present studies extended our earlierwork (Jansson et al. 1996) to develop a novel solid formulation of emamectin benzoatethat was as effective as a liquid emulsifiable concentrate (EC) formulation at control-ling lepidopterous pests. The soluble granule (SG) formulations reported herein arenovel to the agrichemical industry and represent a significant breakthrough in aver-mectin delivery systems for agriculture.

M

ATERIALS

AND

M

ETHODS

Formulations Tested

Experimental formulations tested were of three types: dry powder blends, wetta-ble dispersible granules, and soluble granules (Table 1); each of these was comparedwith the effectiveness of a 0.16 EC formulation at controlling lepidopterous pests. Thedry powder blend (formulation 81) was prepared by combining all ingredients (ai, di-luent, surfactant) and then blending until homogeneous. The wettable dispersiblegranule (WG) (83) and soluble granule (SG) formulations (85, 86, 87, 88) were pre-pared by combining all ingredients (ai, diluents, surfactants), blending until homoge-neous, and then granulating. The EC formulation (formulation 49) was prepared by


427

combining all ingredients and stirring until all solids had dissolved as described pre-viously (Jansson et al. 1996). The EC formulation (0.16 EC) and the dry powder blendcontained 2.0-2.2% w/w of emamectin benzoate. The WG and SG formulations con-tained 4.8-5.2% w/w of emamectin benzoate.

Chemical availability, or the percentage of ai in solution within one hour after dis-solving in water, was estimated for all formulations tested using methods describedpreviously (Jansson et al. 1996). Estimates for percentages of available emamectinbenzoate in solution that were > 95% could not be measured accurately based on themethods used.

Glasshouse Tests

Methods used in all glasshouse tests were similar to those described previously(Jansson et al. 1996). Three trials were conducted to compare the residual efficacy ofthe six solid formulations of emamectin benzoate with the EC formulation (Table 1).Formulations tested in each trial are given in Table 1. In all three trials, formulationsof emamectin benzoate were applied to plants at two rates: the proposed field use rate(8.4 g ai/ha) and 1% of this rate (0.084 g ai/ha).

Residual efficacy of each formulation was evaluated by challenging neonates ofthree lepidopterous pests, tobacco budworm,

Heliothis virescens

(F.), beet armyworm,

Spodoptera exigua

(Hübner), and cabbage looper,

Trichoplusia ni

(Hübner).

Heliothisvirescens

was tested on two-week old chickpea,

Cicer arietinum

cv. Burpee Garbanzo5024, plants;

T. ni

was tested on two-week old cabbage,

Brassica oleracea

var.

capitata

T

ABLE

1. F

ORMULATION

TYPE

,

COMPOSITION

,

AND

PERCENTAGE

OF

AVAILABLE

AI

OFSEVEN

FORMULATIONS

OF

EMAMECTIN

BENZOATE

(MK-0244)

TESTED

INGLASSHOUSE

AND

FIELD

TRIALS

.

Treatment Formulation type Composition Trials

1

% available

ai

MK-0244-81 2 WP Dry powder blend ai, diluents,surfactants

GH 1,2; F 1-3 47

MK-0244-83 5 WG Wettable granule ai, solvents,carrier,surfactants

GH 1,2; F 1-3 > 95

MK-0244-85 5 SG Soluble granule ai, solublediluents,surfactants

GH 1,2,3; F 1-4 > 95

MK-0244-86 5 SG Soluble granule ai, diluents,surfactants

GH 3; F 4 > 95

MK-0244-87 5 SG Soluble granule ai, diluents,surfactants

GH 3; F 4 > 95

MK-0244-88 5 SG Soluble granule ai, solublediluents,surfactants

GH 3; F 4 > 95

MK-0244-49 0.16 EC Emulsifiable concentrate

ai, solvents,surfactants

GH 1,2,3; F 1-4 > 95

1

GH, Glasshouse; F, Field; numbers correspond to trial number (e.g., GH 1,2,3 = trials 1, 2, and 3 in the glass-house).

428



L. cv. Early Jersey Wakefield, plants; and

S. exigua

was tested on five-week old pepper,

Capsicum annuum

L. cv. Pimento, plants, two-week old sugarbeet,

Beta vulgaris

L. cv.USH-11, plants, or excised leaves of scarlet runner bean,

Phaseolus coccineum

L. Cut-tings from scarlet runner bean were excised when plants were approximately 6-8 daysold, placed in an Aquapic™ containing deionized water, and subsequently sprayedwith the various formulations as described previously (Jansson et al. 1996).

Plants were sprayed with different formulations of emamectin benzoate using atrack-sprayer system that delivered 153.2 liters/ha at 3.4 kg/cm

2

and at 3.5 km/h (Jan-sson et al. 1996). All formulations were applied in combination with a nonionic sur-factant (0.0625%; Leaf Act 80A, PureGro Co., West Sacramento, CA). In all threetrials, 100 plants for each species were treated with two rates of each formulation us-ing a CO

2

track-sprayer system described previously (Jansson et al. 1996). Plantswere air-dried after applications were made and then moved to a glasshouse (trials 1and 2) for the duration of the experiment. In the third trial, plants were moved out-doors after they were air-dried. All plants were bottom watered to minimize wash-offof emamectin benzoate from foliage. Ten plants were randomly selected from eachtreatment on days 0, 4, 7, 10, 14, 17, and 21. One representative leaf was randomly ex-cised from each plant and placed in water agar dishes. Approximately ten neonateswere placed in each dish on each sample date; mortality was recorded after 96 hours.

High control mortality was found in the second trial. For this reason, an additionaltest was conducted using a miniature volume assay similar to that described previ-ously (Jansson et al. 1998). Formulations 81, 83, 85 and the EC (49) were applied attwo concentrations (4 and 20 ng/ml [ppb]) to foliage of scarlet runner bean,

Phaseoluscoccineum

L., ‘Pimento’ pepper, and chickpea using an airbrush applicator and thenchallenged with neonate

S. exigua

(scarlet runner and pepper) and

H. virescens

(chickpea) using methods described previously (Jansson et al. 1998). Mortality of lar-vae was recorded on 0, 3, and 7 days after application (DAA). Approximately 100 ne-onates were tested per treatment combination per evaluation time.

Field Tests

Four field tests were conducted in 1994 and 1995 in Florida. Experimental formu-lations were compared with the EC formulation at the proposed use rate (8.4 g ai/ha).In all except the last field test, formulations were applied at 7- and 14-day intervals.Tests were conducted in Loxahatchee, FL, in two commercial cabbage,

B. oleracea

var

capitata

cv. Monument, fields; in Belle Glade, FL in a commercial celery,

Apium gra-veolens

L. cv. Florida 683 K-strain, field; and in Immokalee, FL, in a commercial bellpepper,

C. annuum

var.

annuum

L. cv. California Wonder, field. Formulations 81, 83,85 and the EC (49) were tested in the first three trials (celery, pepper and one cabbagetrial); formulations 85, 86, 87 and 88 were tested in the last trial on cabbage. All for-mulations were applied in combination with a nonionic surfactant (0.0625%; Leaf Act80A, PureGro Co., West Sacramento, CA).

‘Florida 683 K-strain’ celery was transplanted 0.2 m apart in rows 0.6 m apart ina muck soil in Belle Glade, FL. Treatments were arranged in a randomized completeblock design with four replications. Each plot was two rows by 7.7 m long. Treatmentswere applied on either three (14-day intervals) or six dates (7-day intervals) in No-vember and December, 1994. Applications were made using a CO

2

backpack sprayerequipped with three equally-spaced (0.3 m) hollow disk/cone nozzles (D5-45). Thesprayer delivered 467.3 liter per ha at 2.7 kg/cm

2

. Numbers of

S. exigua

and

T. ni

lar-vae were recorded on five randomly selected plants per replicate on seven dates. Mar-ketability was determined by harvesting the center 3.0 m from each row andrecording the weight, size, and number of marketable celery stalks.


429

Two rows of ‘California Wonder’ bell pepper were transplanted into beds (1.2 mwide between centers) covered with plastic mulch in a light sandy soil in Immokalee,FL. Plants were spaced 0.3 m apart within rows 0.6 m apart. Treatments were ar-ranged in a randomized complete block design with four replications. Each plot wasone bed by 6.2 m long. Treatments were applied on either three (14-day intervals) orsix dates (7-day intervals) between December, 1994 and January, 1995 using a CO

2

backpack sprayer system described previously. Numbers of southern armyworm,

S.eridania

(Cramer), larvae were recorded on six randomly selected plants per replicateon two dates. Percentage marketability was determined by harvesting the center 20plants from each plot, and then dividing the number of marketable fruit by the totalnumber of fruit per plot.

Four rows of ‘Monument’ cabbage were transplanted into 1.2 m beds in a sandy soilin Loxahatchee, FL. Plants were spaced 0.2 m apart within rows 0.3 m apart. Treat-ments were arranged in a randomized complete block design with four replications.Each plot was one bed by 4.7 m long. Treatments were applied on either three (14-dayintervals) or six dates (7-day intervals) between December, 1994 and January, 1995using a CO

2

backpack sprayer system described previously. Numbers of diamondbackmoth,

Plutella xylostella

(L.), larvae were recorded on five randomly selected plantsper replicate on three dates. Damage ratings were recorded on five dates using a scalefrom 1 to 5 modified from Greene et al. (1969) where 1 = no damage and 5 = damagecomparable to the nontreated control. Percentage marketability (damage rating

≤

2)was determined based on the center 20 plants from each plot and evaluating eachplant for unacceptable damage to the head.

In the fourth trial, transplants of ‘Monument’ cabbage were planted into two rowsper bed (0.9 m) in Loxahatchee, FL in March, 1995. Plants were spaced 0.2 m apartin rows 0.3 m apart. Treatments were arranged in a randomized complete block de-sign with four replications. Each plot was two beds wide by 7.7 m long. Treatmentswere applied on four dates (7-day intervals) between April and May using the CO

2

backpack sprayer system described previously. Numbers of

P. xylostella

larvae wererecorded on five randomly selected plants per replicate on five dates. Damage ratingsand percentage marketability were not recorded because ambient temperatures in-creased considerably at the end of the trial thereby reducing head formation.

Data Analysis

Data were analyzed using both nonparametric methods (Conover 1980) and leastsquares analysis of variance techniques (Zar 1984). Chemical availability of emamec-tin benzoate was compared among formulations by chi-square analysis (Conover1980). Percentage mortality was transformed to the arcsine of the square root to nor-malize error variance. Means were separated by the Waller-Duncan

K

-ratio

t

-test(WDKR, Waller & Duncan 1969). Percentage data from field experiments were alsotransformed to the arcsine of the square root; all data from field studies were analyzedusing standard analysis of variance techniques. Means were separated by Duncan’snew multiple range test (

P

= 0.05) (SAS Institute 1990).

R

ESULTS

AND

D

ISCUSSION

Percentage Availability of Emamectin Benzoate

Percentages of ai (emamectin benzoate) that completely dissolved into water afterone hour and were then available for delivery differed (

X

2

= 30.2;

P

< 0.001) among the

430



formulations tested. Most of the variation was attributable to a single formulation(81). The percentage of emamectin benzoate that was available in solution was con-siderably lower for formulation 81 (2WP; 47%) compared with all other formulationstested (> 95%) (Table 1).

Glasshouse Tests

In the first trial, all of the formulations tested were very effective and comparable(

K

-ratio = 100; WDKR) at killing both Lepidopteran targets when applied at the highrate (8.4 g ai/ha) on all dates (Tables 2 and 3). High levels of mortality (96-100%) wereachieved up to 17 DAA for all formulations.

At the low rate (0.084 g ai/ha), differences in mortality of

S. exigua

larvae did notdiffer among formulations on most dates, although mortality achieved with formula-tion 83 was significantly lower than that produced by formulation 81 and 49 on 14 and17 DAA (Table 2). Mortality of

H. virescens

did not differ among most formulations onmost dates, albeit trends in the data suggested that the EC (49) was the least effectiveat controlling

H. virescens

at the low rate (0.084 g ai/ha) (Table 3).In the second trial, the effectiveness of all four formulations at controlling both

Lepidoptera was comparable at both rates applied (Tables 4 and 5). Despite high con-trol mortality on certain dates, no differences in larval mortality were observed, evenon dates when control mortality was acceptable (

≤

20%). In the miniature volume as-say, mortality of

S. exigua

larvae on pepper and

H. virescens

larvae on chickpea didnot differ among formulations on all dates at the high concentration (20 ng/ml) (Table6). On clipped leaves of scarlet runner bean, formulations were comparable in their ef-fectiveness at killing

S. exigua

on days 0 and 3 after application; however, on 7 DAA,formulation 83 was superior to formulation 81. All other formulations were compara-ble in their effectiveness at killing

S. exigua

. Formulations differed markedly whenapplied at the lower concentration (4 ng/ml) (Table 6). On pepper, most formulationsdid not differ on all three dates; formulation 81 was the least effective formulation onpepper. Formulations 83 and 49 were consistently the most effective formulations atcontrolling

H. virescens

on chickpea. None of the formulations was effective at control-ling

S. exigua

on 3 and 7 DAA on scarlet runner bean when applied at 4 ng/ml. On day0, mortality of

S. exigua

on plants treated with formulations 85 and 49 was higherthan on those treated with formulations 81 and 83.

Mortality of

S. exigua

on scarlet runner bean was markedly lower than that ob-served on pepper at both concentrations of each formulation tested. We recognize thatseveral factors (i.e., leaf structure, cuticle thickness, etc.) may account for these dif-ferences; however, excision of scarlet runner leaves may have reduced translaminarmovement of emamectin benzoate into parenchyma tissue thereby affecting the res-ervoir of the toxicant inside foliage over time. Translaminar movement of avermectininsecticides is central to the prolonged residual efficacy observed in a variety of cropsunder glasshouse and field conditions (Jansson & Dybas 1997).

In the third trial, all formulations were comparable at controlling

S. exigua

on sug-arbeet and

H. virescens

on chickpea when applied at the high rate (Tables 7 and 8). Ef-fectiveness at controlling

T. ni

on cabbage differed among formulations, even at thehigh rate (Table 9). The EC formulation was consistently more effective at controlling

T. ni

than formulations 86 and 88 on days 7 to 14 after application. Formulations 85and 87 were comparable to the EC on most dates; formulations 86 and 88 were con-sistently the least effective at controlling

T. ni

.At the low rate, formulation 88 was consistently more effective at controlling

S. ex-igua

than most other experimental formulations, but did not differ from controlachieved with the EC formulation on any evaluation date (Table 7). Formulations 85


431

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432 Florida Entomologist 80(4) December, 1997

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).

Jansson et al.: Novel Formulation for Emamectin Benzoate 433

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4-08

5 5

SG

0.08

423

.0(8

.6)c

d12

.5(4

.4)c

7.8(

4.8)

c3.

3(3.

3)c

11.5

(5.8

)dM

K-0

244-

086

5 S

G0.

084

17.7

(7.9

)d7.

5(4.

8)c

2.2(

2.2)

c4.

0(4.

0)c

12.3

(7.4

)dM

K-0

244-

087

5 S

G0.

084

22.1

(9.2

)cd

5.9(

3.7)

c0.

0(0.

0)c

5.0(

3.3)

c12

.9(5

.0)d

MK

-024

4-08

8 5

SG

0.08

444

.7(1

6.1)

bc2.

3(2.

3)c

9.7(

5.2)

c1.

5(1.

5)c

3.1(

1.9)

dM

K-0

244-

049

0.16

EC

0.08

452

.2(8

.9)b

11.7

(7.3

)c2.

2(2.

2)c

6.7(

6.7)

c4.

4(2.

9)d

MK

-024

4-08

5 5

SG

8.4

100.

0(0.

0)a

100.

0(0.

0)a

100.

0(0.

0)a

88.7

(7.4

)ab

93.5

(4.9

)ab

MK

-024

4-08

6 5

SG

8.4

100.

0(0.

0)a

81.7

(11.

9)b

71.1

(18.

5)b

31.3

(23.

2)c

56.9

(19.

1)c

MK

-024

4-08

7 5

SG

8.4

100.

0(0.

0)a

95.8

(4.2

)ab

96.9

(3.1

)a85

.0(9

.3)a

b80

.5(1

1.1)

bcM

K-0

244-

088

5 S

G8.

410

0.0(

0.0)

a10

0.0(

0.0)

a77

.8(1

1.1)

b76

.5(1

0.8)

b48

.4(2

1.0)

cM

K-0

244-

049

0.16

EC

8.4

100.

0(0.

0)a

100.

0(0.

0)a

100.

0(0.

0)a

100.

0(0.

0)a

100.

0(0.

0)a

Non

trea

ted

chec

k—

3.3(

3.3)

e4.

9(3.

2)c

2.2(

2.2)

c1.

8(1.

8)c

10.0

(4.7

)d

1 Mea

ns

wit

hin

th

e sa

me

colu

mn

fol

low

ed b

y th

e sa

me

lett

er a

re n

ot s

ign

ifica

ntl

y di

ffer

ent

by t

he

Wal

ler-

Du

nca

n K

-rat

io t

-tes

t (K

-rat

io =

100

).


and 87 were consistently the least effective at controlling this insect when applied atthe low rate. All formulations were comparable in their effectiveness at controlling H.virescens at the low rate (Table 8). Effectiveness at controlling T. ni differed amongformulations on day 0 after application (Table 9). The EC formulation was superior toformulations 85, 86, and 87 when applied at the low rate; formulation 88 was compa-rable to the EC on this date. The effectiveness of formulations at controlling T. ni didnot differ on all remaining evaluation dates.

Field Trials

All of the field trials demonstrated that solid formulations of emamectin benzoatewere as effective as the EC formulation at controlling Lepidoptera and reducing dam-age on vegetable crops (Table 10). In the first cabbage trial, mean numbers of P. xylos-tella larvae did not differ (P < 0.05) among formulations applied at either 7- or 14-dayintervals on all dates, albeit only data for the peak population counts (7 days after thefifth application [7DAA5]) are shown (Table 10). No larvae were found per 5 plants inplots treated with all of the formulations of emamectin benzoate, whereas high larvalpressure was observed on nontreated plants (146.5 larvae/5 plants). Similar resultswere found at harvest. Damage ratings did not differ among formulations (data notshown); all formulations resulted in 100% marketability of heads, whereas only 2.5%of heads were marketable in nontreated plots.

Similar results were found in the celery trial on all dates (although all data are notshown). All formulations were comparable at controlling lepidopterous pests and re-sulted in between 98 and 100% marketability of the crop (Table 10). On pepper, meannumbers of S. eridania larvae did not differ among formulations on all evaluationdates, albeit only two evaluation dates are shown (Table 10). Percentages of market-able fruit did not differ (P < 0.05) among most formulations; however, plants that weretreated with formulation 81 at 7-day intervals and with formulation 83 at 14-day in-tervals produced lower percentages of marketable fruit (86.3%) than those treatedwith the EC formulation (49) at 7-day intervals (98.8%) (Table 10). All other formula-tions produced similar percentages of marketable fruit (88.8-95.0%).

The lower (although not consistently significant) efficacy of formulation 81 at con-trolling lepidopterous pests (as noted on pepper) concurs with an earlier report (Jan-sson et al. 1996), and is presumably due to the lower percentage availability of theactive ingredient in solution. This formulation, however, was included in the presenttests because it served as a lead solid formulation with a novel composition. Formu-lation 85 was subsequently designed from formulation 81, and as the data show, wasas effective as the EC formulation in all of the tests conducted. The improved effec-tiveness of formulation 85, compared with formulation 81, was probably due, in part,to its higher percentage of available ai in solution.

The fourth field trial was conducted to determine the effects of slight differences inthe composition of 5 SG formulations on field performance. All four of the formula-tions were comparable to the EC formulation at controlling Lepidoptera on cabbage inthe field (Table 11).

As found in an earlier study (Jansson et al. 1996), excellent efficacy of all formula-tions of emamectin benzoate was found for up to 14-17 days after application when ap-plied at a rate as low as 0.084 g ai/ha under glasshouse conditions. Similar resultswould not be expected in the field because avermectins are very susceptible to photo-degradation. MacConnell et al. (1989) showed that the half-life of abamectin was < 10h in light; the half-life for foliar dislodgeable residues of emamectin benzoate on celerywas approximately 15 h (Merck, unpublished data).


TA

BL

E 1

0.M

EA

N (

± S

EM

) N

UM

BE

RS O

F L

AR

VA

E P

ER

SA

MP

LE

UN

IT A

ND

PE

RC

EN

TA

GE

MA

RK

ET

AB

ILIT

Y O

N T

HR

EE

VE

GE

TA

TIV

E C

RO

PS T

RE

AT

ED

WIT

H D

IFF

ER

EN

T F

OR

MU

LA

TIO

NS O

F E

MA

ME

CT

IN B

EN

ZO

AT

E (

MK

-024

4).

Tre

atm

ent

Rat

e,g

ai/h

a

Spr

ay

inte

rval

, da

ys

Cab

bage

1P

eppe

r1C

eler

y1

Mea

n n

o. D

BM

2 /5 p

lan

tsM

ean

no.

SA

W3 /p

lan

tM

ean

no.

BA

W4 /p

lan

t

7 D

AA

5 5%

mar

k67

DA

A5 3

7 D

AA

5 8%

mar

k67

DA

A5 2

7 D

AA

5 6%

mar

k6

MK

-024

4-08

1 2

WP

8.4

70.

0b10

0.0a

0.0b

0.0b

86.3

b0.

0b0.

0b98

.0a

MK

-024

4-08

1 2

WP

8.4

140.

0b10

0.0a

0.3b

0.0b

91.3

ab0.

5b0.

0b99

.0a

MK

-024

4-08

3 5

WG

8.4

70.

0b10

0.0a

0.0b

0.0b

95.0

ab0.

0b0.

0b99

.5a

MK

-024

4-08

3 5

WG

8.4

140.

0b10

0.0a

0.0b

0.0b

86.3

b0.

0b0.

0b99

.0a

MK

-024

4-08

5 5

SG

8.4

70.

0b10

0.0a

0.0b

0.0b

93.8

ab0.

0b0.

0b99

.0a

MK

-024

4-08

5 5

SG

8.4

140.

0b10

0.0a

0.3b

0.0b

88.8

ab0.

3b0.

0b99

.5a

MK

-024

4-04

9 0.

16 E

C8.

47

0.0b

100.

0a0.

0b0.

0b98

.8a

0.0b

0.0b

98.5

aM

K-0

244-

049

0.16

EC

8.4

140.

0b10

0.0a

0.0b

0.0b

93.8

ab0.

0b0.

0b10

0.0a

Non

trea

ted

chec

k—

—14

6.5a

2.5b

4.5a

3.0a

58.8

c2.

3a3.

0a18

.5b

1 Mea

ns

wit

hin

th

e sa

me

colu

mn

fol

low

ed b

y th

e sa

me

lett

er a

re n

ot s

ign

ifica

ntl

y di

ffer

ent

by D

un

can

’s m

ult

iple

ran

ge t

est

(P =

0.0

5).

2 DB

M, d

iam

ondb

ack

mot

h.

3 SA

W, s

outh

ern

arm

ywor

m.

4 BA

W, b

eet

arm

ywor

m.

5 Sam

ple

date

, day

s af

ter

appl

icat

ion

(D

AA

); e.

g., 7

DA

A 5

= s

even

day

s af

ter

the

fift

h a

ppli

cati

on.

6 Per

cen

tage

mar

keta

bili

ty.


The composition of pesticide formulations can affect their acute toxicity and safetyto mammals (Hudson & Tarwater 1988). The acute oral toxicity of technical grade em-amectin benzoate is about 70 mg/kg (rat) in an ingestion assay (Anomymous 1995).The acute oral LD50 of the 0.16 EC and 5 SG formulations are 2,646 and 1,516 mg/kgbody weight (rat), respectively (Anonymous 1995, Merck, unpublished data). The 5SG formulation is more toxic than the EC formulation because it is 2.5-fold more con-centrated. However, other safety features (ocular and skin irritation in rabbit) aregreatly improved with the 5 SG formulation compared with the 0.16 EC formulation(Anonymous 1995). These improvements in safety have reduced the potential risks ofexposure during mixing and loading of the product into spray equipment and have im-proved its FIFRA classification from category 1 (DANGER) to category 3 (CAUTION).In addition to lowering risks of exposure, the 5 SG has additional attributes, includingelimination of volatile organic solvents as a part of the composition of the formulation;its compatibility with water-soluble packaging to further reduce risks of exposure;and potentially reducing the need for plastic packaging thereby reducing the environ-mental burden.

These studies concurred with an earlier study that demonstrated that solid formu-lations of the benzoate salt of emamectin were effective at controlling lepidopterouspests on vegetable crops in the glasshouse and in the field (Jansson et al. 1996). Moreimportantly, they helped to identify a 5 SG formulation with a delivery system that isnovel for both avermectin chemistry as well as for the agrichemical industry (Merck,unpublished). The 5 SG formulation has been developed along with the 0.16 EC for-mulation for control of lepidopterous pests on a variety of vegetable crops and willsoon be available commercially. Because of its compatibility with integrated pestmanagement programs (Jansson & Dybas 1997), the new formulation of emamectinbenzoate should be an important tool for control of lepidopterous pests in the future.

ACKNOWLEDGMENTS

We thank G. Misich, L. Limpel, M. Poling (Ricerca, Inc., Painesville, OH), M. Alva-rez (Merck & Co., Inc., Three Bridges, NJ), and D. Remick (Entocon, Inc.) for technical

TABLE 11. MEAN (±SEM) NUMBERS OF P. XYLOSTELLA LARVAE PER FIVE PLANTS ONCABBAGE TREATED WITH DIFFERENT FORMULATIONS OF EMAMECTIN BEN-ZOATE (MK-0244).

Formulation treatmentRate,

g ai/ha

Spray interval,

days

Mean no. DBM1/5 plants2

7 DAA31 7 DAA32 7 DAA33 7 DAA34

MK-0244-085 5 SG 8.4 7 2.0b 2.3b 4.5b 1.3bMK-0244-086 5 SG 8.4 7 13.0b 2.8b 0.8b 1.0bMK-0244-087 5 SG 8.4 7 5.0b 1.8b 3.0b 1.0bMK-0244-088 5 SG 8.4 7 4.0b 1.5b 2.3b 1.0bMK-0244-049 0.16 EC 8.4 7 2.5b 1.3b 0.3b 0.0bNontreated check — — 31.0a 23.0a 16.8a 32.0a

1DBM, diamondback moth.2Means within the same column followed by the same letter are not significantly different by Fisher’s pro-

tected LSD (P < 0.05) (Zar 1984).3As in Table 10.


assistance. We thank L. D. Payne, C. L. Lanning, D. L. Cox, D. Rugg, and S. Branchickfor critically reviewing the manuscript. This is Merck Research Laboratories Publica-tion No. 97-MS-0118.

REFERENCES CITED

ANONYMOUS. 1995. Technical data sheet, emamectin benzoate insecticide. Merck Re-search Laboratories, Merck & Co., Inc., Three Bridges, NJ. 11 p.

CAMPBELL, W. C., R. W. BURG, M. H. FISHER, AND R. A. DYBAS. 1984. The discoveryof ivermectin and other avermectins, pp. 5-20. in P. S. Magee, G. K. Kohn & J.J. Menn [eds.]. Pesticide synthesis through rational approaches. ACS Symp.Ser. No. 255. American Chemical Soc., Washington, DC.

CONOVER, W. J. 1980. Practical nonparametric statistics, 2nd ed. J. Wiley, New York.DYBAS, R. A. 1989. Abamectin use in crop protection, pp. 287-310. in W. C. Campbell

[ed.]. Ivermectin and abamectin. Springer-Verlag, New York.DYBAS, R. A., N. J. HILTON, J. R. BABU, F. A. PREISER, AND G. J. DOLCE. 1989. Novel

second-generation avermectin insecticides and miticides for crop protection,pp. 203-212. in A. L. Demain, G. A. Somkuti, J. C. Hunter-Cevera & H. W. Ross-moore [eds.]. Novel microbial products for medicine and agriculture. Elsevier,Amsterdam, Netherlands.

EDWARDS, M. H., S. A. KOLMES, AND T. J. DENNEHY. 1994. Can pesticide formulationssignificantly influence pest behavior?: the case of Tetranychus urticae and dico-fol. Entomol. Exp. Appl. 72: 245-253.

GREENE, G. L., W. G. GENUNG, R. B. WORKMAN, AND E. G. KELSHEIMER. 1969. Cab-bage looper control in Florida - a cooperative program. J. Econ. Entomol. 62:798-800.

HARTLEY, G. S., AND I. J. GRAHAM-BRYCE. 1980. Physical principles of pesticide be-haviour: the dynamics of applied pesticides in the local environment in relationto biological response. Vol. 1 and 2. Academic Press, London.

HUDSON, J. L., AND O. R. TARWATER. 1988. Reduction of pesticide toxicity by choicesof formulation., p. 124-130. in B. Cross & H. Scher [eds.]. Pesticide formula-tions. ACS Symp. Ser. No. 371, American Chemical Soc., Washington, DC.

JANSSON, R. K., AND R. A. DYBAS. 1997. Avermectins: biochemical mode of action, bi-ological activity, and agricultural importance. in I. Ishaaya [ed.], Insecticideswith novel modes of action: mechanism and application. Springer-Verlag, NewYork, (in press).

JANSSON, R. K., AND S. H. LECRONE. 1992. Efficacy of nonconventional insecticides forcontrol of diamondback moth, Plutella xylostella (L.), in 1991. Proc. FloridaState Hort. Soc. 104: 279-284.

JANSSON, R. K., W. R. HALLIDAY, AND J. A. ARGENTINE. 1998. Evaluation of miniatureand high volume bioassays for screening insecticides. J. Econ. Entomol. (inpress).

JANSSON, R. K., R. F. PETERSON, W. R. HALLIDAY, P. K. MOOKERJEE, AND R. A. DYBAS.1996. Efficacy of solid formulations of emamectin benzoate at controlling lepi-dopterous pests. Florida Entomol. 79: 434-449.

JANSSON, R. K., R. BROWN, B. CARTWRIGHT, D. COX, D. M. DUNBAR, R. A. DYBAS, C.ECKEL, J. A. LASOTA, P. K. MOOKERJEE, J. A. NORTON, R. F. PETERSON, V. R.STARNER, AND S. WHITE. 1997. Emamectin benzoate: a novel avermectin deriv-ative for control of lepidopterous pests. in A. Sivapragasam [ed.], Proceedingsof the 3rd International Workshop on Management of Diamondback Moth andOther Crucifer Pests. MARDI, Kuala Lumpur, Malaysia.

LASOTA, J. A., AND R. A. DYBAS. 1991. Avermectins, a novel class of compounds: im-plications for use in arthropod pest control. Annu. Rev. Entomol. 36: 91-117.

LEIBEE, G. L., R. K. JANSSON, G. NUESSLY, AND J. L. TAYLOR. 1995. Efficacy of ema-mectin benzoate and Bacillus thuringiensis at controlling diamondback moth(Lepidoptera: Plutellidae) populations on cabbage in Florida. Florida Entomol.78: 82-96.


MACCONNELL, J. G., R. J. DEMCHAK, F. A. PREISER, AND R. A. DYBAS. 1989. Relativestability, toxicity, and penetrability of abamectin and its 8,9-oxide. J. Agric.Food Chem. 37: 1498-1501.

SAS INSTITUTE. 1990. User’s guide: statistics. Ver. 6. 4th ed. SAS Institute Inc., Cary,NC.

WALLER, R. A., AND D. B. DUNCAN. 1969. A Bayes rule for the symmetric multiplecomparisons problem. J. Amer. Statist. Assn. 64: 1484-1503.

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

ZAR, J. H. 1984. Biostatistical analysis. Prentice-Hall, Englewood Cliffs, NJ.

Doud et al.: Immatures of

Pygospina spinata 443

DESCRIPTIONS OF NYMPHS OF THE CAT-TAIL FEEDING

DELPHACID PLANTHOPPER

PYGOSPINA SPINATA

(HOMOPTERA: FULGOROIDEA)

C

ARL

W. D

OUD

1

, S

TEPHEN

W. W

ILSON

1

,

AND

J

AMES

H. T

SAI

2

1

Department of Biology, Central Missouri State UniversityWarrensburg, Missouri 64093

2

Fort Lauderdale Research and Education Center, University of Florida, IFASFort Lauderdale, Florida 33314

A

BSTRACT

Adult male and female genitalia and the first through fifth instar nymphs of thedelphacid planthopper

Pygospina spinata

Caldwell, collected from southern cattail(

Typha domingensis

(Pers.) Steudel) in south Florida are described and illustratedand a key to instars is provided. Nymphal instars are distinguished by differences inbody size and proportions, spination of the metatibiae, metatibial spurs, and metatar-someres, and by the number of metatarsomeres.

Key Words: Insecta, Homoptera, Delphacidae,

Pygospina spinata

, immature stages,

Typha

R

ESUMEN

Se hacen descripciones del primer y quinto instar ninfal y del aparto reproductorde hembras y machos del salta plantas

Pygospina spinata

Caldwell, colectado de laenea del sur (

Typha domingensis

(Pers.) Steudel) en el sur de Florida. Se publicanilustraciones y una clave para identificación de la especie. Los instares ninfales se dis-tinguen por ciertas diferencias en el tamaño y proporciones del cuerpo, en las espinasde la metatibia, las espuelas de la metatibia y metatarsomeros y por el número de me-

tatarsomeros.

The Neotropical delphacid genus

Pygospina

includes five species,

P. aurantii

(Crawford),

P. reducta

Caldwell,

P. rezendensis

(Muir),

P. spinata

Caldwell, and

P.

444



spinigera

(Fennah) (Caldwell & Martorell 1951). No information on biology or imma-tures of any of these species is available. While collecting in southern Florida, we(SWW & JHT) found adults and nymphs of

P. spinata

at the bases of leaves in the in-ner whorls of southern cattail (

Typha domingensis

(Pers.) Steudel; Typhaceae).

Py-gospina spinata

was described from two specimens from Puerto Rico (Caldwell &Martorell 1951); one specimen has been collected in a Florida light trap (Frost 1964)and two specimens were found from Cocos Island (unpublished data). The apparentrarity of this species is probably due to its feeding habit. We were only able to collectspecimens by stripping the leaves from about ten cattails where 104 orange nymphsand four adults were found.

Pygospina spinata

is the only New World delphacid recorded from cattails; fourother delphacid species have been recorded from cattails in Europe and Asia.

Changeondelphax velitchkovski

(Melichar) has been recorded from

T. laxmannii

Lep-echin in South Korea (Kwon 1982);

Chloriona tateyamana

Matsumura has been foundon

Phragmites australis

(Cav.) Trin. (Poaceae) in Asia (Yang 1989) and

T. laxmannii

in eastern Russia

(Vilbaste 1968);

Kakuna sapporonis

(Matsumura) has been re-corded from

T. laxmanni

in eastern Russia (Vilbaste 1968), and

Matutinus putoni

(A.Costa) feeds on

T. latifolia

L. and

T. angustifolia

L. in Europe (D’Urso & Guglielmino1986).

M

ATERIALS

AND

M

ETHODS

Specimens used for description have the following collecting data: Florida: Bro-ward Co., I75 12 miles north of I595, 31-V-1994, ex.

Typha domingensis

, coll. S. Wilsonand J. Tsai (2 males, 2 females, 27 first instars, 17 second instars, 15 third instars, 23fourth instars, 22 fifth instars). Specimens are housed in S. W. Wilson’s planthoppercollection at Central Missouri State University, Warrensburg.

The fifth instar is described in detail but only major differences are described forfourth through first instars. Arrangement and number of pits is provided for the fifthand fourth instars; this information is not given for earlier instars because the pitsare extremely difficult to discern (those that could be observed relatively easily are il-lustrated). Measurements are given in mm as mean

±

SD. Length was measured fromapex of vertex to apex of abdomen, width across the widest part of the body, and tho-racic length along the midline from the anterior margin of the pronotum to the poste-rior margin of the metanotum.

D

ESCRIPTIONS

Adult.

A lateral view of an adult and a somewhat diagrammatic illustration

of themale genitalia were provided by Caldwell & Martorell (1951).

Male genitalia

(Fig. 1A, B, C). Pygofer, in lateral view, triangular,

with an acutelateral process on laterocaudal aspect on either side, and an elongate blunt process onventrocaudal aspect;

diaphragm below aedeagus v-shaped, unarmed. Anal tube, inlateral view, with a single spinose process originating on the ventrocaudal aspect ofthe tube. Styles, in caudal view, broadest across basal third, narrowing distally to abulbous apex. Aedeagus subcylindrical, with an acute dorsocaudally directed processin basal third, and a postapical flange extending laterally on right (Fig. 1B).

Female genitalia

(Fig. 2A, B, C). The terminology used in describing the femalegenitalia follows Asche (1985) and Heady & Wilson (1990). Tergite nine oriented an-teroventrally (see Asche 1985), elongate, longitudinally concave in ventral midline.Anal tube subcylindrical. Genital scale very large, subovate. Valvifers of segment



eight each covering approximately one-fourth of tergite nine anterolaterally; slender,broadly concave on median margin. Lateral gonapophyses of segment nine elongate,spatulate posteriorly. In lateral view, median gonapophyses of segment nine saber-shaped, with approximately 25 prominent small teeth on dorsal margin in distal one-half. Gonapophyses of segment eight adhering tightly to median gonopophyses of seg-ment nine; slender, acute apically.

Fifth Instar

(Figs. 3A, B). Length 2.4

±

0.2 mm; thoracic length 0.9

±

0.06 mm; tho-racic width 1.04

±

0.08 mm; N = 13.

Body straw colored with white middorsal line ex-tending from vertex almost to end of abdomen. Form elongate, subcylindrical slightlyflattened dorsoventrally. Vertex subtriangular; narrowing anteriorly with two pairs oflongitudinal carinae which extend onto frons. Frons border with clypeus slightly con-cave; lateral margin strongly convex and carinate (outer carinae) and paralleled bysecond pair of carinae (inner carinae) continuous with lateral margins of vertex; areabetween inner and outer carinae with nine pits on each side (six visible in ventralview, three in dorsal aspect); four pits between each outer carina and eye. Clypeusnarrowing distally, consisting of subconical basal postclypeus and cylindrical distalanteclypeus. Beak three-segmented, cylindrical, segment one hidden by anteclypeus,segment two subequal in length to segment three, with black apex. Antennae three-segmented; scape short, cylindrical; pedicel subcylindrical, 2

×

length of scape, with

Fig. 1. P. spinata male genitalia. (A) Pygofer, anal tube, and style, lateral view. (B)Lateral view of aedeagus and ventral view of apex of aedeagus. (C) Pygofer, anal tube,and styles, caudal view. Bar = 0.5 mm.

446



about ten small pits, four pits visible in dorsal aspect; flagellum bulbous basally, withelongate bristle-like extension distally, bulbous base approximately 0.2

×

length of

Fig. 2. P. spinata female genitalia. (A) Ventral view. (B) Lateral view. (C) Lateralview of ovipositor (median gonapophyses of segment 9). Bar = 0.5 mm.



pedicel. Eyes black; in dorsal aspect, median border red. Thoracic nota divided by mid-dorsal line into three pairs of plates. Pronotal plates subtriangular (in dorsal view);anterior margin convex; posterior border sinuate; each plate with a weak posterolat-erally directed carina and seven pits extending anteriorly from near middorsal lineposterolaterally to lateral margin (lateralmost pits often not visible in dorsal view).Mesonotum with median length 1.5

×

that of pronotum; elongate lobate wingpads ex-tending to tips of metanotal wingpads; each plate with very weak posterolaterally di-rected carina originating on anterior margin in median one quarter and terminatingon posterior margin in lateral one third, triangular area between carinae elevated;two pits near middle of plate on either side of carinae and two pits on lateral one halfof plate. Metanotum with median length slightly shorter than that of mesonotum,subtriangular; lobate wingpads extending to third tergite; each plate with one pitnear middle. Pro- and mesocoxae elongated and directed posteromedially; metacoxaefused to sternum. Metatrochanter short and subcylindrical. Metatibia with twospines on lateral aspect of shaft, an apical transverse row of five black-tipped spineson plantar surface and a subtriangular flattened movable spur with one apical toothand 15-19 other teeth on posterior aspect. Pro- and mesotarsi with two tarsomeres,tarsomere one wedge-shaped; tarsomere two subconical, with pair of apical claws andmedian membranous pulvillus. Metatarsi with three tarsomeres; tarsomere one with

Fig. 3. P. spinata fifth instar nymph. (A) Habitus, dorsal view. (B) Frontal view ofhead. Bar = 0.5 mm.

448



apical transverse row of seven black tipped spines; tarsomere two cylindrical, approx-imately 0.3

×

length of tarsomere one, with apical transverse row of four black tippedspines on plantar surface; tarsomere three subconical, slightly longer than tarsomeretwo, with pair of apical claws and median pulvillus. Abdomen nine segmented; flat-tened dorsoventrally; widest across fourth abdominal segment. Tergite one small,subtriangular; tergite two subtriangular approximately 1.3

×

width of first; tergitesthree through eight subrectangular, four with one pit on both lateral margins, fivewith two lateral margin pits on each side, six through eight each with three pits oneach side; segment nine surrounding anus, with three pits on each side; female withone pair of acute processes extending from juncture of sternites eight and nine; maleslacking processes.

Fourth Instar

(Fig. 4D) Length 1.8

±


±


±

0.03 mm;

N

=

15.

Antennal flagellum with basal portion approxi-mately 0.3

×

length of pedicel, about seven small pits. Mesonotal wingpads shorter,each covering approximately two-thirds of metanotal wingpad laterally. Metanotalmedian length 1.5

×

that of mesonotum; wingpad extending to tergite three. Metatibialspur smaller, with one apical tooth and seven to eight marginal teeth. Metatarsi with

Fig. 4. P. spinata first through fourth instar nymphs. (A) First instar. (B) Secondinstar. (C) Third instar. (D) Fourth instar. Bar = 0.5 mm.



two tarsomeres; metatarsomere one with apical transverse row of six black-tippedspines; metatarsomere two with three black-tipped spines in middle of tarsomere.

Third Instar

(Fig. 4C). Length 1.4

±


±


±

0.03 mm; N = 15.

Mesonotal wingpads shorter, each covering one-third of metanotal wingpad laterally. Metanotal wingpads extending to tergite two.Metatibial spur smaller, with one apical tooth and one to three marginal teeth. Meta-tarsomere one with apical transverse row of five black-tipped spines on plantar sur-face.

Second Instar

(Fig. 4B). Length 1.3

±


±


±

.02 mm; N = 14.

Wingpads undeveloped. Metatibia with apical rowof three black-tipped spines; spur small with one apical tooth and no marginal teeth,approximately 3

×

longer than longest metatibial spine. Metatarsomere one with fourapical black-tipped spines.

First Instar

(Fig. 4A). Length 1.07

±


±


±

0.02 mm; N = 15.

Bulbous base of antennal flagellum 0.7

×

length ofpedicel. Metatibia lacking lateral spines on shaft; metatibial spur smaller, approxi-mately 1.5

×

length of longest metatibial spine.

K

EY

TO

THE

N

YMPHAL

I

NSTARS

OF

P

YGOSPINA

S

PINATA

1. Metatibial spur with seven to nineteen marginal teeth (Fig. 5); mesonotal wing-pads extending to half length of metanotal wingpads (Figs. 3A, 4D) . . . . . . . . . . 2Metatibial spur with fewer than seven marginal teeth (Fig. 5); mesonotal wing-pads not extending beyond half length of metanotal wingpads (Figs. 4A, B, C) . 3

2. Metatarsi with three tarsomeres; metatibial spur with more than ten marginalteeth (Figs. 3A, 5) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5th InstarMetatarsi with two tarsomeres; metatibial spur with fewer than eight marginalteeth (Figs. 4D, 5) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4th Instar

Fig. 5. P. spinata apices of metathoracic legs, plantar surface, of first (left) throughfifth (right) instar nymphs. Bar = 0.5 mm.

450



3. Metatarsomere one with apical transverse row of five spines; spur with one tothree marginal teeth (Fig. 5) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3rd InstarMetatarsomere one with apical transverse row of four spines; spur lacking mar-ginal teeth (Fig.

5) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44. Metatibia with three lateral spines on shaft and metatarsomere one with apical

transverse row of four spines; spur more than 3

×

length of longest apical spine(Figs. 4B, 5) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2nd InstarMetatibia without lateral spines on shaft and apical transverse row of threespines; spur about 1.5

×

length of longest apical spine (Figs.

4A, 5) . . . 1st Instar

A

CKNOWLEDGMENT

We thank Dr. David Sutton for identifying the host plant. Florida Agricultural Ex-periment Stations Journal Series #R-05537.

R

EFERENCES

C

ITED

A

SCHE

, M. 1985. Zur Phylogenie der Delphacidae Leach, 1815 (Homoptera CicadinaFulgoromorpha). Marburger Entomol. Publ. 2(1): 1-910.

C

ALDWELL

, J. S.,

AND

L. F. M

ARTORELL

. 1951. Review of the auchenorynchous Ho-moptera of Puerto Rico. Part II. The Fulgoroidea except Kinnaridae. J. Agric.Univ. Puerto Rico 34: 133-269.

D’U

RSO

, V.,

AND

A. G

UGLIELMINO

. 1986. Sviluppo postembrionale di

Matutinus putoni

(Costa, A., 1888) (Homoptera, Delphacidae) e note sulla sua biologia. Animalia13(1/3): 77-93.

F

ROST

, S. W. 1964. Insects taken in light traps at the Archbold Biological Station,Highlands County, Florida. Florida Entomol. 47: 129-161.

H

EADY

, S. E.,

AND

S. W. W

ILSON

. 1990. The planthopper genus Prokelisia (Ho-moptera: Delphacidae): Morphology of female genitalia and copulatory behav-ior. J. Kansas Entomol. Soc. 63: 267-278.

KWON, Y. J. 1982. New and little known planthoppers of the Family Delphacidae (Ho-moptera: Auchenorrhyncha). Korean J. Entomol. 12: 1-11.

VILBASTE, J. 1968. On the Cicadine fauna of the Primosk region. Tallin, 180 pp.YANG, C. T. 1989. Delphacidae of Taiwan (II) (Homoptera: Fulgoroidea). Nat. Sci.

Council (Rep. China) Spec. Publ. 6: 1-334.

Medal et al.: Three-cornered Alfalfa Hopper Predation

451

PREDATION OF

SPISSISTILUS FESTINUS

(HOMOPTERA:MEMBRACIDAE) NYMPHS BY HEMIPTERAN PREDATORS IN THE PRESENCE OF ALTERNATIVE PREY

J. C. M

EDAL

1

, A. J. M

UELLER

1

, T. J. K

RING

1

AND

E. E. G

BUR

, J

R

2

.

1

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

2

University of Arkansas, Agricultural Statistics Laboratory, Fayetteville, AR 72701

A

BSTRACT

The feeding preferences of

Geocoris punctipes

(Say) and

Nabis roseipennis

Reuterwere studied in the laboratory. Female adult predators were exposed for 24h to three

Spissistilus festinus

(Say) nymphal densities and two

Pseudoplusia includens

(Walker) larval densities. Feeding responses of the predators when exposed to secondand third

S. festinus

nymphal stages and second instar

P. includens

and/or

Helicov-erpa zea

(Boddie) as a food choice also were studied. Predation of

S. festinus

nymphsby

G. punctipes

and

N. roseipennis

did not differ significantly in the presence of

P. in-cludens

and/or

H. zea

larvae as alternative prey.

Geocoris punctipes

and

N. roseipen-nis

caused mortality of

S. festinus

nymphs of 33 to 83% and 33 to 100%, respectively,even in the presence of the lepidopterous larvae.

Key Words: Three-cornered alfalfa hopper,

Geocoris punctipes, Nabis roseipennis

, bio-logical control

R

ESUMEN

Las preferencias alimentarias de

Geocoris punctipes

(Say) y

Nabis roseipennis

Reuter fueron estudiadas en el laboratorio. Las hembras predatoras adultas fueronexpuestas durante 24 horas a tres densidades ninfales de


y a dosdensidades larvales de


(Walker). También fueron estudiadaslas respuestas alimentarias de los predatores cuando se expusieron a el segundo y ter-cero estadios ninfales, y a

P. includens

y/o

Helicoverpa zea

, en el segundo estadio lar-val. La predación de ninfas de

S. festinus

por

G. punctipes

y

N. roseipennis

no mostródiferencias significativas cuando estaban presentes larvas de

P. includens

y/o

H. zea

como presas alternativas.

Geocoris punctipes

y

N. roseipennis

causaron mortalidadesde ninfas de

S. festinus

del 33 al 83%, y del 33 al 100%, respectivamente, aun cuando

tenían como alternativa alimentarse de las larvas lepidopteras.

Geocoris punctipes

(Say) (Heteroptera: Lygaeidae) and

Nabis roseipennis

Reuter(Heteroptera: Nabidae) are polyphagous predators commonly found in soybean,

Gly-cine max

(L.), fields (Turnipseed 1974, Irwin and Shepard 1980). They feed on a diver-sity of arthropod pests (Elvin et al. 1983, Crocker and Whitcomb 1980) includingnymphs of the three-cornered alfalfa hopper,


(Say) (Heteroptera:Membracidae) (Spurgeon 1992). The rate of predation on a given prey may be influ-enced by the presence of alternative prey (Ridgway and Jones 1968, Murdoch 1969,Ables et al. 1978). Although generalist predators such as

Geocoris spp

. and

Nabis spp

.attack a variety of prey, they may exhibit a preference for specific prey size or a preywith limited or no defense. Crocker and Whitcomb (1980) found that the largest per-centage (79%) of target prey captured by

Geocoris spp

. were those that remained pas-

452



sive during physical contact with the predator.

Geocoris spp

. hunting behavior onsoybean plants includes both searching actively on all plant parts and remaining mo-tionless waiting for prey (Crocker and Whitcomb 1980).

Geocoris spp

. attack by walk-ing fast or running toward their prey with the beak extended straight forward andquickly inserting the stylet to subdue the prey. This predator has been observed some-times to lift the prey in the air with its beak while feeding.

Nabis roseipennis

is larger and more aggressive than

G. punctipes

. Its huntingstrategy also involves active random movements searching for prey in the soybeancanopy and remaining motionless or ‘waiting’ for relatively long periods of time. Thispredator has been observed using its legs to grasp prey.

Previous laboratory and field studies indicate that

G. punctipes

and

N. roseipennis

feed on

S. festinus

nymphal stages (Medal et al. 1995).

Geocorispunctipes

has a pref-erence for early (1st, 2nd) and intermediate (3rd) nymphal developmental stages,while

N. roseipennis

feeds equally well on all

S. festinus

nymphal stages.Laboratory studies were designed to determine the feeding response or change in

number of prey attacked by

G. punctipes

and

N. roseipennis

female adults as the

S.festinus

nymph density increased, and how the presence of


(Walker) (Lepidoptera: Noctuidae) and

Helicoverpa zea

(Boddie) (Lepidoptera: Noctu-idae) larvae as alternate prey affected predation on

S. festinus

.

M

ATERIALS

AND

M

ETHODS

Feeding Responses at Different Prey Densities

Geocoris punctipes

used in these studies were obtained from a laboratory colony es-tablished from adults collected in southwestern Arkansas soybean, and alfalfa,

Medi-cago

sativa

L. fields during the spring and summer of 1992-3.

Nabis roseipennis

werecollected as immatures and reared in the laboratory to the adult stage on

H. zea

eggsand green bean,

Phaseolus vulgaris

L. pods. The 1-3 week old female adult predatorswere held with only bean pods for 24h before the experiment. Second and third

S. fes-tinus

instars and second

P. includens

instars were obtained from a laboratory colony.


were maintained on

P. vulgaris

pods and

P. includens

on artificialdiet (Burton 1969) at 26

°±

1 C, 70 to 80% RH, and a photoperiod of 14:10 (L:D)h. Thestudies were conducted in a growth chamber under similar environmental conditions.

Predator and prey were caged on individual potted soybean plants (CV: Bragg) ingrowth stages V2-3. The cages were 2-liter clear plastic soda bottles with the tops andbottoms removed. The top was covered with fine cloth to allow air movement. The baseof the cage in contact with the soil was sealed by placing tape around the bottom of thecage and the upper rim of the pot.

Treatments were a predator species (single

G. punctipes

or

N. roseipennis

adult fe-male), three

S

.

festinus

nymphal densities (3, 6, 9), and three

P. includens

larval den-sities (0, 2, 4) which were arranged in a 3

×

3 factorial in a completely randomizeddesign with four replications for each predator. The two predator species with their re-spective prey combinations were run as two separate experiments. Prey mortality wasrecorded after 24h. Percent prey mortality data for each predator species were trans-formed using arcsin

√

y and analyzed separately by an analysis of variance (SAS Insti-tute 1988). Means were separated using a LSD procedure when appropriate.

Feeding Responses with

P. includens

and

H. zea

as Alternative Prey

One early or intermediate

S. festinus

nymphal stage was provided along with sec-ond instar (1-week old)

H. zea

and/or

P. includens

larvae as alternative prey choices.

Medal et al.: Three-cornered Alfalfa Hopper Predation

453

Source of predators and

S. festinus

was as previously described. These alternativeprey were chosen because these lepidopteran larvae are commonly found on soybeanplants when

S. festinus

nymphs are present.The study was conducted in an environmental chamber under conditions previ-

ously described.

Geocoris punctipes

was exposed to second

S. festinus

nymphal stage,and

N. roseipennis

was exposed to third nymphal stage. Treatments included onestarved, 1-3 week old female

G. punctipes

or

N. roseipennis

adult exposed for 24h toeach of the following four prey combinations: 1) one

S. festinus

second or third instar,2) one each

S. festinus

(N2 or N3) +

P. includens,

3) one each

S. festinus

(N2 or N3) +

H. zea

, and 4) one each

S. festinus

(N2 or N3) +

P. includens

+

H. zea

. Prey (all combi-nations) with no predator were included as controls. All treatments were arranged ina completely randomized design with six replications. The two predator species withtheir respective prey combinations were conducted as two separate experiments. Preymortality was recorded after 24h. Percent mortality data were analyzed by a 2-samplebinomial test for equal proportions (Ott 1984).

R

ESULTS

AND

D

ISCUSSION

Feeding Responses at Different Prey Densities


nymphal density (P = 0.09),

P. includens

larval density (P =0.72), and their interaction (P = 0.48) did not significantly affect the percent

S. festi-nus

nymphal mortality due to

G. punctipes.

The data indicate that a near constantpercent prey mortality occurred regardless of the prey density (Table 1). Nonsignifi-cance may be due to the relatively large variability in feeding among the individualpredators.


nymphal density and

P. includens

larval density interactionhad a significant effect (P = 0.02) on percent

S. festinus

mortality when

N. roseipennis

was the predator (Table 2). Analysis of percent

P. includens

mortality due to

N.roseipennis

also indicated a significant interaction (P = 0.04). The percent

S. festinus

T

ABLE

1. M

EAN

PERCENT

MORTALITY

*

OF

S

PISSISTILUS

FESTINUS

NYMPHS

AND

P

SEUDOPLUSIA

INCLUDENS

(P.I.)

LARVAE

WHEN

EXPOSED

SIMULTANEOUSLYTO ADULT FEMALE GEOCORIS PUNCTIPES FOR 24H.

PreyP.I.

Density

S. festinus Density

Mean3 6 9

S. festinus**

0 50.0 50.0 50.0 50.02 75.0 29.2 33.3 45.84 58.3 33.3 25.0 38.9 Mean 61.1 37.5 36.1 44.9

P. includens**2 0.0 12.5 12.5 8.34 25.0 12.5 6.6 14.6 Mean 12.5 12.5 9.4 11.5

*Average of four replications. Analysis of variance was made using arcsin√y transformed data.**Spissistilus festinus density, P. includens density, and their interaction were not significant (P = 0.05, F-

test).


mortality due to N. roseipennis, when the predator did not have P. includens as an al-ternative prey, did not differ significantly at the various S. festinus density levels (Ta-ble 2).

Percent mortality of S. festinus nymphs due to N. roseipennis was not significantlyincreased in the presence of P. includens larvae, but the percent S. festinus mortalitywas significantly decreased with this predator only at the six S. festinus and four P. in-cludens density combinations (Table 2). The number of P. includens larvae killed dueto N. roseipennis at the various S. festinus and P. includens density combinationsranged from 1.5 to 3.0. These values are higher than those obtained with G. punctipeswhich ranged from 0-1.

Nabis roseipennis and G. punctipes did not exhibit a preference for P. includens orS. festinus. Nabis roseipennis fed on approximately the same number of total preywhen they consisted of both S. festinus nymphs and P. includens larvae. Murdoch(1969), and Murdoch and Marks (1973) indicated that generalist predators tend toconcentrate their attack on the most abundant prey species, if it is an acceptable prey.Increased feeding by either predator on either prey species was not exhibited at thehigh prey densities although more frequent encounters between predators and preywould be expected at high prey densities. This suggests that N. roseipennis and G.punctipes do not have a strong preference for either of these prey and that they canfeed on both prey when they are present simultaneously.

These results obtained indicate that S. festinus is a potential prey of adult G. punc-tipes and N. roseipennis, and that predator feeding responses were not generally af-fected by the presence of one-week old P. includens larvae at the prey density levelsevaluated.

Feeding Responses with P. includens and H. zea as Alternative Prey

Mortality in control treatments (prey without predators) was extremely low (<5%), so that correction was not necessary. The percent mortality of S. festinus nymphsdue to adult G. punctipes did not differ significantly (P = 0.05, binomial test) in the

TABLE 2. MEAN PERCENT MORTALITY OF SPISSISTILUS FESTINUS NYMPHS ANDPSEUDOPLUSIA INCLUDENS (P.I.) LARVAE WHEN EXPOSED SIMULTANEOUSLYTO ADULT FEMALE NABIS ROSEIPENNIS FOR 24H.

PreyP.I.

Density

S. festinus Density

Mean3 6 9

S. festinus**

0 33.3 abc 41.7 ab 47.2 ab 40.72 16.7 bc 45.8 ab 25.0 abc 29.24 58.3 a 8.3 c 22.2 abc 29.6Mean 36.1 31.9 31.5 33.2

P. includens**

2 75.0 ab 75.0 ab 100.0 a 83.84 75.0 ab 62.5 bc 37.5 c 58.3 Mean 75.0 68.7 68.7 70.8

*Average of four replications. Analysis of variance was made using arcsin√y transformed data.**Values within prey species followed by the same letter do not differ at the 0.05 probability level using LSD

test.

Medal et al.: Three-cornered Alfalfa Hopper Predation 455

presence of P. includens and/or H. zea larvae as alternative prey (Table 3). Spissistilusfestinus mortality ranged from 33 to 83%.

Comparison of the percent mortality of the two alternative prey species shows thatthe P. includens mortality was significantly higher (P = 0.05, binomial test) than thatof H. zea (Table 3). Geocoris punctipes did not feed on H. zea larvae. A possible expla-nation for this lack of feeding may be related to the defense of H. zea larvae when at-tacked. When disturbed by a predator, H. zea swung its anterior or posterior end ormade quick lateral body movements to repel the predator. Observations made byCrocker and Whitcomb (1980) on hunting behavior of Geocoris spp. under natural con-ditions indicated that when prey are abundant, this predator tends to abandon preythat resist capture.

Spissistilus festinus nymphal mortality by N. roseipennis was not significantly af-fected (P = 0.05, binomial test) by the presence of P. includens and/or H. zea larvae(Table 4). Nabis roseipennis showed a more generalist feeding response than G. punc-tipes, consuming individuals of all three kinds of prey available. Nabis roseipennis

TABLE 3. MEAN PERCENT MORTALITY* OF SPISSISTILUS FESTINUS (S.F.), PSEUDOPLU-SIA INCLUDENS (P.I.), AND HELICOVERPA ZEA (H.Z.) EXPOSED TO GEOCORISPUNCTIPES FOR 24H.

Prey S.F.

Treatment

S.F. + P.I. S.F. + H.Z. S.F. + P.I. + H.Z.

S.F. P.I. S.F. H.Z. S.F. P.I. H.Z.

S. festinus 67a** 33a 67a 83aP. includens 67a 50aH. zea 0b 0b

*Average of six replications.**Values followed by the same letter do not differ at the 0.05 probability level using 2-sample binomial test

for equal proportions.

TABLE 4. MEAN PERCENT MORTALITY* OF SPISSISTILUS FESTINUS (S.F.), PSEUDOPLU-SIA INCLUDENS (P.I.), AND HELICOVERPA ZEA (H.Z.) EXPOSED TO NABISROSEIPENNIS FOR 24H.

Prey S.F.

Treatment

S.F. + P.I. S.F. + H.Z. S.F. + P.I. + H.Z.

S.F. P.I. S.F. H.Z. S.F. P.I. H.Z.

S. festinus 67ab** 50b 100a 33bP. includens 100a 33bH. zea 67ab 83ab

*Average of six replications.**Values followed by the same letter do not differ at the 0.05 probability level using a 2-sample binomial test

for equal proportions.


was able to overcome (9 out of 12 events) the H. zea defensive responses probably be-cause of its larger size and its aggressive use of the front legs to grasp prey.

Geocoris punctipes and N. roseipennis caused mortality of S. festinus nymphs of 33to 83%, and 33 to 100%, respectively, even in the presence of the caterpillars as a foodchoice (Tables 3-4). Results indicate that predators such as G. punctipes and N.roseipennis contribute to the reduction of S. festinus even in the presence of lepi-dopterous larvae. Further biological studies on predator-prey interactions under fieldconditions will provide basic information to develop predictive models on populationdynamics of crop pests and their natural enemies that can be used in pest manage-ment programs.

ACKNOWLEDGMENTS

We thank D. T. Johnson, W. C. Yearian, and S. Y. Young (Department of Entomol-ogy, University of Arkansas) for reviewing the manuscript. This research was sup-ported in part by an Arkansas Soybean Promotion Board grant. Article published withthe approval of the Director, Arkansas Agricultural Experiment Station, University ofArkansas, Fayetteville.

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ELVIN, M. K., J. L. STIMAC, AND W. H. WHITCOMB. 1983. Estimating rates of arthro-pod predation on velvetbean caterpillar larvae in soybeans. Fla. Entomol. 66:319-330.

IRWIN, M. E., AND M. SHEPARD. 1980. Sampling predaceous Hemiptera on soybean.pp. 503-531 in M. Kogan and D. C. Herzog (eds.). Sampling methods in soybeanentomology. Springer-Verlag, New York. 587 pp.

MEDAL, J. C., A. J. MUELLER, T. J. KRING, AND E. E. GBUR, JR. 1995. Developmentalstages of Spissistilus festinus (Homoptera: Membracidae) most susceptible tohemipteran predators. Fla. Entomol. 78: 561-564.

MURDOCH, W. W. 1969. Switching in general predators: experiments on predatorspecificity and stability of prey populations. Ecological Monogr. 39: 335-354.

MURDOCH, W. W., AND J. R. MARKS. 1973. Predation by coccinellid beetles: experi-ments on switching. Ecology 54: 160-167.

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

RIDGWAY, R. L., AND S. L. JONES. 1968. Plant feeding by Geocoris pallens and Nabisamericoferus. Ann. Entomol. Soc. Am. 61: 232-233.

SAS INSTITUTE. 1988. SAS procedures guide, release 6.03 ed. SAS Institute. Cary,N.C.

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

TURNIPSEED, S. G. 1974. Sampling soybean insects by various D-Vac, sweep andground cloth methods. Fla. Entomol. 57: 219-223.

Li & Christiansen: New

Homidia

from China

457

A NEW SPECIES OF

HOMIDIA

FROM CHINA (COLLEMBOLA: ENTOMOBRYIDAE)

L

IU

-R

U

L

I

1

AND

K

ENNETH

A. C

HRISTIANSEN

2

1

Department of Biology, Nanjing University, Nanjing 210093, P.R. China

2

Grinnell College, Grinnell, IA 50112 USA

A

BSTRACT

A new species of Entomobryidae,

Homidia

pentachaeta

, is described from China.It is unique in the presence of 5 lateral macrochaetae on each side of abdominal seg-ment 3.

Key Words: Collembola, Entomobryidae,

Homidia pentachaeta

, new species, China

R

ESUMEN

Una nueva especie de Entomobryidae,

Homidia pentachaeta

, es descrita de China.La especie es única por la presencia de 5 macrochetae en cada lado del tercer seg-

mento abdominal.

Many species of the genus

Homidia

Börner have been described from Japan andKorea but only five species have so far been described from China: the widespread

Ho-midia socia

Denis,

H. nigrocephala

Uchida,

H. sinensis

Denis, n. status,

H. transitoria

Denis, and a species from Tibet currently in press. A sixth species is described here.

Homidia pentachaeta

sp. nov. (Figs. 1- 15).

Maximum body length 3.0 mm. Pattern as in Figs. 1, 4: background color white topale purplish; Ant. III & IV pale purple; eye patches dark blue; interantennal patchdark, small, and nearly triangular; Th. III with a pair of irregular slightly darkerpatches near midline; Abd. III with a wide, slightly darker, band on the central partof dorsum; other segments with unevenly scattered pigment.

Antenna 2.9 - 3.5 times as long as head. Mean ratios of antennal segments 1-4: 1.0/1.2/1.0/1.8. Ant. IV with 2 apical bulbs (Fig. 6). Dorsal chaetotaxy of head (after Szep-tycki, 1973): 4-6 antennal (A), 3 ocellar (O), 6 sutural (S) macrochaetae on frontalarea. Eyes 8+8, G and H much smaller than others and masked by dark pigment (Fig.3). Labrum without papillae, seta a

2

shorter than a

1

, but longer than b

2

(Fig. 7). Setalformula of labial base as

M

,

R

, E, L

1

,

L

2

; setae E & L

1

smooth, others ciliate (Fig. 8).In this paper we follow the groupings of the body macrochaetae developed in the

work on

Sinella

s.s. by Chen & Christiansen (1993). Thorax with macrochaetae onthoracic tergites as in Fig. 2: Th. II with 4 macrochaetae in group I and 5 (6) in groupII. Macrochaetal formula of coxae 3/4+1,3/4+2 (Fig. 9). Trochanteral organ with 28-35smooth setae (Fig. 10). Inner tibiotarsal differentiated setae large, finely ciliate, andclearly different from the normal ciliate setae, only distalmost one on third pair of legsstraight and smooth. Tenent hairs strongly clavate and slightly longer than innermargin of unguis. Unguis with 3 small inner teeth. Outer edge of unguiculus smooth,without tooth (Fig. 11).

458



Abdomen: Dorsal chaetotaxy of Abd. I-III as in Fig. 2. Abd. I with 10 macrochaetaeon each side; Abd. II with 3 macrochaetae in M3 arch, 3 inner to M3 arch, and 1 lateralon each side; Abd. III with 3 dorso-central (Group I) and 5 lateral macrochaetae(Group II) on each side. Anterior part of Abd. IV with 10-13 macrochaetae on eachside; posterior part with 5 + 5 macrochaetae arranged in U-shape, inside which 7-9macrochaetae present (Fig. 5). Except numerous small ciliate setae, ventral tube with3 + 3 ciliate macrochaetae on anterior face, line connecting proximal one (Pr) and ex-ternal-distal one (Ed) oblique to ventral groove (Fig. 12); posterior face with 5 smooth

Figs. 1-8. Homidia pentachaeta n. sp. (type specimens): Fig. 1. habitus; 2. semi- di-agrammatic dorsal chaetotaxy of Thor. II-Abd. III (right side), 3. dorsum of head; 4.body showing color pattern; 5. semi-diagrammatic dorsal chaetotaxy of Abd. IV.; 6. an-tennal apical bulbs; 7. labrum, 8. labial triangle (left side).

Li & Christiansen: New

Homidia

from China

459

subapical setae, median one much shorter than others (Fig. 13); each lateral flap with6 smooth setae (Fig. 14). Ratio of manubrium /(dens + mucro) = 1.0 / 1.2-1.3. Basal halfof dens with 31-45 spines along inner edge in adult; basal setae (bs1 & bs2) subequaland multilaterally ciliate; proximal-internal seta (pi), much thinner and longer thanbs (Fig. 15). Male genital plate not seen.

The name of this new species is derived from the Greek

pente chaite

= five chaetae.It refers to the unique feature of the species—the presence of 5 lateral macrochaetaeon each side of Abd. III (in contrast to the 3-4 setae found in all other species).

Found only at the type locality in the soil among grassroots under a willow woods.Holotype female and 6 female paratypes.

China

: Jiangsu: Nanjing: Baguazhou,IX-17-1994, collection number 8417, coll. by Jian-xiu Chen. Deposited in Departmentof Biology, Nanjing University, China.

Remarks: For convenience, we name the “proximal seta” and “external-distal seta”on the anterior face of ventral tube as “Pr” and “Ed” respectively. In this new species,there are more macrochaetae than in most species of the genus, especially in the dor-sal cephalic groups, group II of Th. II, and dorso-central group on the posterior part

Figs. 9 - 15 Homidia pentachaeta n. sp. (type specimens): Fig. 9. macrochaetae ofcoxae, a. leg I, b. leg II, c. leg III; 10. trochanteral organ; 11. hind foot complex; 12. an-terior face of ventral tube; 13. posterior face of ventral tube (showing apical smooth se-tae); 14. right lateral flap of ventral tube; 15. basal part of dens (bs1 & bs2—basalsetae, pi—proximal-internal seta).

460



of Abd. IV. The unique character of the species lies in the presence of 5 lateral macro-chaetae on each side of Abd. III, whereas all other species have 4 (3) macrochaetae. Itis similar to the Korean species

H. similis

Szeptycki and

H. sinensis

Denis; however,it differs from both as shown below:

In addition

H. penatachaeta

differs from

H. sinsensis

in having 10-13 anterior setaeper side on the 4th abdominal segment as compared with 8 for

H. sinensis

. It also dif-fers in chaetotaxy of the third thoracic and first abdominal segments (compare figures2, 9).

H. sinensis

was originally described as a variation of

H. sauteri

but it differsfrom

H. sauteri

in these last two features and should be considered a valid distinctspecies.

A

CKNOWLEDGMENTS

We thank Mr. Liu Ren-hua of Nanjing University, who made the final drawings forthis paper. We also thank Judith Najt and Jean Marc Thibaud of the Paris Museum,who made the types of

H. sinensis

available to us. Thanks are also given to Dr. PeterBellinger of the Department of Biology, California State University, USA, and Prof.Jian-xiu Chen in the Department of Biology, Nanjing University, China, for their use-ful help to our work.

R

EFERENCES

C

ITED

C

HEN

, J. X.,

AND

K. A. C

HRISTIANSEN

. 1993, The genus

Sinella

with special referenceto

Sinella S.S.

(Collembola: Entomobryidae) of China. Oriental Insects 27: 1-54.

D

ENIS

, J. R. 1929. Notes sur les Collemboles récoltés dans ses voyages par le Prof. F.Silvestri. Seconde Note sur les Collemboles D’Èxtreme Orient. Bull. Lab. Zool.Gen. Agrar. Portici 22: 305-320.

S

ZEPTYCKI

, A. 1973. North Korean Collembola. I. The genus

Homidia

Börner 1906(Entomobryidae). Acta Zool. Cracov.18 (2):23-39.

U

CHIDA

, H. 1943. On Some Collembola-Arthropleona from Nippon. Bull. Tokyo Sci.Mus., Tokyo 8: 1-18.

Character

H. pentachaeta H. similis H. sinensis

Labral papillae absent present absentLabral setae a2 > b2 a2 < b2 a2

≈

b2Labial basal seta L1 smooth ciliate ?Dorsal cephalic chaetotaxy 4-6A, 3O, 6S 3A, 3O, 5S 3A, 3O, 4SCoxal macrochaetae 3/4+1,3/4+2 3/4+1,3/4+3 3/?’/ 4 +2Macrochaetae of Abd III in group I 3 2 3

in group II 5 4 4Position of line connecting Pr & Ed to median furrow of ventral tube

oblique parallel ?

LaSalle & Peña: A New Species of

Galeopsomyia 461

A NEW SPECIES OF

GALEOPSOMYIA

(HYMENOPTERA: EULOPHIDAE: TETRASTICHINAE): A FORTUITOUS

PARASITOID OF THE CITRUS LEAFMINER,

PHYLLOCNISTIS CITRELLA

(LEPIDOPTERA: GRACILLARIIDAE)

J

OHN

L

A

S

ALLE

1

AND

J

ORGE

E. P

EÑA

2

1

International Institute of Entomology, 56 Queen’s Gate, London, SW7 5JR, UK

2

Tropical Research and Education Center, University of FloridaHomestead, Florida, 33031, USA

A

BSTRACT

Galeopsomyia fausta

LaSalle sp.n. (Hymenoptera: Eulophidae: Tetrastichinae) isdescribed as a fortuitous parasitoid of the citrus leafminer,

Phyllocnistis citrella

Stain-ton (Lepidoptera: Gracillariidae: Phyllocnistinae). This species is widely distributed inthe Neotropics, being known from Mexico and Puerto Rico to Argentina.

G. fausta

isthe first species of

Galeopsomyia

which is not associated biologically with galls.

G.fausta

represents an example of an indigenous parasitoid recruited onto an invadingpest species, and the implications of this for the valuation of biodiversity are dis-cussed.

Key Words:


, parasitoids, biological control, biodiversity

R

ESUMEN

Se describe

Galeopsomyia fausta

LaSalle sp.n. (Hymenoptera: Eulophidae: Tetras-tichinae) un parasitoide fortuito del minador de los citricos,


Stainton (Lepidoptera: Gracillariidae: Phyllocnistinae). La especie

G. fausta

esta dis-tribuida ampliamente en el neotrópico, desde México, Puerto Rico hasta Argentina.

G.fausta

es la primera especie de

Galeopsomyia

la cual no se encuentra asociada con in-sectos productores de agallas.

G. fausta

es un ejemplo característico de un parasitoidenativo atacando una especie plaga invasora. Se toma este ejemplo para discutir sus

implicaciones en lo que respecta a el valor de la biodiversidad.

The citrus leafminer (CLM),


Stainton (Lepidoptera: Gracilla-riidae: Phyllocnistinae), has only recently invaded the tropical and semi-tropical ar-eas of the New World. The arrival of

P. citrella

in Florida in 1993, and its rapid spreadthrough the Neotropics, has been documented by Heppner (1993), and Knapp et al.(1995). These papers offer much additional information on the biology, distribution,and management of

P. citrella

.Heppner (1993) recorded about 30 species of Asian parasitoids of

P. citrella

. Thereare now almost 80 species of parasitoids which have been reared from

P. citrella

throughout the world (Schauff et al., submitted). Many of these are indigenous para-sitoids which have moved over onto

P. citrella

as it has spread, and there are alreadyover 20 such species known from the New World (Schauff et al., submitted; Table 1).A few of these species appear to be capable of exerting substantial levels of control onthe

P. citrella

populations. The purpose of this paper is to describe one of these species,

Galeopsomyia fausta

LaSalle sp.n., and comment on the importance these indigenousspecies can play in biological control programs.

462



Galeopsomyia fausta

as a biological control agent of

P. citrella

G. fausta

is a widespread species that has been recorded as a parasitoid of

P. cit-rella

from throughout the Neotropics. We have examined material from Puerto Rico,Mexico, Nicaragua, Honduras, Colombia, Brazil and Argentina, and it will certainlybe present in many other countries in the region.

T

ABLE

1. I

NDIGENOUS

N

EW

W

ORLD

PARASITOIDS

RECORDED

ATTACKING

C

ITRUS

L

EAF-MINER

(

COMPILED

FROM

S

CHAUFF

ET

AL

.,

SUBMITTED

).

Species

EULOPHIDAE

Chrysocharis

sp. Honduras

Chrysocharodes

sp. Colombia, Mexico

Cirrospilus nigrivariegatus

Girault USA: Florida

Cirrospilus

sp. A Honduras, Mexico, Nicaragua, USA: Flor-ida, Venezuela

Cirrospilus

sp. B Honduras, Peru

Cirrospilus

sp. C Argentina, Brazil, Colombia, Honduras, Mexico

Closterocerus cinctipennis

Ashmead USA: Florida, Texas

Closterocerus

sp. or spp. Colombia, Honduras, Mexico

Diglyphus begini

(Ashmead) USA: Florida

Elachertus

sp. or spp. Argentina, Honduras, USA: Florida

Galeopsomyia fausta

LaSalle sp.n. Argentina, Brazil, Colombia, Honduras, Mexico, Nicaragua, Puerto Rico

Horismenus sardus

(Walker) USA: Florida

Horismenus

sp. or spp. Brazil, Colombia, Honduras, Mexico, Nic-aragua, Puerto Rico

Pnigalio minio

(Walker) USA: Florida

Pnigalio

sp. or spp. Mexico, USA: Florida, Texas

Sympiesis

sp. USA: Florida

Zagrammosoma americanum

Girault USA: Florida

Zagrammosoma multilineatum

(Ash-mead)

Colombia, Mexico, USA: Florida

Zagrammosoma

sp. or spp. Mexico, Puerto Rico, USA: Texas, Venezuela

ELASMIDAE

Elasmus tischeriae

Howard Mexico, USA: Florida

Elasmus

sp. or spp. Brazil, Colombia, Mexico, Nicaragua

EUPELMIDAE

Eupelmus

sp. Brazil

PTEROMALIDAE

Catolaccus aeneoviridis

(Girault) USA: Florida


Galeopsomyia 463

Surveys have repeatedly identified

G. fausta

as one of the important indigenousparasitoids of

P. citrella

(Cano 1996, Cano et al. 1996, Castaño et al. 1996, Cave 1996,Cobo 1996, de la Llana 1996, Martinez 1996: all as

Galeopsomyia

sp.).Cano (1996) collected parasitoids in different areas of Nicaragua, and found

G.fausta

to be the most abundant parasitoid, representing 19-59% of the parasitoid spe-cies composition collected from pupae of

P. citrella

in 1995 and 1996. Cano (1996) dem-onstrated that

G. fausta

was abundant in the dry-subtropical region of Nicaraguacomprising 45% of the fauna followed by

Horismenus

sp., (36%),

Cirrospilus

sp. (9%)and

Elasmus

sp. (9%). Similar results were reported by de la Llana (1996).

G. fausta

was observed parasitizing

P. citrella

throughout the year, with highest peaks observedin January, July and October 1995-1996 (Cano 1996). Levels of 28 and 68% parasiti-zation of pupae were observed during June 1995 and January 1996 (Cano 1996).

Biological Considerations of

Galeopsomyia fausta

G. fausta

is the first species of

Galeopsomyia

which is known to attack leafminers.All other species of

Galeopsomyia

attack galls, mostly as parasitoids of Cynipidae orCecidomyiidae, but occasionally as inquilines (LaSalle 1994). The native host of

G.fausta

is not known. The wide distribution of

G. fausta

on

P. citrella

in the short periodof time that

P. citrella

has been in the Neotropics suggests that this species has an in-nate ability to switch hosts onto

P. citrella

, rather than having made a single hostswitch and then spreading.

Galeopsomyia fausta

and Biodiversity Considerations

Various authors have claimed that one of the values of conserved biodiversity isthat it represents a pool of potential biological control agents (Waage 1991, LaSalle &Gauld 1993, LaSalle 1993). Thus, we are retaining the ability to control future pestproblems in a manner that is both environmentally and economically sound. Withoutthis option for biological control, we may have to rely upon control measures whichwill accelerate the present decline in environmental quality.

The spread of

P. citrella

in the New World has provided support for these claims.The only species of introduced parasitoid which has been established in the NewWorld is

Ageniaspis citricola

Logvinovskaya in Florida (Hoy & Nguyen 1994, Knappet al. 1995, Hoy et al. 1995), Louisiana (Johnson et al. 1996), Bahamas (Hoy et al.1995), and Honduras (Castro et al. 1996, Cave 1996). However, a large complex of na-tive parasitoids are now attacking

P. citrella

, and in many cases native species areproviding control which is as effective or more effective than that supplied by

A. citri-cola

(Cano 1996, Cano et al. 1996, Castaño et al. 1996, Cave 1996, Cobo 1996, de laLlana 1996, French & Legaspi 1996, Gravena 1996, Martinez 1996, Peña et al. 1996,Perales & Garza 1996, Perales et al. 1996).

Table 1 lists over 20 indigenous species which have now been recorded from

P. ci-trella

in the New World (Schauff et al., submitted). Many of these species are inciden-tal and will offer no substantial control. However, others of these species appear toplay a major role in regulating the population levels of

P. citrella

(such as species of

Cirrospilus

, and

G. fausta

).Several papers have discussed the relevance of being able to provide direct mea-

sures of the value of preserving biodiversity, and methods of attempting to do it (sev-eral chapters in Wilson 1988, Orians et al. 1990, Swanson 1995, Kunin & Lawton,1996). The recruitment of indigenous parasitoids onto an introduced pest provides adirect method of quantifying one small portion of the value of conserved biodiversity.Evaluation of the cost effectiveness of biological control using introduced parasitoids

464



has been performed on many occasions (e.g. Dean et al. 1979, van den Bosch et al.1982, Norrgard 1988a, b, DeBach & Rosen 1991). This methodology can just as easilybe applied to indigenous parasitoids to quantify one of the financial benefits of biodi-versity.

M

ATERIAL

AND

M

ETHODS

Terminology follows LaSalle (1994). The term basigastral carina is borrowed fromthe ant workers to describe a strong, transverse carina along the anterior margin ofthe first gastral tergite; any longitudinal carinae extending posteriorly from the basi-gastral are termed basigastral costulae.

Galeopsomyia fausta

, LaSalle sp.n.(Figs. 1-9)

Galeopsomyia

sp.: Cano, 1996; Cano et al., 1996; Castaño et al., 1996: Cave, 1996;Cobo, 1996; de la Llana, 1996; Martinez, 1996.

Diagnosis

Body strongly sclerotized. Gaster (Figs. 4, 5) non-collapsing in dried specimens,distinct basigastral carina and basigastral costulae present; petiole (Fig. 4, 6) distinct,wider than long, strongly sculptured dorsally; gastral tergites, and particularly thefirst one generally lightly sculptured, terminal gastral tergites reticulate dorsally.Propodeum (Figs. 3, 4) strongly reticulate, with a paraspiracular carina, and posterioredge sharply margined. Malar space (Fig. 2) with a triangular fovea below eye, thebottom of this fovea with sculpture. Fore wing (Fig. 7) with 4-5 setae on dorsal surfaceof submarginal vein.

Female

Length 1.15-1.7 mm. Head, mesosoma, metasoma and coxae black, usually withdark blue metallic shine which is particularly strong on the mesosoma. Antenna withscape yellow to light brown; pedicel yellow to light brown, with dark dorsal patch; fu-nicle dark brown. All femora predominantly brown to dark brown, generally brown toyellow apically. Tibiae yellow to light brown. Tarsal segments 1-3 yellow to white, seg-ment 4 brown.

Head

(Figs. 1, 2) strongly sculptured. Scrobal cavity without distinct sulci, butwith a longitudinal median ridge. Face with strong furrow between torulus andmouth margin; this furrow carinate ventrally. Clypeus distinctly bilobed. Malar spacewith a triangular fovea below eye, the bottom of this fovea with sculpture.

Antenna

(Fig. 8) with 3 anelli, 3 funicular segments, 3 segmented club. Each suc-cessive funicular segment only very slightly increasing in length; funicular segmentstogether slightly longer than club.

Mesosoma

(Fig. 3) with distinct reticulation. Mesoscutum with notaulus very deep;median line present as a broad, vaguely defined furrow; adnotaular setae in 1-2 rows.Scutellum with submedian lines broad and shallow; sublateral lines broad and later-ally carinate; distinct transverse groove along posterior margin; several (4-6) pairs ofscattered setae, these small and indistinct when examining specimens under normalmagnification. Propodeum strongly reticulate, with a paraspiracular carina, and pos-terior margin sharply margined.


Galeopsomyia 465

Figs. 1-6. Galeopsomyia fausta, /. 1, head, frontal view. 2, head, side view. 3, me-sosoma. 4, propodeum, petiole, base of gaster. 5, gaster. 6, propodeum, petiole, base ofgaster, lateral view.

466



Fore wing

(Fig. 7) without even rudimentary postmarginal vein. Dorsal surface ofsubmarginal vein with 4-5 setae.

Metasoma

(Figs. 5, 6). Petiole distinct, wider than long, strongly sculptured dor-sally. Gaster with distinct basigastral carina and basigastral costulae present; gastraltergites, and particularly the first one generally lightly sculptured, terminal gastraltergites reticulate dorsally. Gastral tergites 1-4 each decreasing slightly in lengthcompared to the previous segment, so that tergite 4 is the shortest gastral tergite;tergite 5 slightly longer than tergite 4, but shorter in length than tergites 1 and 2.

Male

Length 1.15-1.35 mm. Similar to female except in sexual differences in genitaliaand antennae. Antenna (Fig. 9) with 4 funicular segments. Funicular segments with-out basal whorls of long setae, with sparsely scattered setae which are shorter thanthe width of the funicle. F1 shorter than remaining segments, F2-4 subequal inlength. Scape with ventral plaque situated in apical half of scape, 0.25-0.28 the totallength of scape.

Discussion

Galeopsomyia

may be distinguished from other genera of Tetrastichinae using thekey provided by LaSalle (1994). The genus can be recognized by the combination of thefollowing characters: body strongly sclerotized, with gaster non-collapsing and allgastral tergites reticulate dorsally; propodeum strongly reticulate, with a paraspirac-ular carina, and a transverse carina along posterior margin; malar space with a tri-angular fovea below eye, this generally with some sculpture; submarginal vein with2 or more dorsal setae.

G. fausta

can be distinguished from other species of

Galeopsomyia

by the combi-nation of the following characters: distinct basigastral carina and basigastral costulaepresent; petiole distinct, wider than long, strongly sculptured dorsally; gastral terg-ites, and particularly the first one, not as strongly reticulate dorsally as other mem-bers of the genus; fore wing with 4-5 setae on dorsal surface of submarginal vein (asopposed to 2 or 3 in most members of this genus); gastral tergites 1-4 each decreasingslightly in length, tergite 5 slightly longer than tergite 4, but not distinctly longerthan segments 1 and 2.

G. fausta

is the only species of

Galeopsomyia

with a distinct petiole. Other mem-bers of

Galeopsomyia

are also generally lacking a basigastral carina. The only other

Galeopsomyia

species which has a basigastral carina like

G. fausta

is the Brazilian

G.viridicyanea

(Ashmead). This species differs from

G. fausta

in lacking a distinctly vis-ible petiole, having all gastral tergites with very strong reticulate sculpture, and hav-ing gastral tergites 1-5 each increasing slightly in length compared to the previoussegment, so that tergite 5 is distinctly the longest gastral tergite.

Material Examined

Note: all specimens ex.


on citrus.Holotype

/

, MEXICO, Veracruz, Cuitlahuac, 20-xi.1995, N. Bautista Mtz.(BMNH).

67

/

, 6

?

Paratypes: PUERTO RICO: Adjuntas, 6.ii.1996 (2

/

UPRM). MEXICO:Veracruz, Cuitlahuac, 20-xi.1995, N. Bautista Mtz. (3

/

CPMM, 2

/

INIA, 2

/

BMNH);Veracruz, Cruz Naranjos, 9.iii.1995, R. Mateos C. (1

/ CPMM). HONDURAS: Fco

LaSalle & Peña: A New Species of Galeopsomyia 467

Morazan, El Zamorano, 31.x.1995, A. Guillen (3/ BMNH, 2/ CNC); Fco Morazan, ElZamorano, 8.xi.1995, A. Guillen (1/ BMNH, 2/ FSCA); Fco Morazan, San Antonio deOriente, El Zamorano, 17.xi.1994, R. Cordero (4/ EAPZ); Fco Morazan, San Antoniode Oriente, El Zamorano, 12.xii.1994, R. Cordero (1/ USNM); El Paraiso, Yuscarán,15 km antes de Yuscarán, 8.ii.1995, R. Cordero (1/ USNM); Atlantida, La Ceiba,Buena Vista, 3.iii.1995, R. Chavez (1/ USNM); Atlantida, La Ceiba, Buena Vista,22.ix.1995, J. Ortega (1/ USNM); Atlantida, 45 km W Tela, 22.i.1996, A. Guillen (1/

USNM). NICARAGUA: C. Azules, Masatepe, 1.viii.1995, A. de la Llana (2/ SEA); C.Azules, Masatepe, 14.viii.1995, A. de la Llana (1/ CENA); C. Azules, Masatepe,4.ix.1995, A. de la Llana (1/ CENA); Jinotéga, Dorranli, 19.vii.1995, A. de la Llana(1/ SEA); León, León, 26.vii.1995, J. Hernandez (1/ BMNH); León, León,28.vii.1995, J. Hernandez (1/ CENA). COLOMBIA: Valle, Palmira, viii.1995, L. Rojas& F. Garcia (3/ 3? BMNH, 2/ 3? USNM). BRAZIL: São Paulo, Jaguariuna,15.viii.1996, J. L. de Silva (4/ DCBU, 2/ BMNH, 1/ USNM, 1/ CNC); São Paulo,Valinhos, 24.v.1996 (2/ DCBU); São Paulo, Valinhos, vi.1996, Paiva (1/ DCBU). AR-GENTINA: Tucumán, El Cadillal, 12.iii.1997, E. Frías & P. Colombres (9/ IML, 4/

MLP, 2/ BMNH, 2/ CNC).

Figs. 7-9. Galeopsomyia fausta. 7, / forewing. 8, / antenna. 9, ? antenna.


Etymology

The species name fausta comes from the Latin for favorable or fortunate. It signi-fies that this species is a fortuitous biological control agent.

Biology

G. fausta has clearly moved over onto P. citrella from some other host(s), but theidentity of its native host or hosts remains unknown.

Cobo (1996) studied Colombian parasitoids of CLM. She reported that G. fausta (asGaleopsomyia sp.) was an important parasitoid of P. citrella, which attacked the larva,prepupa and pupa. It paralyzes the host, and later deposits its eggs near the host.When several eggs are deposited at the same time, the first eclosing larva feeds on theremaining eggs. Eggs are hymenopteriform, round in one end and sharp at the oppo-site end, and small and almost transparent when newly oviposited. After oviposition,the host stops any movement and becomes darker. The parasitoid larva developsquickly, pupating at a distance from the host. The pupa is initially pale yellow, anddarkens to a shiny black color. G. fausta is mostly a pupal parasitoid, parasitizing87.77% pupae, 9.83% prepupae, 2.39% larvae (Cobo, 1996).

G. fausta appears to be mainly thelytokous, with only occasional males. Of the 74type specimens mentioned in this paper, only 6 were males, and these were all fromthe same locality (Colombia) and date. Since this paper was submitted, another 150specimens were sent to us from Brazil, all of which were female.

ABBREVIATIONS

BMNH The Natural History Museum, London, UKCNC Canadian National Collection, Ottawa, CANADACPMM Coleccion de Insetos, Instituto de Fitosanidad, Colegio de Postgraduados,

Montecillo, MEXICODCBU Departemento de Ciências Biológicas, Universidade Federal de São Carlos,

São Carlos, SP (São Paulo), BRAZILEAPZ Departemento de Proteccion Vegetal, Escuela Agricola Panamericana, El

Zamorano, HONDURASFSCA Florida State Collection of Arthropods, Gainesville, Florida, USAIML Fundación e Instituto Miguel Lillo, Universidad Nacional de Tucumán, San

Miguel de Tucumán, ARGENTINAINIA Instituto Nacional de Investigaciones Agricolas, Secretaria de Agricultura y

Ganaderia, Chapingo, MEXICOCENA Museo de Entomologia, Centro Nacional de Protectión Vegetal, Ministerio

de Agricultura y Ganadería, Managua, NICARAGUAMLP Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata,

La Plata, ARGENTINASEA Servicio Entomológico Autónomo, Museo Entomológico, SEA, León, NICA-

RAGUAUPRM Department of Entomology, University of Puerto Rico, Mayaguez, PUERTO

RICOUSNM United States National Museum (Natural History), Washington, D.C., USA

ACKNOWLEDGMENTS

Many people have kindly made specimens or information available to us. These in-clude N. Bautista Mtz., E. Cano, R. Cave, V. A. Costa, A. de la Llana, G. Evans, P. Fi-dalgo, F. Garcia, J. Hernandez, A. Pantoja, A. Penteado-Dias, M. Schauff, A. Trochez.

LaSalle & Peña: A New Species of Galeopsomyia 469

Space and facilities during this study were kindly provided to JL by the Depart-ment of Entomology, The Natural History Museum, London; technical assistance fromthe SEM and photography units of the BMNH is also gratefully acknowledged; specialthanks to Nick Hayes (BMNH) for the printing of the photomicrographs.

Florida Agricultural Experiment Station Journal Series No. R-05660.

REFERENCES

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CANO, E., A. DE LA LLANA, J. HERNANDEZ, F. RUIZ, J. E. PEÑA, AND G. EVANS. 1996.Dynamics and biological control of the citrus leafminer in Nicaragua. p. 76, inHoy, M. A. (Ed.) Managing the Citrus Leafminer. Proceedings from an Interna-tional Conference, Orlando, Florida, April 23-25 1996. 119 pp. [Abstract].

CASTAÑO, O., R. F. GARCIA, A. TROCHEZ, L. ROJAS, J. E. PEÑA, AND G. EVANS. 1996.Biological control of the citrus leafminer, Phyllocnistis citrella, in Colombia. p.76, in Hoy, M. A. (Ed.) Managing the Citrus Leafminer. Proceedings from an In-ternational Conference, Orlando, Florida, April 23-25 1996. 119 pp. [Abstract].

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FRENCH, J.V., AND J. C. LEGASPI. 1996. Citrus leafminer in Texas: population dynam-ics, damage and control. p. 80, in Hoy, M.A. (Ed.) Managing the Citrus Leaf-miner. Proceedings from an International Conference, Orlando, Florida, April23-25 1996. 119 pp. [Abstract].

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JOHNSON, S. J., A. VAUGHN, AND W. J. BOURGEOIS. 1996. Rearing and release meth-ods for Ageniaspis citricola for a classical biocontrol program of the citrus leaf-miner in Louisiana. p. 63, in Hoy, M. A. (Ed.) Managing the Citrus Leafminer.Proceedings from an International Conference, Orlando, Florida, April 23-251996. 119 pp. [Abstract].


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MARTINEZ BERNAL, C. 1996. Insectos parasitoides del minador de la hoja de los citri-cos, Phyllocnistis citrella Stainton, en tres localidades de la zona centro del es-tado de Tamaulipas, Mexico. Universidad Autonoma de Tamaulipas, Cd.Victoria, Tamaulipas, Mexico. MSc thesis. 47 pp.

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WAAGE, J. K. 1991. Biodiversity as a resource for biological control. pp. 149-162, inHawksworth, D. L. (ed.) The Biodiversity of Microorganisms and Invertebrates:Its Role in Sustainable Agriculture. CAB International, Wallingford, UK.

WILSON, E. O. (ed.). 1988. Biodiversity. National Academy Press. Washington, D.C.521 pp.

Shapiro et al.: Citrus Root Resistance Bioassay

471

RESISTANCE OF CITRUS ROOTSTOCKS AND

GLYCOSMIS PENTAPHYLLA

AGAINST LARVAL

DIAPREPES ABBREVIATUS

(COLEOPTERA: CURCULIONIDAE) IN LIVE ROOT OR DIET-

INCORPORATION ASSAYS

J

EFFREY

P. S

HAPIRO

, K

IM

D. B

OWMAN

AND

H

UNTER

S. S

MITH

USDA, Agricultural Research Service, 2120 Camden Road, Orlando, Fl 32803

A

BSTRACTS

The growth of larval

Diaprepes abbreviatus

L. was measured after rearing them onroots of rutaceous seedlings for 35 or 42 days. Larvae were fed on seedlings of twocommon citrus rootstocks, two new hybrids that are under development as rootstocks,and one citrus relative. Live weights of larvae reared on Carrizo or Swingle rootstocksfor 42 days increased an average of 10.3- and 10.2-fold, respectively; weight increaseson the citrus hybrids HRS-802 and HRS-896 for 35 days averaged 7.6- and 6.1-fold, re-spectively; and weight increase on

Glycosmis pentaphylla

Retzius for 42 days aver-aged 2.5-fold. A bioassay to test for potential phytochemical sources of resistanceagainst the larvae was developed by incorporating finely milled roots into larval diet.Milled root samples were incorporated into a standard semi-defined diet at 5% con-centrations (w/v), and growth of larval weevils was recorded following a 32-day feed-ing period. Roots collected from uninfested control seedlings in the previousexperiment were used. On diet containing no roots, mean larval weight increased16.8-fold, while weights increased 13.9-fold on diet containing roots of Carrizo, 12.0-fold on Swingle, 15.1-fold on HRS-802, 12.3-fold on HRS-896, and only 5.5-fold on

G.pentaphylla

. Both tests indicate that

G. pentaphylla

may represent a source of root re-sistance to

D. abbreviatus

, and the diet-incorporation tests indicate potential phy-tochemical or microbial sources of resistance.

Key Words:


, citrus root weevil, rootstock resistance, larvalgrowth, diet-incorporation assay

R

ESUMEN

Fue medido el crecimiento de larvas de


L. criadas en raícesde plántulas de rutáceas durante 35 o 42 días. Las larvas fueron alimentadas en dospatrones comunes de cítricos, dos nuevos híbridos que están bajo desarrollo como pa-trones, y un pariente de los cítricos. El crecimiento en los patrones Carrizo o Swingledurante 42 días promedió 10.3 y 10.2 veces, respectivamente; el crecimiento sobre loshíbridos HRS-802 y HRS-896 durante 35 días promedió 7.6 y 6.1 veces, respectima-mete, y el crecimiento en

Glycosmis pentaphylla

durante 42 días promedió 2.5 veces.Se desarrolló un bioensayo para probar fuentes potenciales fitoquímicas de resisten-cia contra la larva mediante la incorporación de raíces finamente molidas a la dietalarval. Las muestras de raíces molidas fueron incorporadas a una dieta estándar se-midefinida a concentraciones del 5% (peso/volumen), y el peso de las larvas fue regis-trado siguiendo un período de 32 días. Fueron usasas las raíces colectadas de lasposturas control en el experimento previo. En una dieta sin raíces, el peso medio lar-val aumentó 16.8 veces, mientras que los pesos aumentaron 13.9, 12.0, 12.3 y 5.5 ve-ces sobre la dieta que contenía raíces de Carrizo, Swingle, HRS-802, HRS-896 y

G.pentaphylla

, respectivamente. Ambos ensayos indicaron que

G. pentaphylla

puede seruna fuente de resistencia radicular hacia

D. abbreviatus

, y que los ensayos de incor-poración a las dietas sirven para indicar fuentes fitoquímicas o microbianas de resis-

tencia.

472



Cultivated varieties of crop plants are routinely evaluated for resistance of foliageor fruit to insect feeding and damage (Smith 1989, Panda & Khush 1995). Evaluatinginsect resistance in roots is less common, however, especially for long-lived horticul-tural crops such as citrus. In Florida, the citrus root weevil


L.(Coleoptera: Curculionidae) causes most of its damage to citrus trees during the lar-val stage while feeding on the root system of the rootstock. There, larvae strip barkfrom the roots of the tree, weakening and eventually killing the root once its circum-ference is fully girdled. We recently reported results from a whole-plant test designedto compare root damage, larval survival, and larval growth among citrus rootstockcultivars, hybrids, and other species of citrus relatives (Shapiro & Gottwald 1995).

The phytochemical composition of citrus roots has been well studied (Shapiro1991; Nordby & Nagy 1981, Gray & Waterman 1978). Structural characterizations ofnumerous coumarins, alkaloids, flavonoids, and limonoids from citrus roots have beenreported, but with few references to biological activities. These classes of phytochem-icals include many examples of defensive compounds. To discover whether such com-pounds impart any resistance against

Diaprepes

, roots must first be screened forbiological activity, then the chemical source of an activity must be identified. A suc-cessful bioassay should enable rapid tests of small quantities of root material from alarge number of samples. A whole-plant assay has already been developed (Shapiro &Gottwald 1995). Of eight commercial rootstocks and new hybrids that were tested inthat assay, only one - Swingle - showed some resistance, in contrast to an earlier study(Beavers & Hutchison 1985). This observation was based on three parameters mea-sured in the bioassay: larval weight gain, larval mortality, and root damage relativeto uninfested control plants. The last parameter was measured by root volume, rootweight, and by digitally integrating the visible areas of roots from photographs, all ofwhich correlated well.

To enable the identification of roots that deter larval growth and of the active phy-tochemicals extracted from them, we have designed a simple diet-incorporation assay,and here compare it with our routine whole-plant assay for resistance to

Diaprepes

larvae (Shapiro & Gottwald 1995).

M

ATERIALS

AND

M

ETHODS

Insects

Larvae were obtained from a weevil colony maintained in isolation on a semi-de-fined diet for over 6 yr, with only occasional infusion of adult weevils from citrusgroves located near Lake Jem in central Florida and in Homestead, Florida. Larvaefrom field-collected adults were added once or twice each year and comprised no morethan 20% of the larvae in the colony. Larvae at one month of age were taken from thecolony and individually weighed. Groups of ten were selected at average weights of25-30 mg/group for placement on seedlings with one group of ten per seedling.

Plants

Seeds for rootstocks or hybrids were obtained from germplasm grown at the USHorticultural Research Laboratory (USHRL) Foundation Farm in Leesburg, FL, andfor

G. pentaphylla

from the Florida Division of Plant Industry Arboretum in WinterHaven, FL. Test seedling plants were grown from seed at the USHRL FoundationFarm and transferred for weevil challenges to the USHRL greenhouses in Orlando,FL.


473

Seedling Challenges

Challenges were conducted as described by Shapiro and Gottwald (1995), exceptthat the duration of those tests was 44 days. The starting weight of each

Diaprepes

larva was taken prior to placing ten larvae on each plant. Larvae were placed at 8 cmdepth in the soil, evenly distributed midway between the trunk of a seedling and thecircumference of the 1-gal pot. Each test consisted of seven replicates of each cultivar,one plant per replicate. Larvae were allowed to feed in the greenhouse on the roots of5 selections including two widely used commercial rootstocks (Carrizo and Swingle;42 days, from June 11 to July 23, 1996), one citrus relative,

G. pentaphylla

(42 days,from June 13 to July 25, 1996), and two citrus hybrids that are in final stages of test-ing as rootstocks (HRS-802 and HRS-896; 35 days, from May 22 to June 26, 1996).Seedlings were removed from pots, larvae were recovered, and survival rates and thelive weight of each surviving larva were recorded.

Diet-Incorporation Tests

Roots for diet-incorporation assays were obtained from uninfested seedlings col-lected from seedling challenge experiments. Following storage at -80

°

C, roots weremilled in a centrifugal mill (Retsch ZM-1000, Brinkmann, Westbury, NY) at 10,000 or15,000 rpm to < 0.5-mm particle size. Diet for incorporation was prepared by first add-ing 14 g agar to approximately 800 ml water, and heating to approximately 100

°

Cwhile mixing with a Braun (Lynnfield, MA) type 4169 hand-held homogenizer. As theagar cooled, 184 g of citrus root weevil diet premix #1675F (Bio-Serve, Frenchtown,NJ), which is used for routine rearing, was added. The mixture was thoroughly mixedand diluted to 1 L with water. Diet was distributed to 100-ml beakers, and 5 g of rootswere blended with 100 ml of diet when diet had cooled to a temperature of approxi-mately 50

°

C, the melting point of the agar used in the diet. Approximately 15 ml of dietwere rapidly poured into each plastic 30-ml shot cup (Jet Plastica, Hatfield, PA), al-lowed to cool, and dried for approximately 6 h under a laminar flow hood. Controls con-sisted of diet only with no roots added. One larva was added to each of 30 cups of dietper treatment, cups were covered, and larvae were allowed to feed for 32 days in theinsectary at an approximate temperature of 29

°

C under a light regime of 10:14 (L:D).Larvae were then separated from the diet and individually weighed for final weights.

Statistics

One-way ANOVA and post-hoc comparison of means (Tukey’s HSD) tests were per-formed using the Statistica (StatSoft 1995) version 5.0 Basic Statistics module.

R

ESULTS

AND

D

ISCUSSION

Larvae that fed for 35 days on roots of the two hybrid selections, HRS-802 andHRS-896, increased 7.6- and 6.1-fold over their initial live weight, to 222 and 184 mg,respectively (Table 1). Those that were fed for 42 days on the two commercial root-stocks, Carrizo and Swingle, increased 10.3- and 10.2-fold over their initial liveweight, to 229 and 236 mg, respectively. In contrast, larvae that were fed on roots of

G. pentaphylla

for 42 days increased only 2.5-fold over their initial live weight, to amean final weight of only 64 mg. There were no significant differences in mean finalweights among larvae grown on Carrizo, Swingle, and HRS-802. Larvae on HRS-896weighed significantly less than those on Swingle and Carrizo, although seven more

474



T

AB

LE

1.

C

HA

NG

E

IN

LA

RV

AL

WE

IGH

T

AN

D

SU

RV

IVA

L

OF

LA

RV

AE

AF

TE

R

FE

ED

ING

35

DA

YS

(

HR

S

-802

AN

D

HR

S

-896

)

OR

42

DA

YS

(C

AR

IZZ

O

, S

WIN

GL

E

,

OR

G.

PE

NT

AP

HY

LL

A

)

ON

RO

OT

S

OF

SE

ED

LIN

G

RO

OT

ST

OC

KS

OR

G.

PE

NT

AP

HY

LL

A

.

Mea

n W

eigh

t (m

g

±

SD

)

Wei

ght

Ch

ange

(m

g)

Su

rviv

al

3

Sta

rtin

g

1

Fin

al

2

N%

Sw

ingl

e23

.0

±

1.8

b23

5.5

±

54.

5a21

2.0

±

53.

5a60

86

±

13a

Car

rizo

22.3

±

1.2

b22

8.8

±

28.

6ab

206.

5

±

28.

7a58

83

±

14a

HR

S-8

0225

.7

±

1.0

a22

1.9

±

28.

2ab

196.

2

±

28.

0ab

6796

±

5a

HR

S-8

9625

.9

±

1.2

a18

4.2

±

14.

0b15

8.3

±

13.

7b61

87

±

10a

G. p

enta

phyl

la

26.1

±

2.0

a64

.3

±

14.

1c38

.2

±

13.

3c40

57

±

14b

1

Mea

n

±

SD

(N

= 7

) of

th

e st

arti

ng

wei

ghts

of

larv

ae p

lace

d 10

per

pla

nt

on e

ach

of

7 pl

ants

per

cu

ltiv

ar.

2

Mea

n

±

SD

(N

= 7

) of

th

e fi

nal

wei

ghts

of

larv

ae s

urv

ivin

g on

eac

h o

f 7

plan

ts p

er c

ult

ivar

.

3

Nu

mbe

r an

d m

ean

per

cen

tage

±

SD

(N

= 7

) of

th

e la

rvae

th

at s

urv

ived

on

eac

h o

f 7

plan

ts p

er c

ult

ivar

.F

igu

res

that

are

fol

low

ed b

y th

e sa

me

lett

er w

ith

in a

col

um

n a

re n

ot s

ign

ifica

ntl

y di

ffer

ent

(P <

0.0

5; A

NO

VA

fol

low

ed b

y T

uke

y’s

HS

D t

est)

.


475

days of feeding (42 days total) would have reduced this difference. However, larvalweight gain on all four cultivars was significantly different from the mean final weightof the larvae fed on

G. pentaphylla

roots for 42 days. This was despite the fact thatstarting weights of the larvae on HRS-802, HRS-896, and

G. pentaphylla

were signif-icantly, though only slightly, greater than the larvae placed on Swingle or Carrizo.

In diet-incorporation assays, larvae were fed for 32 days on the standard rearingdiet with or without milled roots incorporated into it (Table 2). Changes in meanweights of larvae fed on diet alone were greater than those fed on live roots. Larvalweights increased 16.8-fold on diet only, 13.9-fold on Carrizo, 12.0-fold on Swingle,15.1-fold on HRS-802, 12.2-fold on HRS-896, and 5.5-fold on

G. pentaphylla

. Mean fi-nal weights of all larvae except those fed on HRS-802 were significantly lower thanthose fed on diet alone. Final weights of larvae fed on

G. pentaphylla

were signifi-cantly lower than those of larvae fed either on diet alone or on diet with any of theother root selections incorporated. In two additional diet-incorporation assays, larvaefed on

G. pentaphylla

also gained significantly less weight than larvae on Swingle orCarrizo (unreported results).

The results are significant from two perspectives. First,

G. pentaphylla

roots sup-ported only very low growth rates, roughly one-third to one-fourth of those supportedby the other root systems. Previous results (Shapiro & Gottwald 1995) showed growthrates on Swingle, Carrizo, and six other cultivars that were 2.8- to 5-fold greater thanthe growth rate on

G. pentaphylla

in this study. On diet that incorporated milled roots,larval growth rates on

G. pentaphylla

were approximately one-half to one-third ashigh as on the other selections. Secondly, results from the diet-incorporation assaymirrored those with live root tests. The comparison between larval growth rates onlive roots and growth on roots incorporated into diet is striking and repeatable.

These tests highlight the usefulness of the diet-incorporation assay as a possiblesubstitute for tests on live plants. Not only does the diet-incorporation assay requireonly a fraction of a plant’s total root system, but roots can be stored indefinitely at -80

°

Cfor repeated tests whenever desired. Roots from any size of tree can also be readily col-lected from the field and tested without destroying the tree. This will allow compara-ble and parallel tests to be run on seedling, juvenile, and mature trees together.Effects of resistance discovered in seedlings can thereby be compared to the potential

T

ABLE

2. C

HANGE

IN

LARVAL

WEIGHT

AFTER

FEEDING

32

DAYS

ON

5

G

MILLED

ROOTSADDED

TO

100

ML

DIET

.

Weight (mg

±

SD)

1

Starting Final Change

Diet only

2

23.2

±

4.7a 390.0

±

99.4a 366.8

±

98.4aSwingle 22.2

±

4.5a 266.3

±

116.8b 244.1

±

115.3bCarrizo 22.6

±

4.4a 315.2

±

103.2b 292.6

±

102.2bHRS-802 21.5

±

4.6a 325.0

±

86.8ab 303.5

±

87.3abHRS-896 23.1

±

4.6a 281.4

±

112.3b 258.3 ± 112.0bG. pentaphylla 20.6 ± 4.0a 113.9 ± 41.8c 93.3 ± 40.6c

1Mean ± SD (N=30) of the weights of 30 larvae, all of which survived. Figures that are followed by the sameletter within a column are not significantly different (P < 0.05; ANOVA followed by Tukey’s HSD test).

2Cups with ‘diet only’ contained no ground roots.


for resistance in other stages of tree grown from similar germplasm. Roots from plantspecies entirely unrelated to citrus can also be tested for their effect on growth andsurvival of Diaprepes larvae.

The diet-incorporation assay will also be very useful for further studies on chemicalor biological constituents of roots that may be responsible for inhibited larval growth.Present results indicate a molecular or microbial source of larval growth inhibition. Inthe diet-incorporation test, finely milled roots of G. pentaphylla at only 5% concentra-tion in diet produced the same relative growth inhibition seen in whole live roots. Thislow requisite concentration of roots will reduce the time and sample size required toidentify active molecules or microbes. Although caveats in the use of diet assays foridentification of active compounds have been examined and discussed (Shapiro, 1992),this assay affords a powerful tool for identification of active root constituents.

In the current search for active biochemical factors in citrus for defense of root-stocks against Diaprepes, we have focused primarily on natural products that are ei-ther small chemical constituents (Shapiro et al., 1988; Shapiro, 1991) ormacromolecules such as defense-related proteins (Mayer et al., 1995; McCollum et al.,1995). Our discovery of growth-inhibiting activity in G. pentaphylla and the develop-ment of a bioassay to examine that activity should contribute to finding or developinga rootstock with resistance to the weevil.

ACKNOWLEDGMENTS

The authors thank Thomas Moyer, Charles Spriggs, and Karin Crosby for their ex-cellent technical assistance on this project, and Stephen Lapointe for writing the Re-sumen. Funds for this project were made available from the Citrus ProductionResearch Marketing Order by the Division of Marketing and Development, FloridaDepartment of Agriculture and Consumer Services.

REFERENCES

BEAVERS, J. B., AND D. J. HUTCHISON. 1985. Evaluation of selected Citrus spp. andrelatives for susceptibility to root injury by Diaprepes abbreviatus larvae (Co-leoptera: Curculionidae). Florida Entomol. 68: 222-223.

GRAY, A. I., AND P. G. WATERMAN. 1978. Coumarins in the Rutaceae. Phytochemistry17: 845-864.

MAYER, R. T., J. P. SHAPIRO, E. BERDIS, C. J. HEARN, T. G. MCCOLLUM, R. E. MC-DONALD, AND H. DOOSTDAR. 1995. Citrus rootstock responses to herbivory bylarvae of the sugarcane rootstock borer weevil (Diaprepes abbreviatus). Physi-ologia Plantarum 94: 164-173.

MCCOLLUM, T. G., H. DOOSTDAR, R. E. MCDONALD, J. P. SHAPIRO, R. T. MAYER, L. W.TIMMER, AND R. M. SONODA. 1995. Exploitation of plant pathogenesis-relatedproteins for enhanced pest resistance in citrus. Proc. Florida State Hort. Soc.108: 88-92.

NORDBY, H. E., AND S. NAGY. 1981. Chemotaxonomic study of neutral coumarins inroots of Citrus and Poncirus by thin-layer, gas-liquid and high-performance liq-uid chromatographic analyses. J. Chromatogr. 207: 21-28.

PANDA, N., AND G. S. KHUSH. 1995. Host plant resistance to insects, 431 pp., CAB In-ternational, Wallingford, UK.

SHAPIRO, J. P. 1991. Phytochemicals at the plant-insect interface. Arch. Insect Bio-chem. Physiol. 17: 191-200.

SHAPIRO, J. P. 1992. Assimilation, transport, and distribution in insects of moleculesfrom natural and artificial diets pp. 63-76 in T. E. Anderson and N. C. Leppla[eds.], Advances in Insect Rearing for Research and Pest Management. West-view Press, Boulder, Colorado.

Shapiro et al.: Citrus Root Resistance Bioassay 477

SHAPIRO, J. P., AND T. R. GOTTWALD. 1995. Resistance of eight cultivars of citrus root-stock to a larval root weevil, Diaprepes abbreviatus L. (Coleoptera: Curculion-idae). J. Econ. Entomol. 88: 148-154.

SHAPIRO, J. P., R. T. MAYER, AND W. J. SCHROEDER. 1988. Absorption and transportof natural and synthetic toxins mediated by hemolymph proteins, pp. 997-1005in F. Sehnal, A. Zabza and D. L. Denlinger [eds.], Endocrinological Frontiers inPhysiological Insect Ecology. Wroclaw Technical University, Wroclaw, Poland.

SMITH, C. M. 1989. Plant resistance to insects: A fundamental approach to insect pestmanagement, 464 pp., John Wiley & Sons, New York.

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

STATSOFT, INC. 1995. STATISTICA, release 5. StatSoft, Inc., Tulsa, OK.

Mitchell et al.: Effect of Parasitoids on Diamondback Moth

477

DIAMONDBACK MOTH (LEPIDOPTERA: PLUTELLIDAE): PARASITISM BY

COTESIA PLUTELLAE

(HYMENOPTERA: BRACONIDAE) IN CABBAGE

E. R. M

ITCHELL

, F. C. T

INGLE

, R. C. N

AVASERO

-W

ARD

AND

M. K

EHAT

1

Center for Medical, Agricultural and Veterinary EntomologyAgricultural Research Service, U.S. Department of Agriculture

Gainesville, Florida 32608

1

Agro. Res. Organization, The Volcani Center, P.O. B. 6, Bet-Dagan 50250, ISRAEL

A

BSTRACT

Cotesia plutellae

Kurdjumov was evaluated as a potential biological control agentfor diamondback moth,

Plutella xylostella

(Linnaeus), in cabbage in spring 1993 and1994. The parasitoids were reared in a commercial insectary in Texas, delivered over-night via air express, and released 24-48 h after receipt in cabbage fields in NortheastFlorida. In 1993, only adult parasitoids were released, but adults and cocoons were re-leased in 1994. The numbers of

C. plutellae

released ranged from 456 per ha per wkin 1993 to 1,334 per ha per wk in 1994. Four consecutive releases were made each yearbeginning in early February. Parasitism of diamondback moth larvae by

C. plutellae

ranged from 3.6 to 10.9%, and the level of parasitism was related to the total numbersof parasitoids released.

C. plutellae

parasitoids were complimentary to the naturallyoccurring parasitoid

Diadegma insulare

(Cresson), and the combined mean seasonalparasitism of diamondback moth exceeded 34% in some fields. There was no evidencethat

C. plutellae

became established in the general area although > 124,000 parasi-toids were released over the 2-year test period.

Key Words:

Plutella xylostella

, biological control, integrated pest management,

Dia-degma insulare

R

ESUMEN

Cotesia plutellae

Kurdjumov fue evaluada como agente potencial de control bioló-gico para

Plutella

xylostella

(Linnaeus) en la col, en las primaveras de 1993 y 1994. Elparasitoide fue criado en un insectario comercial en Texas, enviado por correo expreso,y liberado a las 24-48 horas de recibido en campos de col del nordeste de la Florida. En

478



1993 solamente fueron liberados parasitoides adultos, pero en 1994 fueron liberadosadultos y capullos. Los números de

C

.

plutellae

liberados estuvieron en el rango de los456 por ha por semana en 1993, a los 1,334 por ha por semana en 1994. Cuatro libe-raciones consecutivas fueron hechas cada año comenzando a principios de febrero. Elparasitismo de

P. xylostella

por

P. plutellae

estuvo en el rango de 3.6 a 10.9%, y el nivelde parasitismo estuvo relacionado con los números de parasitoides liberados. Los pa-rasitoides fueron complementarios del parasitoide natural

Diadegma insulare

(Cres-son), y el parasitismo combinado estacional de

P. xylostella

excedió el 34% en algunoscampos. No hubo evidencia que

C

.

plutellae

llegara a establecerse en el área a pesarde que más de 124,000 parasitoides fueron liberados durante los dos años del período

de prueba.

The diamondback moth,

Plutella xylostella

(Linnaeus), is a serious pest of crucif-erous crops throughout the world. In tropical and subtropical areas, crucifer produc-tion has been seriously affected in recent years by populations that have developedresistance to a wide range of insecticides (Talekar & Shelton 1993). Until the mid-1980s in North America, diamondback moth was considered a minor pest, possibly be-cause biological control by natural enemies maintained populations below economi-cally damaging levels. In the United States, increases in the pest have been mostsevere in southern states, especially Florida, Georgia, North Carolina, and Texas. In-secticide resistance appears to be the most important cause (Leibee & Savage 1992,Leibee et al. 1995).

Bacillus thuringensis-

based pesticides and growth regulators areeffective control agents with minimal environmental impact, provided resistance canbe avoided (Shelton et al. 1993).

Combining pest control tactics may be the best approach for handling pesticide re-sistance in diamondback moth.

Biever et al. (1994) described the evolution and imple-mentation of a biological control-integrated pest management system for lepidopterouspests of crucifers developed over a period of 24 years. Basically the program consists ofthree elements: regular scouting of the crop to estimate plant damage and larval infes-tations; application of pesticides only when needed with reliance upon

Bacillus thur-inginesis

-based insecticides; and preservation of natural enemies combined withperiodic releases of parasitoids.

Cotesia plutellae

Kurdjumov frequently is mentioned as a possible biological con-trol agent for diamondback moth (Talekar & Shelton 1993). There have been sporadicreleases of this parasitoid in Florida

(

Frank & McCoy 1993), but little data are avail-able on its recovery or efficacy. This study reports on the recovery of

C. plutellae

incommercial cabbage fields subjected to conventional pest control practices followinginoculative releases of this parasitoid. Data also were collected on the seasonal occur-rence and effectiveness of

Diadegma insulare

(Cresson), a naturally-occurring larvalparasitoid of

diamondback moth. The trials were conducted near Bunnell, FlaglerCounty, Florida during the winter-spring cabbage growing seasons of 1993 and 1994.

M

ATERIALS

AND

M

ETHODS

Parasitoid Source

Cotesia plutellae

parasitoids used in this study were purchased from Biofac, Inc.,Mathis, TX. The parasitoids were shipped overnight via air express to Gainesville, FL.Adult parasitoids were shipped in 1993 and cocoons were shipped in 1994. The adults


479

(about 250 ea) were packaged in small cardboard cylinders (12.7 cm long

×

3.81 cmdiam) capped at both ends. The cylinders were wrapped with old newsprint and bun-dled in a Styrofoam chest containing packets of ice enclosed in plastic bags (alsowrapped with old newsprint) to keep the insects immobile while in transit.

In 1994, cocoons on paper towels (about 1,000 ea) were enclosed in plastic bags,wrapped with old newsprint and inserted in Styrofoam containers for shipping as de-scribed for adult parasitoids. Upon arrival, the cocoons were subdivided as requiredto meet test requirements. Adult parasitoids released in 1994 were received as co-coons and allowed to emerge in the laboratory. The parasitoids were fed a 10% honey-sugar water solution while in confinement.

Adult parasitoids released in 1993 were placed in the field within 48 h after ship-ment from the insectary in Texas. Adult parasitoids released in 1994 were shipped toFlorida as cocoons, allowed to emerge in the laboratory, and placed in the field within24 h after emergence.

Pesticide Applications

Grower cooperators applied pesticides to the cabbage crop at their discretion.

1993 Field Trials

Parasitoid Release

-Adult parasitoids were released in two cabbage fields in 1993(Fig. 1). Release area 1 (field 1) was 12.1 ha in size and part of a large cabbage field to-

Fig. 1. Schematic of experimental site. Inset shows arrangement of parasitoid re-lease stations and sampling sites (1994 only) in fields A, C, and D. Field B had six re-lease stations and sampling sites (2 rows of 3 each). Bunnell, Flagler County, FL.

480



taling 24.2 ha, the western half of which was designated as a control area (field 2). Thesecond release area (field 3, 8.1 ha) was located about 1.3

km west of release area 1(Fig. 1). The second control area (field 4, 4.0 ha) joined field 3 along the southeast edge.

The test fields were located in agricultural areas devoted to the production of cab-bage and potatoes. Field 1 was bordered on the eastern edge by wooded swamp, thesouth by potato fields, the west by the control (field 2), and the north by potato fields.Control field 2 was bordered on the south and north by potatoes and on the west byopen pasture land. Field 3 (release area 2) was bordered on the north by woodedswamp, the east and west by cabbage in various stages of maturity, and the south bycabbage (field 4) and fallow crop land.

Cotesia plutellae

were released in fields 1 and 3 at a target rate of 494 adults perha for four consecutive weeks beginning 24 February. This release rate was basedupon the recommendation of D. Biever (pers. comm.) from his experiences in develop-ing an integrated management system for pests of crucifers over a 24-year period(Biever et al. 1994).

Estimates of actual release rates were made by examining the re-lease containers for dead parasitoids. The sex ratio was approximately 1:1 as deter-mined from examination of representative samples of adults before they werereleased. The parasitoids were transferred from shipping cylinders into 0.24 liter pa-per cartons equipped with screened lids for release. A cotton ball in a small plastic cupsaturated with 10% honey-sugar water solution provided a food source for the parasi-toids. The cartons were placed in the field at the base of cabbage plants and opened toallow the parasitoids to escape. Thirty release sites were established in field 1 (12.1ha) and 20 were established in field 3 (8.1 ha). The release sites were spaced equidis-tant throughout the field in either a 5

×

6 (field 1) or 4

×

5 grid (field 3). Thus, each re-lease site was near the center of a 0.4 ha block of cabbage.

Sampling procedure

-Each parasitoid release field and correspondent control fieldwas systematically sampled weekly throughout the growing season for evidence of

C.plutellae

activity. Each field was divided into four sections nearly equal in size acrossits width; each section then was subdivided into thirds throughout the length of thefield. Timed searches of cabbage plants selected at random were conducted in each ofthe 12 sections (10 min ea). Thus, each field was scouted for diamondback moth larvaeand cocoons or parasitoids for a total of 2 h per wk. The larvae and cocoons collectedwere returned to the laboratory and held at ambient conditions of 25

±

2

°

C, 70-80%RH and under continuous fluorescent lighting for emergence of adult moths or para-sitoids. The larvae were held individually in 29.6 ml plastic cups on a modified pintobean diet (Guy et al. 1985) until emergence of adult moths or parasitoids, or until thelarvae died. Diamondback moth pupae and parasitoid cocoons were held separately in0.24 ml plastic cups until emergence of adults or death.

1994 Field Trials

The location of cabbage fields used in 1994 are shown in Fig. 1. Fields A and D were12.1 ha in size, field C was 10.5 ha, and field B was 4.8 ha. Field D was the same fieldused as a control area (i.e., field 2) in 1993. Field A was bordered on the south and northby cabbage, the east by wooded swamp, and the west by a drainage ditch, unpavedcounty road, and open pasture land. Field B was bordered on the north and east by ma-turing cabbage fields ready for harvest or that had been harvested but the plant residuehad not been destroyed; potato fields bordered the field on the west; and the south sidewas bordered by a state highway across which was maturing or harvested cabbage fields.

Parasitoid release

-Parasitoids were released either as cocoons or adults. Cocoonswere released in fields A and C at a target rate of 1,482 and 741 per ha, respectively,and adult parasitoids were released in field B at a target rate of 741 per ha. Estimates


481

of actual release rates were established later by examining the release containers fordead cocoons or adults a few days after each release. Four releases of adult parasitoidsor cocoons were made every two weeks beginning 06 February. The sex ratio as deter-mined from cocoons held in the laboratory for emergence was about 1:1. Releasecages, measuring 60 cm long

×

38 cm wide

×

30 cm high, were partially covered on thesides with 0.32-cm mesh hardware cloth to allow adult parasitoids to exit (Fig. 2). Acotton ball in a plastic cup was saturated with 10% honey-sugar water solution to pro-vide a food source for the adults upon emergence.

Turlings et al.(1989, 1990a and b) conditioned

C. marginiventris

(Cresson)

femalesto search for larval hosts after exposure to odors from plants damaged by beet army-worm [(

Spodoptera

exigua

(Hübner)] larvae. They also reported that

C.

marginiven-tris

females were significantly more responsive to the odors after a brief contactexperience with host-damaged leaves contaminated with host by-products; but actualencounters with hosts were not required to improve subsequent responses to host-re-lated odors. We obtained similar results with

C. plutellae

females in flight tunnel as-says after exposure to cabbage plants damaged by diamondback moth larvae(unpublished). Thus, cabbage plants bearing diamondback moth larvae were placedinside each release cage to condition adult

C. plutellae

parasitoids to search for hostsupon exiting the release station.

The release cages (9 in fields A and C, 6 in field B) were spaced equidistance apartthroughout each field (Fig. 1). The cages were mounted on metal conduit poles indrainage ditches so that the bottom of the release station was about 0.5 m above thetop of the cabbage plants. Cocoons, still attached to paper toweling, were placed in pa-per cups and set in the cages next to a potted cabbage plant with feeding diamondbacklarvae. Adult parasitoids in 0.24 liter paper cups were chilled in a Styrofoam chest fortransport to the field. A paper cup containing the requisite number of parasitoids wasplaced in the release cage adjacent to a potted cabbage plant with feeding diamond-back moth larvae.

Sampling procedure

-The fields were sampled weekly for host larvae and pupaeand cocoons of parasitoids, namely

C. plutellae

and

D. insulare.

Nine sites were sam-pled in fields A, C, and D and six in field B (Fig. 1, see inset). The sample sites wereabout equally spaced throughout each field. Initially, all cabbage plants (mean = 65)on 15.2 m of row were examined for larvae, pupae, and cocoons; but as the season pro-gressed and the plants grew in size, the distance was decreased to 3 m per site (mean= 13 plants) the week of harvest.

The diamondback larvae collected were brought into the laboratory where mostwere dissected to determine if they were parasitized (Day 1994). Some larvae wereheld on artificial diet as previously described for emergence of moths or adult parasi-toids to confirm identifications determined by dissections. Diamondback moth pupaeand parasitoid cocoons also were held separately in 0.24 ml plastic cups until theyemerged or died.

Statistical analysis

-Parasitism of diamondback moth larvae in 1993 was analyzedusing unpaired t-tests (Littell et al. 1991). The analyzes compared the combined ef-fects of field and treatment, i.e., field 1 + parasitoid releases vs. field 2 + no parasitoidrelease; and field 3 + parasitoid releases vs. field 4 + no parasitoid release (Fig. 1). Inthe 1994 trial, a 1-way analysis of variance (ANOVA) was used with fields as the fac-tor and mean percent parasitism or number of diamondback moth larvae per plant asthe response variable. As in the 1993 trial, the analyzes compared the combined ef-fects of field and parasitoid releases (A, B, and C) or field and no parasitoid release (D)(Fig. 1). Differences indicated by significant ANOVA were compared using the Waller-Duncan K-ratio t-test (Littell et al. 1991).

482



Fig. 2. Release station for Cotesia plutellae parasitoids. Cocoons or adult parasi-toids were placed in open paper cups and set in the release cage next to a potted cab-bage plant infested with diamondback moth larvae.


483

R

ESULTS

1993 Release

The number of parasitoids targeted for release was 494 per ha. Examination of therelease cartons within 24 h after each release period revealed that only 7.5% of theparasitoids had died. Thus, the actual number of parasitoids released was about 456per ha. Over the release period, an estimated total of 18,500

C. plutellae

adults werereleased in fields 1 and 3 (Fig. 1).

A total of 2,802 diamondback moth forms (1,415 larvae and 1,387 pupae) were col-lected in the four test fields which yielded 725 parasitoids and 1,246 diamondbackmoth adults. The remainder died in the holding cups before pupation or eclosion asadults.

Although low, percent parasitism (mean

±

s.e.) of host larvae by

C. plutellae

wassignificantly greater (unpaired t-test, Littell et al. 1991) in release fields 1 and 3 thanin the correspondent controls, fields 2 and 4 (Fig. 1): field 1 = 0.76

±

0.29 vs. field 2 =0, t = 2.315, 21 d.f., P = 0.031; and field 3 = 2.14

±

0.76 vs. field 4 = 0, t = 2.384, 17 d.f.,P = 0.029.

There also was no significant difference in the percentage of diamondback larvaeparasitized by the naturally-occurring

D.insulare

in the parasitoid release fields (1and 3) versus the control fields (2 and 4): field 1 = 28.51

±

3.27 vs. field 2 = 25.86

±

3.14;t = 0.572, 21 d.f., P = 0.573; and field 3 = 24.65

±

5.42 vs. field 4 = 22.26

±

4.68; t =0.316, 17 d.f., P = 0.756. Mean parasitism of host larvae by

D. insulare

in the fourfields was 25.68

±

2.05%.

1994 Release

Examination of the cartons used to release cocoons and adults revealed that > 90%of the parasitoids had survived and escaped the release cage. Thus, the targeted re-leases of 1,482 and 741 cocoons or adults per ha actually was about 1,334 and 667 co-coons or adults, respectively. Over the release period, an estimated total of 105,840

C.plutellae

parasitoids were released in fields A, B, and C.A total of 3,310 diamondback moth forms (2,004 larvae and 1,306 pupae) were col-

lected in all fields in 1994. A total of 653

D. insulare

and 162

C. plutellae

also were re-covered, most all of which were identified from dissections of diamondback mothlarvae (Day 1994). Specimens of a few other species also were noted, but they were notidentified.

The seasonal occurrence of diamondback larval populations in fields A-D and thelevel of larval parasitism in each are shown in Fig. 3. There was no significant differ-ence in the mean (

±

s.e.) number of diamondback moth larvae per cabbage plant infields A (0.035

±

0.010), B (0.016

±

0.006), C (0.030

±

0.009), and D (0.030

±

0.005)when averaged over the season. These results were not surprising as the grower co-operators sprayed their cabbage as frequently as deemed necessary to protect the cropfrom economic damage.

As expected, the highest mean level of parasitism of diamondback larvae by

C. plu-tellae

was recorded

in field A (10.9%) where the largest number of cocoons were re-leased. However, mean larval parasitism by

C. plutellae

in this field was notsignificantly different from field C (5.4%) where about 50% fewer cocoons were re-leased (Table 1). Parasitism of diamondback larvae by

C. plutellae

in field B (target of741 adults per release) and D (no parasitoids released) was 3.6

±

1.5% and 0%, respec-tively. The weekly levels of parasitism by

C. plutellae

in each field closely paralleledthe release of the parasitoid (Fig. 3). After parasitoid releases were terminated, par-

484



asitism by

C. plutellae

in fields A, B, and C became progressively less through the re-mainder of the season.

Mean parasitism over the cabbage-growing season by the naturally-occurring par-asitoid

D. insulare

was highest in fields A (29.4%) and B (31.3%); intermediate in fieldD where no

C. plutellae

were released (20.7%); and lowest in field C (8.6%) (Fig. 3 andTable 1). Mean total parasitism attributed to both

C. plutellae

and

D. insulare

alsowas highest in fields A (40.3%) and B (34.9%). Mean total parasitism of diamondbacklarvae in fields C and D was 13.7% and 20.7%, respectively.

There was no evidence that

C. plutellae

survived and became established in thetest area following releases made in 1993 or 1994. Growers typically plant the same

Fig. 3. Seasonal incidence of diamondback moth larval populations and parasitismby Cotesia plutellae and Diadegma insulare in cabbage. R = date parasitoids were re-leased; S = date field was sprayed with insecticide. Bunnell, FL. 1994.


485

fields in cabbage year after year. Thus, we were able to examine the fields in whichparasitoids were released in 1993 and 1994 to determine if there was carryover of

C.plutellae

into the following spring cabbage growing season. No

C. plutellae

were re-covered in field D in spring 1994 although

C. plutellae

were recovered in this area inspring 1993 following release of adult parasitoids in field 1 (Fig. 1). In spring 1995,cabbage in field A (where parasitoids were released in spring 1994, Fig. 1) and field Dwere sampled intensely at weekly intervals from February through April and not asingle

C. plutellae

parasitoid was recovered. Cabbage in field C, where

C. plutellae

co-coons were released in spring 1994 (Fig. 1) and parasitism of host larvae averaged5.4% for the season (Table 1), also was sampled intensively at weekly intervalsthroughout the winter-spring 1995 cabbage growing season. As in fields A and D, no

C. plutellae

were recovered.In fall 1992, we released a total of 24,981

C. plutellae

adults in two cabbage fieldstotaling 12 ha near Zellwood in Central Florida (unpublished). Three releases of aboutequal numbers of parasitoids (target number per ha = 625) were released at weeklyintervals beginning 16 November. These parasitoids also were purchased from Biofac,shipped overnight via air express as described, and released the following morning di-rectly from shipping tubes (250 adults ea) in which they were received. The tubeswere evenly spaced throughout each field and placed beneath cabbage leaves forshade. As in the 1993 and 1994 trials, the fields used in 1992 were sprayed heavily,

T

ABLE

1. R

ELATIONSHIP

BETWEEN

RELEASES

OF

C

OTESIA

PLUTELLAE

AND

THE

NATU-RALLY

-OCCURRING PARASITOID DIADEGMA INSULARE ON PARASITISM OF DIA-MONDBACK MOTH LARVAE IN CABBAGE IN 1994. BUNNELL, FL.

Field Cotesia Released1 Stage Number/ha Mean % Parasitism (± s.e.)2

Parasitism by Cotesia (P = 0.0003)A Cocoons 1482 10.9 ± 2.9aB Adults 741 3.6 ± 1.5bC Cocoons 741 5.4 ± 1.7abD None 0 0c

Parasitism by Diadegma (P = 0.0023)A Cocoons 1482 29.4 ± 4.4aB Adults 741 31.3 ± 7.4aC Cocoons 741 8.3 ± 3.4bD None 0 20.6 ± 4.5a

Total parasitism (P = 0.0013)A Cocoons 1482 40.3 ± 3.8aB Adults 741 34.9 ± 7.0abC Cocoons 741 13.7 ± 3.6cD None 0 20.7 ± 4.5bc

1The targeted number of parasitoids per release is shown. The actual numbers released, based upon subse-quent mortality counts, was about 90% of total shown. Parasitoid releases were made at 2-week intervals on fourdifferent occasions starting 06 February.

2Means in the same group with different letters are significantly different, Waller-Duncan K-Ratio T test (P-values are shown in parentheses).


TABLE 2. PESTICIDES USED FOR INSECT CONTROL IN CABBAGE FIELDS WHERE THE PARASI-TOID COTESIA PLUTELLA WAS RELEASED IN 1994. BUNNELL, FL.

Date Material Rate/ha Mortality Index1

Field A - 1,482 cocoons/ha22-Feb Monitor 0.71 liter 4

Xentari 0.24 liter 110-Mar Monitor 0.71 liter 424-Mar Monitor 0.71 liter 401-Apr Phosdrin 0.71 liter 4

Field B - 741 cocoons/ha03-Feb Monitor 4 0.47 liter 408-Mar Lannate LV 0.47 liter 418-Mar Lannate LV 0.47 liter 4

Dipel 2X 0.45 kg 128-Mar Lannate LV 0.47 liter 402-Apr Thiodan 0.95 liter ND

Dipel 0.45 kg 112-Apr Lannate LV 0.47 liter 4

Xentari 0.23 kg 1

Field C - 741 cocoons/ha07-Feb Xentari 0.34 kg 121-Feb Monitor 0.71 liter 4

Dipel 0.45 kg 109-Mar Dipel 0.45 kg 116-Mar Agree 0.45 kg 123-Mar Phosdrin 0.95 liter 431-Mar Lannate LV 0.71 liter 4

Xentari 0.23 kg 105-Apr Phosdrin 0.71 liter 4

Field D - control10-Feb Monitor 0.71 liter 4

Agree 0.34 kg 108-Mar Phosdrin 0.83 liter 4

Agree 0.23 kg 121-Mar Asana 0.24 liter 108-Apr Agree 0.23 kg 1

Dipel 0.23 kg 1

1Mortality index for Cotesia adults: 1 = harmless (50%); 2 = slightly harmful (50-79%); 3 = moderately harm-ful; 4 = harmful (> 99%); ND = no data. All materials sprayed were relatively harmless to Cotesia cocoons. (Kaoand Tzeng 1992).

Mitchell et al.: Effect of Parasitoids on Diamondback Moth 487

and diamondback larval populations were low. Total parasitism of diamondback by C.plutellae was < 0.1%; and no C. plutellae were recovered in these fields in spring or fall1993.

DISCUSSION

Numerous attempts have been made to introduce C. plutellae into different areasof the world with mixed results (Talekar & Shelton 1993). In the western hemisphere,C. plutellae reportedly flourished after introductions into Barbados and Jamaica, andit is credited with affecting significant control of diamondback moths on these andother Caribbean islands (Alam 1992). However, attempts to introduce C. plutellae intoHonduras, Belize, Costa Rica, and Florida (USA) have not resulted in suppression ofdiamondback moths (Andrews et al. 1992, Frank & McCoy 1993).

Explanations for establishment of C. plutellae in some areas and not others are notreadily apparent. Cotesia plutellae are numerically responsive to increasing popula-tions of diamondback moths (Ooi 1992, Rowell et al. 1992) and thrive in environmentsthat have not been sprayed with insecticides (Alam 1992). In Florida, cabbage andother cole crops are treated regularly with insecticides to keep pest populations lowand prevent damage by diamondback moth larvae (McLaughlin & Mitchell 1993,McLaughlin et al. 1994, Leibee et al. 1995, and Table 2).

In conclusion, C. plutellae reproduced in the fields where released, did not survivemore than one year, and probably was much less important than the naturally-occur-ring parasitoid D.insulare. There also was no evidence that C. plutellae dispersed toother fields nearby. However, in a subsequent study Mitchell (unpublished) found thatC. plutellae parasitoids spread down wind from the release area but parasitism of di-amondback moth larvae on sentinel cabbage or collard plants decreased as the dis-tance from the release area increased up to 800 m.

ACKNOWLEDGMENTS

We appreciate the help of W. Copeland and J. Rye in sampling the fields and pre-paring the release sites; B. Monroe for constructing the parasitoid release cages; J.Gillet for checking larvae for evidence of parasitism; and J. Leach for compiling thedata and preparing the graphics. We extend a special thanks to V. Chew for helpfulsuggestions on analysis of the data. This article reports the results of research only.Mention of a proprietary product does not constitute an endorsement or the recom-mendation for its use by USDA.

Lannate 0.95 liter 414-Apr Asana 0.24 liter 122-Apr Asana 0.24 liter 1

TABLE 2. (CONTINUED)PESTICIDES USED FOR INSECT CONTROL IN CABBAGE FIELDS WHERETHE PARASITOID COTESIA PLUTELLA WAS RELEASED IN 1994. BUNNELL, FL.

Date Material Rate/ha Mortality Index1

1Mortality index for Cotesia adults: 1 = harmless (50%); 2 = slightly harmful (50-79%); 3 = moderately harm-ful; 4 = harmful (> 99%); ND = no data. All materials sprayed were relatively harmless to Cotesia cocoons. (Kaoand Tzeng 1992).


REFERENCES CITED

ALAM, M. M. 1992. Diamondback moth and its natural enemies in Jamaica and someother Caribbean islands, pp. 233-243 in N. S. Talekar [ed.], Diamondback Mothand Other Cruciferous Pests: Proceedings of the Second International Work-shop. Shunhua, Taiwan. Asian Vegetable Research and Development Center.

ANDREWS, K. L., R. J. SÁNCHEZ, AND R. D. CAVE. 1992. Management of diamondbackmoth in Central America, pp. 487-497 in N. S. Talekar [ed.], DiamondbackMoth and Other Cruciferous Pests: Proceedings of the Second InternationalWorkshop. Shunhua, Taiwan. Asian Vegetable Research and DevelopmentCenter.

BIEVER, K. D., D. L. HOSTETTER, AND J. R. KERN. 1994. Evolution and implementationof a biological control-IPM system for crucifers: 24-year case history. AmericanEntomol. 40: 103-108.

DAY, W. H. 1994. Estimating mortality caused by parasites and diseases of insects:Comparison of the dissection and rearing methods. Environ. Entomol. 23: 543-550.

FRANK, J. H., AND E. D. MCCOY. 1993. The introduction of insects into Florida. FloridaEntomol. 76: 1-53.

GUY, R. H., N. C. LEPPLA, J. R. RYE, C. W. GREEN, S. L. BARRETTE, AND K. A. HOLLIEN.1985. Trichoplusia ni, pp. 487-494 in P. Singh and R. F. Moore [eds.]. Handbookof Insect Rearing, Vol. 2. Elsevier, Amsterdam.

KAO, S.-S., AND C.-C. TZENG. 1992. Toxicity of Insecticides to Cotesia plutella, a para-sitoid of diamondback moth, pp. 287-296 in N. S. Talekar [ed.], DiamondbackMoth and Other Cruciferous Pests: Proceedings of the Second InternationalWorkshop. Shunhua, Taiwan. Asian Vegetable Research and DevelopmentCenter.

LEIBEE, G. L., AND K. E. SAVAGE. 1992. Evaluation of selected insecticides for controlof diamondback moth and cabbage looper in central Florida with observationson insecticide resistance in the diamondback moth. Florida Entomol. 75: 585-591.

LEIBEE, G. L., R. K. JANSSON, G. NUESSLY, AND J. L. TAYLOR. 1995. Efficacy of ema-mectin benzoate and Bacillus thuringinesis at controlling diamondback moth(Lepidoptera: Plutellidae) populations on cabbage in Florida. Florida Entomol.78: 82-96.

LITTELL, R. C., R. J. FREUND, AND P. C. SPECTOR. 1991. SAS System for linear models,3rd edition, Cary, NC: SAS Institute. 329 pp.

MCLAUGHLIN, J. R., AND E. R. MITCHELL. 1993. Integration of mating disruption tocontrol lepidopterous pests of cabbage, pp. 104-108 in L. J. McVeigh, D. R. Hall& P. S. Beevor [eds.], Use of Pheromones & Other Semiochemicals in IntegratedControl - Pheromone Technology in Europe and The Developing Countries. Nat.Resources Inst., Chatham, England. Proc. OILB-SROP/IOBC Working Group,10-14 May, 1993 (Vol. 16(10).

MCLAUGHLIN, J. R., E. R. MITCHELL, AND P. KIRSCH. 1994. Mating disruption of dia-mondback moth (Lepidoptera: Plutellidae) in cabbage: Reduction of matingand suppression of larval populations. J. Econ. Entomol. 87: 1198-1204.

OOI, P. A. C. 1992. Role of parasitoids in managing diamondback moth in the CameronHighlands, Malaysia, pp. 255-262 in N. S. Talekar [ed.], Diamondback Moth andOther Cruciferous Pests: Proceedings of the Second International Workshop.Shunhua, Taiwan. Asian Vegetable Research and Development Center.

ROWELL, B., A. JEERAKAN, AND S. WIMOL. 1992. Crucifer seed crop pests, parasitesand the potential for IPM in northern Thailand, pp. 551-563 in N. S. Talekar[ed.], Diamondback Moth and Other Cruciferous Pests: Proceedings of the Sec-ond International Workshop. Shunhua, Taiwan. Asian Vegetable Research andDevelopment Center.

SHELTON, A. M., J. L. ROBERTSON, J. D. TANG, C. PEREZ, S. D. EIGENBRODE, H. K.PREISLER, W. T. WILSEY, AND R. J. COOLEY. 1993. Resistance of diamondback

Mitchell et al.: Effect of Parasitoids on Diamondback Moth 489

moth (Lepidoptera: Plutellidae) to Bacillus thuringinesis subspecies in thefield. J. Econ. Entomol. 86: 697-705.

TALEKAR, N. S., AND A. M. SHELTON. 1993. Biology, ecology, and management of thediamondback moth. Annu. Rev. Entomol. 38: 275-301.

TURLINGS, T. C. J., J. H. TUMLINSON, W. J. LEWIS, AND L. M. VET. 1989. Beneficial ar-thropod behavior mediated by airborne semiochemicals. Viii. Learning of host-related odors induced by a brief contact experience with host by-products in Co-tesia marginiventris (Cresson), a generalist larval parasitoid. J. Insect Behav-ior 2: 217-225.

TURLINGS, T. C. J., J. H. TUMLINSON, AND W. J. LEWIS. 1990a. Exploitation of herbi-vore-induced plant odors by host-seeking parasitic wasps. Science 250: 1251-1253.

TURLINGS, T. C. J., J. W. A. SCHEEPMAKER, L. E. M. VET, J. H. TUMLINSON, AND W. J.LEWIS. 1990b. How contact foraging experiences affect preferences for host-re-lated odors in the larval parasitoid Cotesia marginiventris (Cresson) (Hy-menoptera: Braconidae). J. Chem. Ecol. 16: 1577-1589.

490



THE “MUSEO DE ENTOMOLOGIA Y BIODIVERSIDAD TROPICAL” OF THE AGRICULTURAL EXPERIMENT STATION,

UNIVERSITY OF PUERTO RICO

R. A. FRANQUI

1

, J. A. SANTIAGO-BLAY

2

, S. MEDINA GAUD

1

and E. ABREU

3

1

Department of Crop Protection, Agricultural Experiment StationUniversity of Puerto Rico, Río Piedras, Puerto Rico 00928

2

Department of Ecology and Evolution, 1101 East 57th StreetThe University of Chicago, Chicago, IL 60637

3

Department of Crop Protection, Agricultural Experiment StationUniversity of Puerto Rico, Isabela, Puerto Rico 00662

H

ISTORY

OF

THE

C

OLLECTION

The collection of the Museo de Entomología y Biodiversidad Tropical (formerly theEntomology Museum) at the Agricultural Experiment Station (AES) of the Universityof Puerto Rico is the largest depository of insects in Puerto Rico (Santiago-Blay

et al

.in prep.). The collection harbors more than 200,000 specimens, mostly from PuertoRico, in its main collection at Río Piedras (not to be confused with the Río PiedrasCampus of the University of Puerto Rico that also houses significant biological collec-tions) and some additional holdings in the Isabela (approximately 5,000 insects of ag-ricultural importance and 1,200 identified Acari).

The collection was started in 1910 by D. L. Van Dine, W. V. Tower, E. G. Smyth, C.E. Hood, and G. N. Wolcott, all entomologists working with sugarcane in Puerto Rico(Cook and Otero 1937). Following the successful control of insect pests in major com-modities in the continental United States, great emphasis was placed in solving prac-tical agricultural problems caused by insects, such as sugarcane white grubs,


(L.) (Coleoptera: Curculionidae), and

Phyllophaga

spp. (Co-leoptera: Scarabeidae), in the Island. Some examples of biological control that influ-enced research activities in Puerto Rican agricultural entomology were: 1) the cottonycushion scale (

Icerya purchasi

Mask., Homoptera: Margarodidae) in California or-anges controlled by

Rhodolia cardinalis

Mulsant (Coleoptera: Coccinellidae) and

Cryptochaetum iceryae

Williston (Diptera: Cryptochaetidae) in the late 1880s), and 2)the sugarcane leafhopper (

Perkinsiella saccharicida

Kirkaldy, Homoptera: Cicadel-lidae) in Hawaii controlled by several parasites, of which

Paranagrus optabilis

Per-kins (Hymenoptera: Mymaridae) was perhaps the most important (Perkins andKirkaldy 1907). These are interesting cases in the history and interactions betweenscience, agribusiness, government, and the general public in Puerto Rico.

Since 1910, the main collection has been housed in several locations within the Bi-ology Building at the AES in Río Piedras, expanded, and kept as a research tool. Oneof the unique aspects of this collection is the detailed accession number catalog thatcross-references about 85% of the pinned specimens with additional biological data.The efforts of dedicated researchers, such as George N. Wolcott, Luis F. Martorell, JoséGarcía Tudurí, Silverio Medina Gaud, Niilo Virkki, and many others contributed tothe collection’s maintenance and development. The collection has had some teachingfunctions and has been used to identify insects for the public.

Since November 1996, the collection has been located on the east wing of the Edi-ficio de Agronomía (Agronomy Building) in front of the Biology Building, and it was of-ficially inaugurated on May 9, 1997. In addition to its space devoted to research

Scientific Notes

491

collections, the “Museo” has beautiful, new exhibits for the public. The stream of vis-itors and local media coverage have been overwhelming. The collection has been for-mally recognized by the administration of the Agricultural Experiment Station, andin its new location the collection occupies 336.5 square meters; an additional 119.7square meters were recently transferred to the “Museo” and they are being developed.

H

OLDINGS

The Museo de Entomología y Biodiversidad Tropical holds approximately 220,000organisms representing the 27 orders of insects known to occur in Puerto Rico (Borror

et al.

1989 classification; Mycrocoryphia, Grylloblattaria, Plecoptera, and Mecopterahave not been reported for the island). Major collections include those of Thysan-optera, Aphididae (Homoptera), Trichoptera (recently donated by Dr. Oliver Flint, Na-tional Museum of Natural History, Washington, D. C.), Muscidae (Diptera), and anassorted collection pertaining to medical and veterinary entomology. The collectionholds a modest number of mollusks, some Diplopoda, Chilopoda, as well as arachnids,

T

ABLE

1. A

PPROXIMATE

NUMBER

OF

HOLDINGS

OF

H

EXAPODA

IN

THE

M

USEO

DE

E

NTO-MOLOGIA

Y

B

IODIVERSIDAD

T

ROPICAL

AT

THE

A

GRICULTURAL

E

XPERIMENT

S

TATION

OF

THE

U

NIVERSITY

OF

P

UERTO

R

ICO

.

TaxonNumbers and

remarks TaxonNumbers and

remarks

Protura 136 Psocoptera 629Collembola 38 Phiraptera 253

1

Diplura 67 Hemiptera 7,647Thysanura 29 Homoptera 10,063

2

Ephemeroptera 793 Thysanoptera 6,899

3

Odonata 2,456 Neuroptera 1,267Phasmida 144 Coleoptera 12,682

4

Orthoptera 729 Strepsiptera 10Mantodea 46 Siphonaptera 317Blattaria 1,422 Diptera 10,767

5

Isoptera 2,622

6

Trichoptera 2,258Dermaptera 189 Lepidoptera 10,775Embiidina 10 Hymenoptera 9,389Zoraptera 81 Total 81,718

Other assorted specimens, in liquid preservatives 137,000

TOTAL 218,718

1

Including 171 identified specimens from Puerto Rico on slides.

2

Including 891 identified specimens of aphids from Puerto Rico on slides.

3

Including 1,453 identified specimens from Puerto Rico on slides.

4

Does not include significant numbers of immature Scarabaeidae and Curculionidae in liquid preservatives.

5

Including 100 identified

Aedes

larvae from Puerto Rico on slides. However, this number does not include sig-nificant holdings of

Anastrepha

immatures in liquid preservatives.

6

Does not include significant holdings of specimens in liquid preservatives.

492



including spiders and scorpions. Details of the holdings for the Hexapoda are summa-rized in Table 1.

L

OAN

P

OLICY

Currently, loans are made for three years and are renewable following written no-tification. Loan requests should be addressed to Dr. R. A. Franqui. We request authorsto forward reprints of any publications resulting from the use of our material. Also, weare pursuing the return of material on indefinite, or unauthorized loans.

R

EFERENCES

C

ITED

B

ORROR

, D. J., C. A. T

RIPLEHORN

,

AND

N. F. J

OHNSON

. 1989. An introduction to thestudy of insects, 6th ed. Philadelphia, PA. Saunders College Publ. 875 pp.

C

OOK

, M. T.,

AND

J. J. O

TERO

. 1937. History of the first quarter of a century of the Ag-ricultural Experiment Station at Río Piedras, Puerto Rico. Bull. 44. Agric. Exp.Stn. 123 pp.

P

ERKINS

, R. L. C.,

AND

G. W. K

IRKALDY

. 1907. Parasites of leaf-hoppers. Report ofwork of the Experiment Station of Hawaiian Sugar Planters’ Association. Bull.4. 66 pp.

Book Reviews

493

BOOK REVIEWS

D

ELOYA

L

OPEZ

, A. C. (ed). 1997. La Sociedad Mexicana de Entomología: pasado,presente y futuro. Sociedad Mexicana de Entomología; Xalapa, México. Paperback, v+ 202 p. ISBN 968-7801-01-8. Available from: Sociedad Mexicana de Entomología,ATTN. Cuauhtémoc Deloya, Apartado Postal 63, 91000 Xalapa, Veracruz, MEXICO(US$15 + $5 packing and shipping to addresses in the USA).

Hallman et al. (1992) American Entomologist 38: 22-32 give thumbnail accounts ofentomological societies in the Americas south of the USA. To the best of my knowl-edge, none of these societies has ever produced such a comprehensive account of itshistory and current activities as has the Sociedad Mexicana de Entomología (SME,the Mexican Entomological Society).

Founded in 1952, SME includes in its 10 principles (Chapter 1) the study of insectsand related arthropod taxa of the Mexican fauna by Mexican nationals and foreigners,comprising the taxonomy, zoogeography, ecology, and biology of these taxa, and methodsfor the control of pest species among them. Chapter 2 is a brief sketch of past-presidents(each of whom served for two years), honors awarded by SME, the founding in 1962 ofthe journal Folia Entomológica Mexicana, the production of newsletters, meetings (anannual congress was inaugurated in 1975), and the existence of regional delegations.

Chapter 3 details the organization of meetings, the composition of the governingboard, and the actions of organizing committees. Chapter 4 explores the production ofFolia Entomológica Mexicana and other publications. Chapter 5 examines attendanceat annual congresses, and the sub-disciplines of the participants. Chapter 6 looks atthe direction followed by SME and compares it with other societies in the Americassouth of the USA.

Chapter 7 has a directory of active members in 1995-1996. It explains SME’s muchlarger total directory which, it is planned, should become searchable by internet earlyin 1998. Chapters 8 and 9 deal with the library maintained by SME at the InstitutoNacional de Diagnóstico y Referencia Epidemiológicos (INDRE) in Mexico City, theagreement establishing the housing of this library, and a detailed list of the journalsthat it holds by exchange with other societies nationally and internationally (the listis impressive) and a few books and theses. Chapter 10 is an analysis of editorial stan-dards of Folia Entomológica Mexicana by its editor. Chapter 11 has three indices ofthe contents of that journal. The first is an author index. The second is a subject indexusing such headings as “medical and veterinary entomology”, “behavior” and “physi-ology”, and “economic entomology” subdivided by agricultural crop. The third is a 39-page author/title index subdivided taxonomically at the levels of order and family.

The final 6 chapters (12-17) contain the current statutes, the rules for organizationof meetings and activities, the rules for organization of national meetings, the rulesfor awarding prizes to students for theses and dissertations, and function of two spe-cial delegations to SME.

What other entomological society from Florida southward could now recount itshistory in such detail? This book is a challenge to the other entomological societiesfrom Florida to Argentina to do as adequate a job before their historical records arelost or damaged.

J. H. FrankEntomology/Nematology DepartmentUniversity of FloridaP.O. Box 110620Gainesville, FL 32611-0630

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