The Ecology and Behavior of a

Subsocial Pentatomid Bug

and Two Scelionid Wasps:

Strategy and Counterstrategy in a

Host and Its Parasites

WILLIAM G. EBERHARD

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SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY • NUMBER 205
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SMITHSONIA N CONTRIBUTION S T O ZOOLOG Y • NUMBE R 20 5

The Ecology and Behavior of a

Subsocial Pentatomid Bug

and Two Scelionid Wasps:

Strategy and Counterstrategy in a

Host and Its Parasites

William G. Eberhard

SMITHSONIAN INSTITUTION PRESS

City of Washington

1975
ABSTRACT

Eberhard, William G. The Ecology and Behavior of a Subsocial Pentatomid Bug

and Two Scelionid Wasps: Strategy and Counterstrategy in a Host and Its Parasites. Smithsonian Contributions to Zoology, number 205, 39 pages, 13 figures,

24 tables, 1975.—The tropical bug Antiteuchus tripterus and two parasites of its

eggs, Trissolcus bodkini and Phanuropsis semiflaviventris, were studied in urban

Cali, Colombia. Female bugs guard both their eggs and first instar nymphs.

Behavioral observations, combined with analyses of the patterns of parasitism

within egg masses of a given form, showed that the details of the bug's defensive

behavior and the wasps' attacks strongly influence the survival rates of eggs in

different positions in an egg mass.

By removing guarding female bugs from their eggs, it was shown that the net

effect of their defense against generalized egg predators is to greatly improve egg

survival but that, paradoxically, the net effect against the parasitic wasps is to

decrease survival. Although the bugs repel wasps that have found egg masses, the

bug's presence over the mass betrays the location of the eggs to hunting wasps.

A hypothetical evolutionary history suggests that as the bugs improved their

protection of eggs, they produced thinner egg shells, and that they are now

trapped into continuing their defense in spite of subsequent advances by the

wasps in their hunting behavior. Experimental removal of bugs guarding first

instar nymphs and calculations of the cost of guarding in terms of egg production

showed that the net effect of this guarding behavior is positive.

Female P. semiflaviventris tend to stay and hunt in the tree where they emerge,

while T. bodkini females tend to disperse. Parasitism rates by P. semiflaviventris

are strongly influenced by the species of tree where the bug eggs are laid, and

both species are influenced by the site of the egg mass (leaf, branch, sucker), but

in different ways. Both species also wait near bugs about to oviposit and attack

eggs as they are laid, apparently recognizing gravid bugs visually. Parasitism

rates of eggs on naturally and experimentally isolated leaves showed that search

behavior is accomplished in flight.

Natural selection with respect to oviposition site varies greatly with tree species

and the site on a given tree. The balance of selection was evidently different

where the bugs evolved than in present-day Cali, where they commonly act

against their own best interests.

Both wasp species agree in general with the behavior pattern for Scelionidae,

but differ in several characteristics associated with oviposition. P. semiflaviventris

is consistently farther from the family norm than is T. bodkini. The two species

of wasp compete at two stages in their life cycle, with neither species consistently

dominating. The males fight and exclude each other from egg masses where

females will emerge, and multiple ovipositions into single bug eggs produce

only single wasps. Both types of competition occur commonly in urban Cali.

Many other aspects of the natural history and ecology of the bugs and wasps

are presented.

OFFICIAL PUBLICATION DATE is handstampcd in a limited number of initial copies and is recorded

in the Institution's annual report, Smithsonian Year. SI PRESS NUMBER 5381. SERIES COVER DESIGN:

The coral Montastrea cavernosa (Linnaeus).

Library of Congress Cataloging in Publication Data.

Eberhard, William G.

The ecology and behavior of a subsocial pentatomid bug and two scelionid wasps.

(Smithsonian contributions to zoology ; no. 250)

Supt. of Doc. no.: SI 1.27:205

1. Antiteuchus tripterus. 2. Trissolcus bodkini. 3. Phanuropsis semiflaviventris. 4. Hostparasite relationships. 5. Insects—Behavior. I. Title. II. Series: Smithsonian Institution.

Smithsonian contributions to zoology ; no. 205.

QL1.S54 no. 205 no. 205 [QL523.P5] 591'.08s [595.7'54] 75-619087
Contents

Page

Introduction 1

Materials and Methods 2

The Natural History of Antitenchus tripterus limbativentris 2

Distribution and Host Plants of the Bugs 3

Eggs 3

First Instar Nymphs 6

Second Instar Nymphs 6

Older Nymphs and Adults 7

Behavior of Females Guarding Eggs and Nymphs 10

The Natural History of the Wasps Trissolcus bodkini and Phanuropsis

semiflaviventris 12

Hunting Behavior 13

Oviposition 17

Stages in the Eggs of A. tripterus 20

Emergence from the Egg 21

Sex Ratios 21

Male Behavior 21

Clusters of Females 22

Interactions between Wasps and Bugs 23

Wasps vs. Bugs Guarding Eggs 23

Wasps vs. Ovipositing Bugs 27

Competition between Species of Wasps 28

Within Bug Eggs 28

Fights between Males 29

Experimental Removal of Bugs Guarding Eggs 29

Other Factors Affecting A. tripterus Survival 30

Unhatched Eggs 30

Leaves and Egg Masses That Fell from Trees 31

Losses of First Instar Nymphs 31

Other Enemies of A. tripterus 33

Discussion 33

Hunting Behavior of the Wasps 33

Competition between the Wasps 34

Evolutionary Relationships of the Wasps 35

Selection Pressures on the Behavior of the Bugs 36

Literature Cited 38

in
FIGURE 1.—Female A. tripterus defending her eggs against the scelionid egg parasites Trissolcus

bodkini (rear edge of egg mass) and Phanuropsis semiflaviventris (in front of bug). As the

P. semiflaviventris female backs in with her abdomen extended, the bug lowers her antennae to

the leaf and scrapes the edge of the egg mass with her front foot, and the T. bodkini female

oviposits in an egg at the poorly guarded rear edge.
The Ecology and Behavior of a

Subsocial Pentatomid Bug

and Two Scelionid Wasps:

Strategy and Gounterstrategy in a

Host and Its Parasites

William G. Eberhard

Introduction

This paper describes the natural history of the

tropical pentatomid bug Antiteuchus tripterus

limbativentris Ruckes and two parasitic wasps,

Trissolcus bodkini and Phanuropsis semiflaviventris Girault, which attack the bug's eggs. Female bugs guard their eggs from the wasps and

also guard their first instar nymphs. The wasps use

special behavior patterns to overcome the female

bug's defensive behavior and oviposit in her eggs

(Figure 1). The wasp larva kills the bug embryo

and consumes the entire contents of the egg; then

it pupates and finally emerges as an adult from the

egg (generally while the female bug is still standing

guard over her nymphs) mates (usually with a

sibling), and then leaves to seek out new eggs to

parasitize.

The quantitative results of the bug's selection of

oviposition site, of her defensive behavior, of competition between the two wasp species, and of the

specialized attack behavior of one of the wasps

(P. semiflaviventris) were measured by analyses

of variations in the patterns of parasitism between

and within egg masses and by experimental reWilliam G. Eberhard, Departmento de Biologia, Universidad

del Valle, Cali, Colombia, and Smithsonian Tropical Research

Institute, P. O. Box 2072, Balboa, Canal Zone.

moval of defending bugs from their eggs and

nymphs. Parental protection of the young (subsocial behavior) has evolved many times in the

insects (see E. O. Wilson, 1971), and in the

Hemiptera is known in 14 species in 12 genera

(Bequeart, 1935; Odhiambo, 1959), but this is

apparently the first detailed study of the precise

effects of parental care in subsocial insects.

ACKNOWLEDGMENTS.—I owe a large debt of gratitude to the people who kindly identified the organisms in this study: M. Becker {A. tripterus),

W. Brown (ants), L. S. Espinal (plants), H. E.

Evans (Bicyrtes), V. Gapud (other pentatomids),

R. D. Gordon (coccinellids), B. Jimenez and D.

Greer (fungus), and L. Masner and C. F. W.

Muesebeck (parasitic wasps). I am especially grateful to James Slater and George Vogt for various

forms of help and encouragement. John Lawrence

helped obtain the sticky material used in various

experiments, and the James Spain family allowed

me to clutter their trees with sleeve cages. M. J. W.

Eberhard, M. Emsley, D. Otte, J. Reiskind, G. W.

Salt, N. G. Smith, and D. Strickland kindly criticized earlier drafts of this manuscript. Figure 1 was

drawn by Dana Gardner.

This study was supported by the Comite de Investigaciones, Universidad del Valle, Cali,

Colombia.
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Materials and Methods

Data used in this study were collected intermittently in and near Cali, Colombia, from November

1969 through December 1972 and in Bucaramanga,

Colombia, in October of 1972. Voucher specimens of A. tripterus, T. bodkini, P. semiflaviventris, and all the species listed in Table 22 have

been deposited in the Museum of Comparative

Zoology at Harvard University, Cambridge, Massachusetts 02138; other voucher specimens have been

placed in the collection of the Universidad del

Valle in Cali, Colombia.

Unless otherwise noted, all tests of significance

were Chi2. Two statistical procedures used need

special explanation. Sometimes, in order to obtain

large numbers of data to test hypotheses, it was

necessary to sum the data from several trees having

different parasitism rates. In these cases, the median was established for each tree and the data

from that tree were classified as either above or

below this median; finally, the data (above the

median, below the median) were summed over

several trees.

In comparing total parasitism rates (between

trees, for example), it was not possible to use

Chi2 because host eggs were laid in groups and

their probabilities of being parasitized were thus

not independent. Instead, all masses in each sample

with the usual number of 28 eggs were ordered on

the basis of numbers of eggs parasitized, and then

the two samples were compared using the Willcoxon Sum of Ranks Test.

The sticky material used to isolate trees and egg

masses from walking insects was "Tack Trap," a

nonvolatile, relatively inert substance manufactured by Animal Repellents, Inc., Griffin, Georgia,

USA.

The reader should keep in mind that all of the

observations were made in the highly unnatural

environment of urban Cali and that great care

must be used in extracting conclusions about the

evolutionary interactions between the organisms

involved on the basis of this data. For instance,

the fact that the bug's oviposition preferences in

Cali cause it to place most of its eggs in relatively

high- rather than low-risk sites does not imply that

natural selection has somehow failed to operate

on the bugs; the most likely explanation is that

one or several of the many causes of egg mortality

is so modified in the urban environment that the

relative mortality rates between oviposition sites

are changed as compared to those in the environment in which the bug evolved. On the other hand,

since many aspects of the behavior of both bugs

and wasps are presumably innate and would be

performed in the same way in any habitable environment in which the insects found themselves,

certain types of evolutionary conclusions can be

drawn. For instance, the fact that the bug's defense

of its eggs, which gives numerous signs of being

designed to combat the parasitic wasps, nevertheless increases rather than decreases the chances of

parasitism by the wasps implies that the parasitic

wasps have in some sense "out-evolved" their hosts.

The behaviors involved—defense by the bug,

searching and attack by the wasps—very likely are

the same in "natural" situations (those in which

the animals originally evolved, if such places still

exist), and the net result of the bug's defense

would thus also be the same.

The Natural History of

Antiteuchus tripterus limbativentris

Antiteuchus tripterus limbativentris Ruckes, a

race described from the Cauca Valley of Colombia

(Ruckes, 1966) belongs to the principally neotropical subfamily Discocephalinae. This species

ranges from Panama to Paraguay. I have found it

in Colombia in zones classified by Espinal and

Montenegro (1963) as dry tropical forest (Cali and

Palmira), humid semitropical forest (Bucaramanga), and humid tropical forest (Buenaventura). In places in Colombia it is an important

pest of cultivated cocoa (cacao) and mango trees,

and is apparently used as a folk cure for intestinal

parasites (Kardonne, 1972). Naundorf (1954) and

Sepulveda (1955) showed that the bug can act as a

vector of the fungus Monilia, which attacks the

fruit of cocoa. Lima (1940) notes that A. amplus

also damages cocoa in Brazil, and Callan (1944b)

records A. piceus as a minor cocoa pest in Trinidad. Rau (1918), Callan (1944a), and Kirkpatrick (1957) have observed that A. tripterus females

stand guard over eggs and first instar nymphs, and

Callan, Kirk pa trick, and Sepulveda (1955) all deduced from the pattern of parasitism of several egg

masses that the bug's defense was at least partially

effective against the scelionid egg parasite Phanu-
NUMBER 205

ropsis semiflaviventris. Callan (1944b) recorded

maternal care in several additional Antiteuchns

species, including A. (A.) piceus, mixtus, and

variolus, and A. (Neodine) macraspis.

DISTRIBUTION AND HOST PLANTS OF THE BUGS

The bug A. tripterns is extremely common in

trees and bushes in urban Cali, Colombia. The

bugs were nonspecific in their host plant selection

and were found on the trees Pithecelobium dulce

(Combretaceae—an exotic), Canagium odoratum

(Anonaceae—also an exotic), Cassia sp. (Cesalpinaceae), Lagerstromia speciosa (Litraceae), Crescentia cujete (Bignoniaceae), cocoa (Theobroma

cacao—Sterculiaceae), and mango (Mangifera

indica—Anacardiaceae). They also occurred on the

shrubs Malvavicus arboreus (Malvaceae), Hibiscus

sp. (Malvaceae), Heliconia sp. (Musaceae), and

Bouganvilla glabra (Mictaginaceae). In the countryside near Cali the bugs were found on P. dulce,

Calliandra sp., Croton sp. (Euphorbiaceae), and

Tabebuia chrysantha (Bignoniaceae). Sepulveda

(1955) presents a similarly varied host list. Bug

populations were generally larger on some species

of plants (such as P. dulce, T. catappa, and Cassia

sp.) than on others (such as B. glabra, M. indica,

and Heliconia sp.), and the majority of my observations were made on the first three species.

Bugs were much more common on plants inside

the city than outside. This difference was clear on

two species of trees (P. dulce and Calliandra sp.)

that occurred commonly in both areas. It also appeared that within the city the bugs tended to be

more common where there was heavy pedestrian

and/or automobile traffic. For instance, nine small

P. dulce trees at the edge of a park near the center

of the city (along the Rio Cali), where many

people walked, supported heavy bug populations,

while other similar trees 10-20 m inside the park

had fewer bugs. The reason for these tendencies is

unknown.

The size and form of a plant also appeared to

influence its attractiveness to A. tripterus. Trees or

bushes of a given species having denser growth

tended to have more bugs. In the case of P. dulce,

many large and small trees were searched, and although the absolute bug populations could not

usually be determined, it was certain that the

densest populations were in medium and small

trees. The bugs were very common. One particularly densely populated tree was about 2.5 m high

at the center and about 7 m in diameter, and had

over 200 female bugs guarding eggs or nymphs at

one time. Based on surveys in other trees, this represents a total adult population of about 2400

bugs.

The effects of both tree form and location on

population size were relatively weak within the city,

however, and I was not able to correctly predict

how many bugs a given tree would have. Bug populations in individual trees sometimes changed

substantially over time.

EGGS

DESCRIPTION.—Eggs were barrel-shaped, 1.47 mm

tall and 0.97 mm in diameter, and lacked the

spines (chorionic processes) found on the rims of

many pentatomid eggs (Esselbaugh, 1947). Their

cuticle was smooth and relatively thin and weak

compared with those of the eggs of other pentatomids such as Nezara sp., Supputius sp., Podisus

cloelia, and Loxa sp. The cap was the strongest

part and was reinforced by a fine network of small

ridges on its inner surface.

Two distinct colors of unparasitized eggs could

often be distinguished within the same mass. Usually (perhaps always—some differences were difficult to be sure of) a group of 28 had 14 of one

color and 14 of another. Most of the eggs of a given

color were usually grouped more or less together.

In some cases where the order of oviposition could

be deduced (see below), it was clear that the eggs

of one color were all laid before any of the others.

Dissection of a female killed just after laying the

14th egg of a mass showed that each of her 14

ovarioles had lost one egg and had one left. Thus

the differences in color of the eggs seem to be associated with the position (basal or apical) of the

eggs in the ovariole.

Almost all embryos in a given group of eggs

were usually oriented in the same direction within

their eggs (upward with their ventral surfaces all

oriented in the same direction), but usually at

TABLE 1.—Sizes of egg masses (N = 230)

Number of eggs in the mass: 28 27 26 14

Frequency: 90% 6% 3% 1%
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 2.—Frequency of masses of 28 eggs that were

in the "compact" form (Figure 12) in different tree

species

Location

Leaves ...

Branches

Canagium

P. dulce Cassia sp. odoratum T. catappa

32%

(N=766)

32%

(N=236)

44%

(N=406)

27%

(N = 189)

42%

N = 224)

least one or two embryos in each group were substantially out of line dorsoventrally with the others.

Since the female's bug orientation during oviposition was constant, these eggs must have turned before or as they emerged.

SITES AND ARRANGEMENTS.—As shown in Table 1,

there were almost always 28 eggs in each egg mass.

The eggs in masses were generally closely packed,

and the most common arrangement was the "compact" form pictured in Figure 12, with minor

variations on this (such as that in Figure 4) also

relatively common. The frequency of the compact

arrangement varied with the species of tree, as

shown in Table 2; both T. catappa and Cassia sp.

differ significantly (p<0.05) from both C. odoratum and P. dulce. Since compact egg masses were

TABLE 3.—Relationship between total number of

egg masses in a P. dulce tree and the frequency of

oviposition on leaves vs. branches (p <.O1)

Site

Leaves ..

Branches

Number

Number

of masses

of trees

Trees with > 20

guarded egg masses

88%

12%

1308

13

Trees with < 20

guarded egg masses

76%

24%

106

9

less heavily parasitized than others (below), these

differences may influence parasitism rates on different trees.

As in other pentatomids (Esselbaugh, 1946), the

eggs were usually laid on the undersurfaces of

leaves or branches. As shown in Table 3, there was

a positive correlation on P. dulce trees between

the relative numbers of masses on leaves vs.

branches and the total number of egg masses on

the tree (probably an indirect measure of the adult

population). This does not necessarily mean that

the bugs were reacting directly to the population

size on a given tree, as an additional factor or factors could influence both population size and

choice of egg sites.

Compact masses of eggs on leaves were usually

oriented so that the group's longitudinal axis was

parallel to that of the leaf and its pointed end was

toward the leaf tip, but this varied somewhat in

different species of tree (Table 4). The orientation of masses on T. catappa was significantly different from those on the other tree species: it may

be that the greater size of its leaves is somehow

responsible for the difference (Figure 2). Since the

orientation of the defending bug is highly correlated with the orientation of the egg mass, and

the orientation of the bug is probably in turn correlated with the hunting behavior of egg parasites

(below), the consistent orientation of the egg masses

on leaves may be the result of selection pressure

exercised by hunting wasps.

Figure 3 shows how oviposition sites varied with

leaf size. On leaves from 3-10 cm long, the eggs

were nearly always placed near the base. On very

small leaves (less than 2 cm long) they tended to

be nearer to the tip (p<0.05), while on very large

leaves they were distributed randomly. The function of the tendency to place eggs near leaf bases is

TABLE 4.—Orientation of "compact" egg masses on the leaves of different trees

Orientation

Longitudinal axis more nearly parallel than

perpendicular to leaf axis

Those so aligned which had point of group

toward leaf tip

Total number of masses observed

P. dulce

100%

95%

163

Cassia sp.

97%

95%

132

Canagium

odoratum

90%

98%

50

T. catappa

65%

69%

87
NUMBER 205

not certain, but it may serve to protect them from

water damage. On observing the undersides of

Cassia sp. and P. dulce leaves just after a rain, I

found that the water standing on them was concentrated along the lower edge of the leaf, and in

most cases this was the tip of the leaf. Thus eggs at

leaf bases are probably less likely to be covered

with water during and after rain. Experimental immersal of eggs in water for various lengths of time

showed that older eggs were killed more readily and

that appreciable reduction in hatching was first

seen after between 6 and 9 hours of immersion,

when it fell from 70% to 10%.

The apparently random positioning of eggs on

large leaves and their placement toward the tips of

small leaves do not at first seem to fit this explanation. Observations of large T. catappa leaves just

after rain indicate, however, that they seldom get

wet at all on the underside where the bug eggs are

nearly always located; and placement of eggs nearer

the bases of leaves less than 2 cm long might be

physically difficult for the bug (length about 1 cm)

since it lays the eggs nearest the leaf base last, and

would thus have to actually climb off the leaf to

lay eggs nearer to the leaf base.

DEVELOPMENT.—No structure was visible within

the eggs until 3.5-4 days after oviposition (the

times varied somewhat, presumably due to temperature variations), when the embryo's eyes and egg

burster became preceptible. They darkened gradually (but did not grow in size) until the nymphs

hatched 130-170 hours (about 5.5-7 days) after

being laid. Sepulveda (1955), working in nearby

Palmira on cocoa (which is grown in the shade

and may have been cooler), reports the egg life as

9-13 days. Eclosion times were spread over up to 12

hours in a given egg mass, but no pattern in the

sequence of hatching was discernible.

FIGURE 2.—Typical forms of the trees studied most intensively: a, Pithecelobium dulce (arrow

marks suckers); b, Cassia sp.; c, Terminalia catappa; d, leaves of (1) Cassia sp., (2) P. dulce,

(3) T. catappa, and (4) Canagium odoratum (arrow marks bug guarding eggs); e, pattern of

leaf growth in P. dulce (arrow marks site where sticky substance was applied in isolation experiments); /, pattern of leaf growth in Cassia sp. (arrow marks site where sticky substance was

applied in isolation experiments). (The scale bars in a, b, and c are approximately 2 m, those

in d and e are 5 cm, and that in / is 10 cm.)
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

100

80

6 0

8 40

SI

§ 1 20

§1POSITI' (%of d

f .

0

 °° w» „ »

• •

* *

» » »

• » _ »

• *

* • •

• • • » » »

a Pithecelobium dulce

v Cosslo sp

. Canagium odoratum

, Terminolia catappa * *

V

w

»

T T »

10 15 20 25 30

LENGTH OF LEAF (cm)

FIGURE 3.—The relationship between position of egg mass on a leaf and the size of the leaf.

35 40

FIRST INSTAR NYMPHS

Sepulveda (1955) found five nymphal instars in

A. tripterus, lasting on the average 7, 12.5, 22.5,

12.5, and 18 days respectively.

Newly emerged nymphs were relatively pale, but

acquired their final red-and-black markings within

five hours. At first they lacked the repellent odor

found in all later stages, but it was found (by

squashing and smelling nymphs of known ages)

that they began to smell faintly nine hours after

hatching, and did not have the odor at its final

strength until after more than 10 hours. Young

nymphs were rounder and less flat than those

which were several days old, and were also somewhat less active when disturbed.

First instar nymphs were generally very inactive,

staying very close to the egg mass. Nymphs displaced from their groups in captivity reassembled

around hatched and unhatched egg masses and/

or other nymphs, but not around adult females.

Assembled nymphs always touched either the eggs

and/or other nymphs (Figure 5b).

The first instar lasted approximately a week

both in nature and captivity, with variations of

more than a day. It is probable that the first instar

nymphs did not feed, as nymphs raised in plastic

vials with water but no food succeeded in moulting

to the second instar.

SECOND INSTAR NYMPHS

Individuals from a given egg mass moulted to

second instar within a period of up to several

hours. Usually a nymph prepared to moult by

climbing onto the surface of the eggs and appeared

to fix its tarsal claws into the eggs by slowly hooking their surfaces and gently pulling with each leg

several times. After about a minute's pause, the

nymph's abdomen began to contract, its cuticle

ruptured dorsally, and the second instar nymph

emerged. This moult (and all subsequent moults)

was accompanied by a temporary loss of repellent

odor, which remained with the shed skin, and this

was probably an especially dangerous time for the

bugs (see Table 22). Second instar nymphs reacquired their odor within 35-45 minutes after

moulting.

Newly moulted second instar nymphs were nearly

white with a few red markings, but they darkened
NUMBER 205

within a few hours to brown with black markings

(see Sepulveda, 1955, for detailed descriptions of

all nymphs). They were longer and wider than

first instars (3.1 mm long X 2.4 mm wide vs. 2.4

mm X 1.7 mm), but flatter and thinner, and were

much more active. They dispersed readily when

disturbed and, if not disturbed, left the egg mass

two to three days after moulting. The nymphs apparently began to feed in this stage, and were found

alone on leaves and twigs far from the nearest egg

mass. They showed little or no gregariousness after

leaving the vicinity of the egg mass, contrary to the

observations of Callan (1944b) on A. tripterus and

A. picea.

OLDER NYMPHS AND ADULTS

Bugs which had left the egg mass were almost

always found on branches and trunks rather than

leaves, except on the very large leaves of T. catappa

where nymphs were often seen along the central

leaf veins. In general, the younger stages tended to

stay on smaller branches. Outside the city most

bugs were found in hidden spots such as in crotches

and under tufts of lichen, but in urban trees, which

had fewer epiphytes and thus fewer hiding places,

they showed little tendency to concealment except

that they usually stayed on the lower rather than

the upper surfaces of branches. In some trees the

older nymphs and adults clustered in groups of up

to 40 or more; one sample group contained 7 males,

10 females, and 11 penultimate nymphs.

OVIPOSITION.—Most adult bugs were found on

twigs and branches, but females with swollen abdomens were not uncommonly found resting

quietly on the undersides of leaves. These females

were evidently ready to oviposit, as they generally

laid eggs within several days without feeding when

brought into captivity. In those trees on whose

leaves the female usually faced the tip while guarding her eggs (below), the swollen females also usually faced the leaf tip. This immobile stage may

represent a period during which the female "monitors" the characteristics of a potential oviposition

site before laying her eggs there. Females may

change sites several times before finally ovipositing;

when I marked the leaves on which five such females were resting (I tried not to disturb the bug

as I marked the leaf), all were deserted several days

later. These movements may serve as defense

against parasitic wasps which have located gravid

bugs before they are ready to lay (below).

The act of oviposition was observed on seven

occasions, and the movements were relatively constant. Figure 4 shows the sequence of the last 21

eggs laid in one egg mass and illustrates a pattern

of placement also seen in other ovipositions. The

bug laid a line of three eggs (i.e., numbers 12, 13,

and 14) on one side of the group, then two (i.e.,

15 and 16) on the other side, and then repeated

this sequence. This behavior appears to be designed to produce compact masses like that in

Figure 12.

The bug began laying an egg by moving forward

until the tip of her abdomen was in line with the

front edge of the group of eggs already laid. Then,

swinging her abdomen slightly from side to side,

she positioned its tip in the groove between two of

these eggs. The side-to-side movements probably

enabled her to feel the positions of already laid

eggs (which she could not see), possibly using the

laterotergites of segment nine. The bug lowered

her abdomen as she positioned herself and touched

FIGURE 4.—The sequence of the last 21 eggs laid by a female

A. tripterus.
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

the emerging egg to the leaf. Then, moving slightly

backward and lifting her abdomen, she drew the

egg out and tilted it back against the sides of the

eggs already laid.

Females paused from 15 to 60 seconds between

ovipositions, some bugs moving backward and more

or less covering the egg mass during these pauses,

others moving back only slightly. The backward

movement may play a part in the defense of the

eggs against parasitic wasps (below). Laying females generally faced the base of the leaf, and after

completing a mass of eggs, they turned 180° and

scraped the sides of the mass several times before

settling down—probably another defense against

wasps.

The period of time between a female's abandonment of her second instar nymphs and the laying

of her next egg mass was determined in the following way. Bugs caught guarding second instar

nymphs on P. dulce trees (i.e., females no more

than a day or two away from deserting their

nymphs) were placed in a sleeve cage on another

P. dulce. The mean time (to the nearest day) to

the next oviposition in two such experiments was

about 17 days (Table 5). Thus the normal time

between ovipositions is probably on the order of

30-35 days (7 days guarding eggs, plus 7 days

guarding first instar nymphs, plus 1-2 days guarding second instar nymphs, plus about 17 days of

feeding to prepare for the next oviposition).

Since female bugs probably seldom if ever feed

while guarding, and since females guarding eggs

have more fat than those guarding second instar

nymphs (below), it seemed likely that females

found guarding new eggs would be able to reoviTABLE 5.—Number of days required by female bugs

to reoviposit

Treatment

Females removed from groups

of second instar nymphs

Experiment 1

Experiment 2

Females removed from

newly laid eggs

Experiment 1

Females removed from groups of

newly hatched first instars

Experiment 2

Average

16.6

17 2

20

19

Range

12-21

13-25

16-25

14-24

Number

of bugs

13

35

21

22

posit sooner when removed from their eggs than

those removed from second instar nymphs. Just the

opposite was true, however, as 21 females which

were found on new eggs and placed in the same

sleeve cage, on the same day, with the females removed from second instar nymphs in the first experiment described above averaged 20 days to the

next oviposition, requiring significantly longer

(p< 0.002, Willcoxon Sum of Ranks Test) than

the others (Table 5). A similar experiment, during

somewhat cooler weather and involving females

taken from newly hatched first instar nymphs and

others taken from second instar nymphs, gave median reoviposition time of 19 and 17 days respectively (Table 5), the females from second instar

nymphs again laying eggs in significantly shorter

time (p<0.01, Willcoxon Sum of Ranks Test).

These data suggest that the female undergoes some

sort of hormonal cycle controlling fat and/or egg

synthesis even when out of contact with her eggs

and nymphs.

These data should perhaps be treated with

caution, at least concerning the absolute lengths of

interoviposition periods, since of 35 masses laid by

females removed from second instar nymphs in the

second experiment 8 had only 14 eggs (differs from

Table I, (p<0.01). Only females taken from second instars showed this behavior, as none of 22

masses laid during the same time by females from

first instar nymphs had 14 eggs (p<0.05). However,

dissections of bugs found guarding newly laid

masses with less than 28 eggs showed that females

probably usually do have a full complement of 28

eggs ready to lay, but may fail to lay some of them.

Each of four females on masses of 14 eggs had 14

more eggs of nearly identical size inside her abdomen and a fifth female on a mass of 15 had 11

more eggs inside.

MIGRATION.—The great majority of nymphs and

adults on one P. dulce tree were removed by hand

on 11-13 September 1972, and the tree was then

revisited and again cleaned of adults and larger

nymphs 16 and 25 days later. These repeat visits

revealed a substantial rate of immigration; 214 females and 213 males were found during the first

re-collection and 71 and 79 during the second, giving a combined rate of 11.5 females and 11.7 males

arriving at the tree per day. This figure may be

slightly high as a few adults were undoubtedly

missed during the first collection. The study tree
NUMBER 205

was not isolated, being part of a row of P. dulce

and only about 2 m and 8 m from its nearest neighbors (trunk-to-trunk distances), both of which had

substantial bug populations. Nevertheless, this

high rate of movement between trees was unexpected because (1) A. tripterus is not an especially good flier and even dislodged bugs usually

simply circled and flew back upwind to land on the

tree where they had been, and (2) bugs were seldom seen flying, even in densely populated areas.

The original collection of adults from this tree

had 518 males and 696 females or a ratio of 0.74

male: female. Assuming that the male: female ratio

in the trees from which the immigrants came was

the same, the relatively large number of males

which actually arrived suggests that males are more

mobile than females (p<0.01). This is perhaps

not surprising since females are immobile approximately two weeks while guarding the eggs and

nymphs of each brood. Since they live approximately 80 days as adults (Sepulveda, 1955) and

probably lay 2-3 batches of eggs, this would

amount to 35%-50% of their life spent immobile.

In fact, assuming conservatively that females spend

only 35% of their time guarding, that both sexes

migrate equally, and that the total sex ratio in the

population is 0.74:1 male:female, the expected

numbers of arriving males and females would be

306 and 269, not significantly different from the

observed 292 and 285.

Migrating females were apparently more likely

to lay eggs than others. Thus 22.2% of the 696 females in the first collection were guarding eggs or

nymphs; assuming a steady immigration rate (11.5

females/day) and the frequency of oviposition

calculated from the first collection (0.017 mass/

female/day), only 33 of the immigrant females

should have been guarding offspring rather than

the observed 58 (p<0.01).

The relative numbers of nymphs and adults

found in this tree suggest the additional conclusion that, despite the high rate of arrivals, even

more bugs left the tree than arrived. Relatively

careful counts of the numbers of unhatched eggs

present 16, 9, and 1 week (s) before the first collection indicated that the adult female population

was approximately constant during this period.

Since the total time from egg to adult is about 10

weeks (Sepulveda, 1955), relatively constant numbers of adults were being produced from nymphs

during at least the last 6 weeks before the first collection was made. The total number of last (5th)

instar nymphs found on the tree in the first collection was 1108, or approximately 90% of the

total number of adults. Since substantial movements between trees by nymphs are unlikely, and

since the duration of the 5th instar is only about

20% that of the adult, it appears that a large portion of the bugs which grew up on the tree left

after reaching maturity.

Several isolated observations indicated that adult

bugs of both sexes leave in especially large numbers

when trees shed their leaves. The best studied case

was in one P. dulce, which had had weekly counts

of 60-75 masses of unhatched bug eggs for five

weeks; within three weeks during which the tree

was shedding, the count fell to 5 masses. Observations of the trunk and branches showed that the

entire adult population in this tree had dropped

dramatically.

Other more casual observations also associated

shedding with bug desertion in both P. dulce and

T. catappa trees. None of the four tree species

which were observed most intensively seemed to

have an established season for shedding and, with

the exception of some individuals of T. catappa,

these trees were never completely without leaves,

new ones emerging before the last of the old ones

fell. I saw no dramatic fluctuations in bug populations during the erratic dry and wet seasons in

Cali, but did not make careful long-range counts.

Eggs were found at all times of the year.

OTHER BEHAVIOR.—Mating, feeding, and defecation were seen on trunks and branches. I found

six mating pairs, each with the two bugs facing

away from each other. Feeding bugs often held the

tips of their abdomens lifted away from the branch,

and sometimes appeared to have difficulty withdrawing their probosces from the wood when disturbed. Although ants such as Ectatomma ruidum

and Campanotus sp. often tended membracids and

coccids in trees harboring A. tripterus, I never saw

an ant show any sign of interest in a bug. The bugs

lifted their abdomens when they defecated a clear,

tasteless (to me) liquid, several drops at a time.

Both adults and nymphs gave characteristic responses when they were disturbed by bugs or other

objects which approached them. The most common responses were to antennate toward the object, to give a brief "shudder" of the entire body,
10 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

and to walk away. Upon more intense disturbance

(pinching a foot, for example), both nymphs and

adults kicked at the offending object with the middle or hind legs and/or gave off an unpleasant

odor. In favorable lighting one could sometimes

see the adults squirt the substance several centimeters laterally. Usually they buzzed their wings

for several seconds a minute or so later, perhaps to

rid themselves of any liquid still clinging to their

bodies. This behavior is probably what Callan

(1944b) took to be part of the defensive behavior

of females guarding eggs.

The repellent substance was poisonous and both

bugs and their eggs were killed by being placed in a

jar where adults had recently given off odor. On

two occasions I saw a first instar nymph die within

a minute after being hit directly by a spray (I had

pushed the female partway off her group of

nymphs). The substance was painful when placed

on soft areas of my skin or near my eyes and also

apparently corroded the plastic of a pen which I

used to nudge females off their groups of eggs and

nymphs.

Both males and females had bright orange bands

along the lateral edges of the ventral surface of

their abdomens. When adult bugs were disturbed

by the wasp Bicyrtes variegata (a predator on

large nymphs—see Eberhard, in press), or by other

stimuli approaching them more or less dorsally,

they sometimes tilted their bodies laterally, a movement probably designed to facilitate spraying the

offending object with repellent fluid (which was

ejected from openings near the bases of the legs).

The orange flanks of the bugs were also exposed by

this tilting of the body and the coloration may

thus be aposematic in function.

Adult males were usually darker (dark brown)

dorsally than females (tan to brown). I was able to

correctly guess the sex of 71 of 75 bugs in the field

solely on the basis of their dorsal coloration, missing two males and two females.

Bugs resting on the undersides of T. catappa

leaves in bright sunlight extended their legs to lift

their bodies away from the leaf surface, a movement probably serving in temperature regulation.

Bugs in raised positions lowered themselves within a few minutes when their leaves were shaded,

and rose up again when the shade was removed.

Both bugs guarding eggs and others raised themselves in this way, but guarding bugs immediately

lowered themselves when disturbed by an

approaching object or shadow.

BKHAVIOR OF FEMALES GUARDING EGGS AND NYMPHS

Female A. tripterus stood over their eggs and

nymphs both night and day and responded to various types of disturbances. They kept the eggs

under the front part of their bodies (Figure 5) and

were not easily displaced by pushing or pulling.

Their defensive movements included: tilting the

body toward the disturbance (thus forming a shield

between it and the eggs or nymphs); waving one or

both antennae toward it; shaking the entire body

with quick shuddering movements; scraping the

edge of the egg mass with the front legs (usually

done alternately, with the bug swinging her body

laterally so that she scraped along most or all of

the entire front and lateral edge of the mass, although occasionally they also scraped with their

middle legs); and kicking backward with the hind

and middle legs. Antennal and, to a lesser extent,

leg movements were directed toward the disturbing

stimulus. First instar nymphs clustered below the

female did not generally respond to her defensive

movements, but second instars often dispersed.

When female defensive responses were tested by

presenting the bugs with a model parasitic wasp,

females guarding eggs gave somewhat different responses than those guarding nymphs. The model

consisted of a small bit of black paper about the

size of a parasitic wasp glued to the end of a 15

mm clear nylon thread that was fixed to the end of

a 25 cm glass tube. The stimulus was moved near

the bug in approximately the pattern shown in

Figure 6. Visual stimuli from my hand may have

also stimulated the bug and, since she usually

moved her antennae toward the model as it approached, presentations often involved tactile stimulation as well. It was clear from these tests and

from observations of wasp-bug interactions, however, that the sight alone of a wasplike object would

release the bug's defensive behavior.

The frequencies of the various defensive responses are presented in Table 6. Scraping behavior diminished significantly when the bugs were

guarding nymphs, but shuddering increased. It is

reasonable that scraping should decrease since (1)

the female might damage her nymphs or knock

them off the leaf, and (2) there is no longer any
NUMBER 205 11

danger of parasitism by the wasps against which

this movement is particularly effective. The significance of the change in shuddering behavior is not

known.

Only very seldom, and only in moments of great

duress, did bugs battling wasps give off enough

odor for me to sense it. I also had the strong impression that bugs guarding eggs were much less

likely to discharge the poisonous repellent odor

when I disturbed them than were bugs over nymphs

or nonguarding bugs.

Female bugs showed no sign of being able to

distinguish their own eggs from those of others and

it was possible to transfer females to new egg

masses if the bug was moved directly from one to

the other. The longer the bug was out of contact

with eggs, however, the less likely she was to accept

the new group (even if she was placed back on her

original mass). On several occasions I saw a female

which had apparently changed groups spontaneously, leaving a group of new eggs unguarded as

she stood over a nearby group of old, empty eggs.

Females guarding nymphs were apparently more

attracted by the nymphs than by the mass of empty

eggs, as several females whose nymphs had clustered a centimeter or so from the egg mass were

standing over the nymphs rather than the eggs.

Females did not show any response to stray nymphs,

however.

Female bugs probably seldom if ever fed while

guarding eggs or nymphs, since I never saw a

guarding female feed and since adults were seen

feeding only on trunks and branches, never on

leaves where most eggs were located. The defensive

behavior of a female with her proboscis stuck in

the plant would probably be less effective since she

would be less mobile, and this may explain the

female's abstinence. Sepulveda (1955) noted puncture marks near egg masses on the stems of cocoa

pods and speculated that defending females may

feed. The evidence is weak, however, since stems

are a preferred feeding site for eggless bugs (Naundorf, 1954). Dissections of ten females collected

guarding newly laid eggs and of ten others collected guarding second instar nymphs also indicated that defending females fed little, if at all.

The females from new eggs all had moderate to

large fat bodies, while the others, which had been

FIGURK 5.—a, Female A. tripterns guarding her eggs on a leaf of C.

odoratum (arrow indicates rear, poorly defended side of egg mass);

b, female bug guarding first instar nymphs on a branch.
12 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 6.—Responses of defending female bugs to

artificial "wasp" stimuli

FIGURE 6.—Pattern of presentation of model wasp to defending

female bug.

guarding for about two weeks, had small or at most

moderate fat bodies. Most of the fat was probably

used to maintain the bug itself, as the ovaries in

both groups of females were undeveloped and approximately the same size.

The females' orientation as they guarded was not

random. On all except very large leaves (i.e., T.

catappa leaves), they tended to align themselves

with the leaf's axis, facing either its base or its tip.

In a study of the position of female bugs on P.

dulce leaves, it appeared that both the leaf itself

and, to a lesser extent, gravity had an orienting

effect on the bug. On nearly horizontal leaves,

83% of 69 females faced toward the tip rather than

the base; on leaves with their bases below their tips,

this percentage was 73% (N = 66); and on leaves

with their tips below their bases, it was 94%

(N = 522) (the last two figures differ significantly,

p<0.01). This orientation, which would seem to

make the bug less able to sense dangers arriving at

its leaf by walking along the stem, may be a result

of the parasitic wasp's tendency to hunt in flight.

Bug's response

Move antenna toward

stimulus

Lean toward stimulus

Move toward stimulus

Shudder

Scrape

Kick

Bug guarding

eggs (43 trials)

43

42

38

17*

28*

16

Bug guarding

nymphs (42 trials)

42

41

41

36*

8*

24

•Differ significantly (p < .05).

The orientation of females when guarding compact egg masses like that in Figure 12 was also far

from random, even on T. catappa leaves where the

egg mass itself was often not aligned with the

leaf's axis (Table 4). Of 94 females found on such

groups in T. catappa, 92% faced so their heads

were over the pointed end of the group (the top

of the group in Figure 12). This consistency probably aids in the defense of the group by bringing

the bug's front legs to bear on the smooth sides of

the mass where their scraping will be most effective.

The frequency with which female bugs deserted

their offspring was lower in some trees than in

others. During weekly visits to one P. dulce tree on

a very busy street where large trucks and buses

often passed close by (but where the bugs were

extremely common), females were missing from

27% of 195 groups of first instar nymphs, while the

corresponding figure from a slightly smaller P.

dulce at the edge of a small park in a residential

section was 11% (N = 82) (p<0.05).

The Natural History of the Wasps Trissolcus

bodkini and Phanuropsis semiflaviventris

The wasp Phanuropsis semiflaviventris Girualt

is the only described species in the genus Phanuropsis (a second species, to be described by L.

Masner, was raised from the eggs of Edessa sp.,

another subsocial penatomid), and there is no

literature on its biology other than that it parasitizes the eggs of A. tripterus and A. picea (Girualt, 1916; Callan, 1944a). Wasps of the genus

Trissolcus are parasites of pentatomid eggs (Ashmead, 1893). Vaukassevitch (1925; cited in F.

Wilson, 1961) describes several aspects of the ovi-
NUMBER 205 13

position behavior of T. simoni which conform to

the general pattern for the family Scelionidae.

Both P. semiflaviventris and T. bodkini "were

found in A. tripterus eggs in Cali and Buenaventura, Colombia, while only P. semiflaviventris

was present in Bucaramanga, Colombia, and apparently in Trinidad (Callan, 1944a); T. bodkini

was the only species in a small sample of four parasitized masses collected in Guapi, Colombia.

HUNTING BEHAVIOR

GRAVID BUGS.—Females of both species of wasp

were not infrequently found on leaves waiting

near swollen female bugs that were apparently

about to oviposit (Figure 7), and on several occasions they were observed parasitizing eggs as the

bug oviposited (female wasps were distinguished

in the field by their more pointed abdomens and

more clubbed antennae). Several females were also

seen waiting near mature male bugs and penultiFIGURF. 7.—Female T. bodkini wasp waiting near a gravid

female bug.

mate nymphs which were resting immobile on

leaves, suggesting that the important cues used to

recognize gravid females were visual—their general

size and the unusual sites (leaves) where they

rested. An experiment designed to test this, however, indicated that additional factors were also

involved.

About 40 mature bugs of both sexes were killed

in alcohol, dried, and mounted with their legs removed on short insect pins. The bugs were then

stuck on the undersides of the leaves of a Cassia

sp. tree, which had substantial populations of bugs

and both species of wasp. When I returned the

next day, only one of the dead bugs had a female

wasp waiting near it; the behavior of this female

(a P. semiflaviventris) suggested why wasps had

not congregated around the models. She walked by

the base of the leaf with the model on it seven times

within about 15 minutes, each time starting out

toward the bug only to turn back before reaching

it. This suggests that the sight of the bug was attractive to the wasp, but that the presence or

absence of some other cue (s) counteracted this

attraction. The wasp eventually flew away.

Gravid bugs probably change leaves from time to

time before laying, but T. bodkini wasps which

were waiting nearby did not seem able to follow

them. When a gravid bug and two female T. bodkini, which were found waiting at her side, were

placed in a large glass jar along with the branch

of C. odoratum on which they were found, the bug

moved periodically from one leaf to another, but

the wasps did not follow her as she moved. In one

typical case neither wasp moved until the bug was

1.5-2.5 cm away, and then they both walked in

apparently random directions rather than toward

the retreating bug. Nevertheless, within 30 minutes the bug was quiet again and both wasps were

waiting near her. The bug's only response to the

wasps in this situation was to antennate toward

them when they approached her. These observations suggest that the immobility of the bug is an

important cue for the wasp, and that once the bug

moves it is no longer attractive until it stops again.

EGG MASSES.—Female wasps of both species behaved as if they used the sight of female bugs to

locate egg masses as well as gravid females. Females

of P. semiflaviventris demonstrated this most dramatically. When a guarding female bug was displaced several centimeters to the side of her group
14

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 7.—Variations in numbers of wasps seen attacking bugs defending eggs

<4 days old in 6 T. catappa trees during one day

Time

P. semiflaviventris

7:00-9:00 AM ...

1:45-3:00 PM

9:00-9:30 PM

T. bodkini

7:00-9:00 AM

1:45-3:00 PM

9:00-9:30 PM

Number of wasps Number of bugs Total number of bugs

seen attacking being attacked seen guarding eggs

30

67

12

4

8

1

24

32

11

4

8

1

87

56

23

87

56

23

of eggs, P. semiflaviventris females which had

been nearby preparatory to attacking (Figure 10a)

would often ignore the undefended eggs and move

so as to realign themselves with the bug's new position, sometimes passing very near the now unguarded eggs (other times the wasps turned and

began to oviposit in the unguarded eggs or moved

away). On one occasion a female wasp was seen

attempting to oviposit (backing in with abdomen

extended) below an adult female bug which did

not have any eggs but nevertheless scraped actively

in defense against the wasp.

Female T. bodkini also behaved as if they used

the bug's presence to locate egg masses. On five different occasions I saw a female walking on a trunk

where there were large numbers of bugs and each

wasp turned to move toward motionless bugs (both

males and females), approached to within about 1

cm and paused for a moment. Then, sometimes

after moving away and approaching again from

another angle, the wasp moved on. The bugs usually remained quiet, but sometimes walked away or

gave small shudders, kicked, or waved an antenna

toward the wasp.

A further indication that females of both species

of wasps hunted defending bugs rather than their

eggs was that they were often seen attacking masses

of nearly mature or already hatched eggs which

were unsuitable for parasitization.

Females of P. semiflaviventris and perhaps also

T. bodkini hunt mainly by day (Table 7); the

numbers of P. semiflaviventris found in the morning and at night are both significantly lower than

the number found in the afternoon (p<0.01), but

the difference between morning and evening counts

is not significant. The T. bodkini numbers show

the same trends, but the differences are not significant (0.1>p>0.05). One possible explanation

for these data is that the wasps begin hunting in

the morning and tend to stay near an egg mass

and battle with the defending bug once one is

found, thus "piling up" around the egg masses as

the day progresses, and then many wasps leave egg

masses in the evening. Most of the P. semiflaviventris females seen near eggs in the evening appeared not to be attacking. None were backing in

toward the eggs with their abdomens extended and

some were facing partially away from the bug, a

position seldom seen during the day. Most had

their antennae quiet and directed toward the

substrate.

EXPERIMENTAL AND NATURAL ISOLATION OF EGG

MASSES IN TREES.—Repeated observations of walking female wasps (especially T. bodkini) suggested

that the wasps might walk while hunting their

hosts. This hypothesis was tested in two ways and

both types of evidence indicated that it was false,

that the wasps fly rather than walk as they hunt.

Young (<4 days old) egg masses (and the bugs

TABLE 8.—Lack of effect of experimental isolation

of egg masses from xoalking insects on parasitism

rates (rates from Cassia sp. are from three separate

experiments in the same tree using nearly equal

numbers of control and experimental egg masses in

each case; those from P. dulce are from three adjacent trees observed simultaneously)

Wasp species

T. bodkini

P. semiflaviventris

Number of egg masses .

Cassia sp.

Isolated

18%

44%

51

Control

19%

45%

89

P. dulce

Isolated

12%

2%

30

Control

13%

1%

29
NUMBER 205 15

defending them) were experimentally isolated from

walking wasps in both Cassia sp. and P. dulce trees

by coating a small area at the base of the branchlet

bearing the leaf with the egg mass (see arrows in

Figure 2) with Tack-Trap. The eggs were collected about a week later and the parasitism rates

were determined. Parasitism in isolated groups did

not differ from control rates in other groups of the

same age from the same trees (Table 8).

Cassia sp. branchlets had pinnately arranged

leaves (Figure 2/), and egg masses on leaves near

the tips were thus naturally more isolated from the

bases of the branchlets (where a wasp hunting on

foot would presumably first arrive). Again the

degree of isolation of the egg mass did not affect

the parasitism rate. Of 56 masses which had less

than the median number of T. bodkini for the

tree where they were found, 25 were in the basal

half of the branchlet and 31 in the distal half; corresponding numbers for P. semiflaviventris were

29 and 36 and neither differed significantly from

the totals of 57 masses in the basal half and 75 in

the distal half. Nor was there any correlation with

the absolute distance from the base of the branchlet: of 58 masses with more than the median number of T. bodkini, 29 were more than four leaves

from the base and 29 were on the basal four

leaves; corresponding figures for P. semiflaviventris

were 38 and 26 (total of 57 of 129 masses more

than four leaves from the base).

MOVEMENTS BETWEEN TREES.—The possibility

that wasps tended to stay in the trees where they

emerged was tested by experimentally removing all

or nearly all wasps before they emerged in alternate T. catappa trees growing in a row along the

side of a small park (distances between the edges

of adjacent trees ranged from 0.9 to 3.1 m). In

four experimental trees I made biweekly collections of all or nearly all egg masses after they were

more than approximately 5 days old (i.e., were no

longer susceptible to further parasitism, but before the wasps emerged from parasitized eggs).

Parasitism rates in these trees were monitored by

examining collected eggs (parasitized eggs were distinguished by the membranes deposited next to the

chorion by the wasp larvae; see Figure 11), while

the rates in five control trees were determined from

weekly collections of eggs from which both bugs

and wasps had already emerged. The numbers of

wasps emerging on the experimental trees were

thus reduced drastically, while the control populations were undisturbed.

The results of this treatment were measured in

two ways. The parasitism rates of the eggs laid each

week in both experimental and control trees were

determined, taking into account that eggs laid in a

given week were collected about two weeks sooner

on experimental trees than on control trees. Figure 8 shows how the rates changed: by the last two

weeks of the experiment the difference between the

control and experimental rates for P. semiflaviventris was significant (p< 0.002, Willcoxon Sum of

Ranks Test), but T. bodkini rates were unchanged.

The fact that P. semiflaviventris rates declined

gradually over several weeks rather than dropping

more suddenly suggests that the wasps live an appreciable length of time and only slowly died out

of or migrated away from the experimental trees.

The same lack of movement by P. semiflaviventris was found by using a second technique—

counting the numbers of wasps seen attacking bugs

P.SEMIFLAVIVENTR1S (control)

P.SEMIFLAVIVENTRIS(exDerimental)

,,,,,,, T.BODKINI (control)

T. BODKIN I (experimental)

60

40

20

1 2 3 4 5 6

WEEK NUMBER

FIGURE 8.—Effect that removal of wasps from T. catappa

trees before they emerged had on the parasitism rates in

those trees.
16

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

(12)

(39)

(8)

(28) (15)

(M)

(65)

(19)

(42)

(26)

(30)

I 1-2 2-3 3-4 4-5 5-6

NUMBER OF DAYS ON TREE

BEFORE COLLECTED

6 AND ALREADY

HATCHED

FIGURE 9.—Rates of T. bodkini parasitism in a P. dulce tree

as a function of the length of exposure to wasps.

defending young (< about 4 days old) eggs. During two weeks of biweekly visits, 84 of 113 masses

on the control trees had P. semiflaviventris females nearby, while only 14 of 78 masses on the

experimental trees had wasps near them (p<0.01;

the eggs observed were those represented in weeks

4 and 5 in Figure 8). The sample of T. bodkini

was not large enough to analyze.

Both types of data show that P. semiflaviventris

females tend to stay and hunt in the tree where

they emerge, thus forming a "viscous" population;

the less conclusive data on T. bodkini suggest that

females of this species do not. One further observation supported both of these ideas. In one P. dulce

tree which I searched weekly, the number of new

egg masses fell from 72 to 5 in a span of three

weeks. The rate of parasitism of these masses by

P. semiflaviventris rose from 13% to 30% (the

rates for the last two weeks differed from those for

the week before the population of eggs began to

decline; p<0.01, Willcoxon Sum of Rank Test).

There was no change, however, in T. bodkini rates

during this period; 15% of the eggs were parasitized at the beginning and 15% at the end. These

data are in accord with the results of experimental

removal of wasps since an increase in parasitism

rates would be expected if the wasps tended to

stay in the tree where they emerged; the relatively

large numbers of wasps produced from the numerous previous egg masses would concentrate their

hunting on a smaller number of egg masses and

thus raise the average rate of parasitism.

CHANGES IN PARASITISM RATES WITH LENGTH OF

EXPOSURE TO WASPS.—It was possible to deduce

how much time had passed since a given egg mass

was laid by noting how long it took the eggs to

hatch in captivity, and parasitism rates could thus

be determined for eggs which had been exposed to

wasps for varying lengths of time. Figure 9 presents

the results of two such studies of T. bodkini parasitism in the same P. dulce tree at different times.

TABLE 9.—Parasitism rates on different species of tree (egg masses on leaves only,

from trees with >10 groups of eggs, and from Cali unless specified)

Wasp species

T. bodkini

Range

Average

Median

P. semiflaviventris

Range

Average

Median

Number of trees

Number of samples

Number of eggs

Cassia sp. Canagium

P. dulce Cali Bucaramanga odoratum T. catappa

4%-26% l%-29% 0% H%-27% 0%-12%

15.8% 12.6% 0% 17% 5.6%

15% 13% 0% 21% 6%

0%-40% 2%-61% 39%-67% 57%-85%

7.9% 41.3% 71.6% 54% 70.9%

4% 43% 46% 70%

18 10 24 8 21

48 25 24 8 22

35,099 18,411 5503 3215 26,302
NUMBER 205 17

TABLE 10.—Parasitism rates on branches and leaves of the same trees (trees with

>10 groups on both leaves and branches in the case of P. dulce, and >5 in the

case of T. catappa)

Wasp species

T. bodkini

Range

Average

Median

P. semiflaviventris

Range

Average

Median

Number of trees ....

Number of samples

Number of eggs ...

P. dulce T. catappa

Branches

31%-43%

34.9%

34%

0%-16%

6.5%

3%

8

11

7463

Leaves

15%-28%

20.6%

24%

0%-37%

9.9%

4 %

13.313

Branches

0%-17%

9.1%

7%

2%-62%

373%

37%

15

27

3845

Leaves

0%-25%

4.6%

7%

40%-85%

71.6%

72%

15.735

Although the final rates of parasitism were quite

different, in both cases parasitism was essentially

complete two days after the eggs were laid.

VARIATION IN DIFFERENT TREE SPECIES.—Table 9

shows that the rates of parasitism by P. semiflaviventris varied within different ranges in different

species of tree. It may be significant that higher P.

semiflaviventris rates occurred in trees with larger

leaves (see Figure 2). Cocoa, which has large leaves,

also apparently has high P. semiflaviventris rates

(Callan, 1944a; Sepulveda, 1955). Parasitism rates

by T. bodkini showed less correlation with tree

species, although rates on T. catappa were significantly lower than those on P. dulce (p<0.01,

Willcoxon Sum of Ranks Test). Competition between the two wasp species probably influenced

the rates on different tree species to some extent.

VARIATION AT DIFFERENT SITES IN GIVEN TREES.—

Branches vs. Leaves: The parasitism rates by both

species of wasp differed for both P. dulce and T.

catappa according to whether the bug eggs were

on leaves or branches, as shown in Table 10. The

T. bodkini rate was higher for egg masses on

branches than for those on leaves in both species of

trees, while the P. semiflaviventris rate was consistently lower.

Suckers vs. Trees: The rates of parasitism by T.

bodkini were consistently lower in groups of eggs

on the leaves of suckers at the bases of P. dulce

trees (Figure 2a) than on the leaves of the same

trees. When the numbers of eggs parasitized in

groups of 26-28 eggs found on suckers around four

trees were compared with the median numbers of

eggs parasitized by T. bodkini on the leaves of each

tree and its suckers, 18 of the sucker masses were

lower than the medians for their respective trees

and 3 were higher (p<0.01). In another sample

from one of these trees, the parasitism of masses

from the suckers (N = 14) was also lower than that

of masses from the tree (N = 21) (p<0.01, Willcoxon Sum of Ranks Test).

OVIPOSITION

BEHAVIOR.—Oviposition behavior actually forms

a part of the attack behavior described below, but

is considered separately here in order to simplify the

descriptions. It should be kept in mind that some

of the "ovipositions" I saw may have been only

probing behavior with the abdomen and/or the

ovipositor which did not result in eggs being laid.

At least some "ovipositions," however, did result

in the production of wasps from otherwise virgin

T. bodkini: When recently laid A. tripterus eggs

were placed in a jar with 2-day-old fertilized female

T. bodkini wasps that had emerged in captivity,

the wasps showed no signs of being attracted to the

eggs, several times passing very close to them without touching them. But as soon as a wasp did encounter eggs, she began to oviposit into them. Both

these wasps and others found attacking egg masses

in nature and induced to oviposit in undefended

groups showed rather consistent behavior. The
18 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 11.—Frequency of super parasitism by wasps attacking undefended eggs

Wasp species

T. bodkini

Observed

Random

P. semiflaviventris

Observed

Random

Number of ovipositions in each egg Number of Number of

3 or more egg masses female wasps

273

20'.)

131

132

185

138

62

65

16

33

22

19

17

wasp began by walking over the group, antennating

successive eggs. After pausing and antennating one

egg for a second or more, she made a brisk 180°

turn and placed the tip of her abdomen on the

egg, then moved forward until the tip was against

the near edge of this egg (or occasionally against

an adjacent one). She stayed motionless, crouching

low with her antennae folded down (Figure 1) for

10—30 seconds. Wasps in this position usually did

not respond to being pushed or nudged. Then, before leaving, the wasp nearly always wiped the tip

of her abdomen from side to side, one or more

times, across the surface of the egg.

This "marking" behavior was similar to that

observed by F. Wilson (1901) in Asolcus basalis

and appeared to have the same function—to prevent multiple ovipositions in single eggs. The

number of times females which were allowed to

parasitize unguarded masses oviposited into each

egg in the mass was determined for 17 masses. The

numbers of eggs which would have been attacked

0, 1, 2, or 3 and more times if the wasps had been

choosing host eggs randomly was calculated using

the formula in Wilson's paper (the number of ovipositions per group varied, so these numbers were

calculated for each egg mass and then summed)

and compared with the observed numbers of ovipositions (Table 11). The wasps reoviposited in

FIGURE 10.—Female P. semiflaviventris wasps attacking bugs defending their eggs: a, wasp

looking in toward bug; b, wasp backing in with her abdomen extended; c, wasp ovipositing into

egg in exterior row of mass (arrow); d, wasp ovipositing into egg in interior of mass (arrow).
NUMBER 205 19

eggs less often than if they had chosen eggs at random, thus indicating that the marking did prevent

multiple ovipositions.

Usually females laid several eggs at first, with

only very short pauses between ovipositions, but

gradually they spent more and more time walking

over the mass antennating eggs between ovipositions and finally, after less than an hour, left. In

most cases the number of eggs laid in the first burst

seemed to depend on the age of the bug eggs,

newer groups being more thoroughly attacked.

The wasp usually left before parasitizing all the

eggs in a mass and usually it flew rather than

walked away.

On several occasions I saw more than one female

T. bodkini waiting near a gravid bug or attacking

a single egg mass, but in no case was there any

sign of aggression between them. In one case in

which both a T. bodkini and a P. semiflaviventris

were attacking an undefended mass, however, the

T. bodkini moved toward the other female several

times and appeared to be responsible for her leaving the eggs.

P. semiflaviventris: It was more difficult to induce P. semiflaviventris to oviposit. Females which

emerged in captivity did not attack groups either

with or without bugs defending them. Those

found attacking masses in nature would only seldom lay into undefended eggs. In order to conduct

studies of development rate and interspecific competition within the egg, it was necessary to glue

eggs with known histories (known virgin eggs, for

example) next to a bug whose eggs were being

attacked by a P. semiflaviventris female. By pushing the bug over onto the other group (which she

then defended), the wasp's attention could be

drawn to them and she would oviposit in them.

Oviposition by P. semiflaviventris differed from

that of T. bodkini in a number of respects. Oviposition lasted for only approximately four seconds

and was always performed with the abdomen extended (Figure 10c). The female did not climb

onto the egg mass, staying on the leaf instead. She

also failed to antennate eggs before laying in them,

moving directly from one to the next with her extended abdomen. Marking behavior was never

performed. Often a wasp laid a series of five to ten

eggs, backing along the base of the egg mass and

parasitizing both edge and internal eggs; to reach

the latter, she inserted her abdomen between the

bases of edge eggs (Figure \0d). The wasp's extended abdomen was very flexible; when she came

to a corner of the egg mass, she curved the tip

around the corner and parasitized the first edge egg

on the next side before bringing her body around

the corner.

Counts of the numbers of eggs reparasitized in

eight different masses confirmed that P. semiflaviventris females do not differentiate eggs which they

have already parasitized from others (Table 11).

Although I observed more than one P. semiflaviventris female attacking a single egg mass simultaneously many times, there was never any sign of

aggression between them.

SUCCESS.—The results of ovipositions by both

wasp species are summarized in Table 12, which

shows that each species can displace the other and

that the winner in any given case is not predictable.

Some of the eggs found in nature may have been

previously parasitized, but 15 of the eggs into

TABLE 12.—Results of ovipositions by wasps in bug eggs found in nature

Age of eggs

Eggs <4 days old oviposited

in by—

T. bodkini

P. semiflaviventris

Both species

Eggs >4 days old oviposited

in by—

T. bodkini

P. semiflaviventris

Species

A. tripterus

19%

3 3%

12%

90%

97%

that emerged

T. bodkini

65%

o%

24%

0%

0%

from the egg

P. semiflaviventris

4"'

5 3%

52%

0%

0%

Fail to

develop

11%

15%

12%

10%

3%

Number

of eggs

200

40

42

34

27
20 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

which both species oviposited were known to have

been virgin except for the observed ovipositions;

these eggs produced six T. bodkini and nine P.

semiflaviventris. Even within a given mass of virgin eggs where all ovipositions by each species

occurred at the same time, some eggs produced

one species of wasp and others the other. The rates

of parasitism for doubly parasitized eggs differ

from those for singly parasitized eggs (p<0.01 for

both species), suggesting some form of competition

between the larvae inside the bug egg, with the

winner eating the loser as in other scelionids (e.g.,

Kamal, 1937; Pickford, 1964). Older bug eggs

were much less susceptible to parasitism (p<0.05

for both species). Other scelionids such as Telenomns gifuensis also parasitize younger pentatomid

eggs more successfully than older ones (Hikada,

1958).

It was clear, in addition, although no measurements were made, that the time between T. bodkini ovipositions (i.e., the time the wasp spent investigating eggs) was much greater on masses of

older eggs than on new ones. Both species were

found attacking mostly newer masses in nature.

The first egg laid by T. bodkini females tended

to be a male. Of 24 masses in which only one egg

was parasitized by this species, 20 produced males

and 4 females. Assuming the frequency of males in

Table 14 and a random assignment of sex to the

first egg, these numbers should be 6 and 18; the

difference is significant (p<0.01).

STAGES IN THE EGGS OF A. triptems

Table 13 shows the developmental times of both

wasp species. The membranes referred to were deposited against the chorion of the bug egg. The

membranes of the two species were distinct; that of

P. semiflaviventris was solid black on the bottom

and sides (Figure lla), while that of T. bodkini

was clear on the bottom and had alternating black

and transparent circular bands like barrel hoops

along the sides (Figure lib). The membranes stayed

intact after the wasps left the eggs, and rates of

parasitism by both wasp species could thus be

determined by examining empty eggs. Although

the most common coloration of the membranes was

black, both species rarely (especially in T. catappa

trees) produced lighter, more brownish membranes, which were occasionally only slightly

clouded. Even in these cases, however, species

TABLE 13.—Developmental times of T. bodkini and

P. semiflaviventris in days (measured from moment

of oviposition by wasp; eggs checked at least once

every 12 hours)

Stage T. bodkini P. semiflaviventris

Larva with membrane

White pupa

Red-eyed pupa

Black pupa

Emergence

3.5- 6.6

5- 6.8

6.1- 8.2

75-11.8

10-12.3

3.8- 7.9

5.8- 8.9

6.8-10.2

7.9-12.7

9.7-13.4

a

FIGURE 11.—Membranes left in bug eggs by: a, P. semiflaviventris; b, T. bodkini.
NUMBER 205 21

TABLE 14.—Sexes of wasps raised from A. tripterus eggs collected in the field

(28 of the 49 groups were parasitized by both species of wasp; averages calculated

on the basis of the number of masses parasitized by a given species)

Average number of males/mass

Average number of females/mass

Ratio of male:female

Maximum number of females/mass

Number of masses with more than 1 male

Number of masses with females but no males

Range of number of wasps/mass

Total number of masses

Total number of wasps

T.bodkini P.semiflaviventris

identity could nearly always be distinguished by

the circular stripes and the paler bottoms of T.

bodkini membranes. The function of the membranes and the reason for the variations in their

color are not known. Species of the scelionid genus

Asolcus also produce characteristic membranes

(Cumber, 1964).

The wasp larvae did not defecate until they had

finished feeding, and then deposited a slab of feces

along one side of the egg. In all cases the feces

were placed ventrally with respect to the wasp pupa

and adult, with the wasp nearly always facing the

cap of the egg. In only one of several thousand

eggs examined was there more than one wasp in a

single bug egg.

EMERGENCE FROM THE EGG

Males developed in less time than females and

the first wasp to emerge from the egg mass was a

male in each of 40 cases for T. bodkini and in 44

of 45 for P. semiflaviventris. The wasps emerged

by cutting away the egg cap with their mandibles.

They sometimes opened the egg in less than an

hour, but other times paused for up to several hours

before completing the task. The two species differed

slightly in the form of the cut made in the cap:

T. bodkini cut mostly along the edge of the cap,

while P. semiflaviventris tended to start in the center and cut in ever-widening arcs until a sufficiently

large hole was produced. P. semiflaviventris tended

to emerge more in the night and early morning

than the day; of 214 wasps which emerged in captivity over a period of a week, 149 emerged between

7 PM and 9 AM (p<0.01).

1.5

4.8

1:3.2

22

13

3

1-25

39

245

SEX

3.1

13.3

1:4.3

23

19

6

1-25

38

527

RATIOS

Males of both species were less common than

females, but nearly every egg mass parasitized produced at least one male wasp (Table 14), perhaps

due to tendencies to lay male eggs first. Only

rarely were males as common as females in a given

mass of eggs (once in each species for the groups in

Table 14), indicating, since unfertilized hymenopteran eggs generally produced males (e.g., E. O.

Wilson, 1971), that either unfertilized females were

rare or that they do not oviposit.

MALE BEHAVIOR

FIGHTS.—Males of both wasp species fought for

possession of egg masses. Unfortunately, they were

usually disturbed when the leaf which the egg mass

was on was placed under a microscope, so the descriptions below are only fragmentary.

Males stayed on the tops or at the sides of the

egg masses from which they had emerged, walking

over the eggs and grooming periodically, but generally remaining quiet. They could distinguish

eggs from other objects, as they almost always

climbed onto eggs and stayed on them when introduced into vials containing several egg masses on

leaves. In this situation they mounted and stayed

on completely hatched masses as well as on ones

about to produce female wasps.

I witnessed both inter- and intraspecific aggressive encounters, and the frequency with which more

than one male emerged from a given egg mass

(Table 14) indicates that both types of fights are

common in Cali.

The males' weapons were their mandibles and,
22 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

although fights did not usually result in injuries,

they were capable of biting off the antennae and

legs of opponents. Aggressive males often opened

their mandibles as they looked toward other males

and, in at least some cases, it was possible to predict the outcome of an encounter by observing

which male opened his mandibles more. Less aggressive males were not as active as others, often

keeping their antennae lowered and still, and

crouching low on the egg mass or next to it.

When one male was much more aggressive than

the other, interactions did not usually involve

physical contact, the loser running off the egg mass

as the other moved toward him. In these cases the

more aggressive wasp did not pursue the other more

than 1-2 cm from the egg mass. In more evenly

matched pairs, the second wasp turned and lowered

his head toward his opponent's rush or even moved

toward him; the two wasps locked mandibles and

apparently struggled, moving from side to side and

backward and forward, with one male finally appearing to dominate, pushing the other backward

off the egg mass.

MATING.—Mating probably normally occurs the

moment the female leaves the egg, and I saw more

than ten matings of this type in each species. As the

female began to climb out of the egg after cutting

open the top, the male eased himself onto the top

of her thorax. He immediately began to antennate

the front of her head and her antennae, and she

responded by folding her antennae ventrally and

staying motionless. Then the male moved backward and bent his abdomen slightly downward to

make contact with the tip of her abdomen. Often

the male moved forward one or more times to

reantennate the female's head before achieving

genital coupling. Both animals usually remained

nearly motionless during the ten seconds while they

were coupled and then the male dismounted.

There were two small differences in the mating

behavior of the two species. Occasionally P. semiflaviventris males rubbed their hind legs briskly

along the dorsal and lateral surfaces of the female's abdomen while antennating her head. Female T. bodkini nearly always walked several

centimeters away from the egg mass immediately

after mating, while P. semiftaviventris females did

not move away.

Males of T. bodkini copulated with virgin females in plastic vials, and one male mated with

four females during his first minute in such a situation. These matings were slightly different and

suggest that mating away from the egg mass is possible in nature. The female remained nearly motionless as the male approached, antennated her

briefly, and mounted her. In one case, the female

moved away, and the male approached again, more

slowly and with more antennation before mounting. Several times a female began to walk as the

male mounted on her attempted genital contact,

and he responded by moving forward to antennate

her antennae until she folded them and became

quiet again, then moved back to attempt genital

contact.

Males could copulate several times and I saw

one T. bodkini male mate with 12 females, and

one P. semiftaviventris male mate with 7 females.

The females mated only once and T. bodkini females, kept in a vial where they could not escape

from a male, avoided additional contacts by moving

away when another wasp came near. Males in this

situation approached both virgins and nonvirgins,

but usually did not attempt to follow wasps which

moved away. I saw one male P. semiftaviventris

mount immobile nonvirgins at the edge of an egg

mass three times; in each case the female stayed

motionless and the male dismounted without attempting to copulate.

I also saw two P. semiftaviventris females emerge

from an egg mass patrolled by a T. bodkini male.

In both cases the male antennated the female as

she emerged, but did not mount her. In one case

the male did not allow the female to stay near the

edge of the egg mass, chasing her away. In groups

collected in nature while the wasps were emerging,

there was only a slight, insignificant tendency

(0.25<p<0.1) for fewer female P. semiftaviventris

(per empty egg parasitized by P. semiftaviventris)

to cluster near masses patrolled by T. bodkini

males (N = 13) than near other groups (N=29),

indicating that such behavior by T. bodkini males

is far from universal. Cumber (1964) found that

males of two species of Asolcus would mount females of the other species, but in neither case was

fertilization accomplished.

CLUSTERS OF FEMALES

Females of both species stayed near the egg mass

for several hours after emerging and mating, al-
NUMBER 205

though they readily walked and flew away when

disturbed. Female T. bodkini were always dispersed, each several centimeters from the egg mass;

on P. dulce trees they were usually each on a different leaf near the leaf with the egg mass. The

avoidance of other wasps by recently mated females

is probably responsible for this pattern. Females of

P. semiflaviventris, in contrast, usually stayed in

contact with the base of the egg mass, each one remaining immobile amidst the bug nymphs as the

female bug stood guard over them all.

As noted above, female bugs guarding nymphs

scraped less often in response to artificial stimuli

than those over eggs (Table 6). I never saw a female bug drive off either female or male wasps

which had emerged from her egg mass. Bugs

guarding masses from which wasps were emerging

gave no response to immobile wasps and only

waved their antennae toward moving wasps. The

bugs often raised themselves off the surface of the

egg mass when touched ventrally by a wasp walking over the eggs. This response probably serves to

give moulting first instar nymphs room to emerge

from their old cuticles after they climb onto the

eggs and hook their claws there (females with

moulting nymphs under them were seen in this

position several times), but it also facilitated the

movements of male wasps over the egg mass.

Interactions between Wasps and Bugs

WASPS VS. BUGS GUARDING EGGS

DIRECT OBSERVATIONS.—I observed parts of more

than 20 interactions between female wasps of each

species and bugs guarding eggs. Behavior of individual wasps varied somewhat, but the two species

were quite distinct.

T. bodkini: Female T. bodkini waited near bugs,

staying out of range of the bug's antennae and

facing in toward the eggs. One common tactic was

to rush to the egg mass and turn quickly to lay into

an egg in the edge of the mass. I had the strong

impression that wasps tended to make such rushes

just after I disturbed the bug by seizing the leaf

with my hand; on several such occasions the bug,

apparently distracted momentarily, failed to respond to the wasp. Another tactic was to wait

several minutes on the other side of the leaf, then

come over the edge and quickly rush to the egg

mass. Usually the bug responded to rushes by

scraping, kicking, waving her antennae, and occasionally shuddering as described above. Often

this behavior served to drive the wasp out of range

of the bug's antennae and bugs occasionally succeeded in knocking wasps completely away from

the egg mass with a kick.

On several occasions a wasp appeared to hurry

her oviposition in a way never seen in attacks on

undefended eggs, omitting antennal inspection of

the bug egg, and simply moving her abdomen

directly from one egg to the next.

The bugs were unable to effectively defend the

rear edge of the egg mass, i.e., the edge under the

bug's abdomen (Figure 1, arrow in Figure 5a).

They apparently could not bend their hind legs so

as to scrape along that edge, and thus a wasp which

was able to insinuate herself into this area was usually able to parasitize several eggs along the back

row with little interference from the guarding bug.

After ovipositing in the back row, T. bodkini females often attempted to move stealthily along the

lateral edge of the group. Usually, however, these

attempts were unsuccessful, as the bug responded

by kicking at the wasp with a hind leg or scraping.

It is interesting that even when a bug gave clear

indications (kicks, shudders, etc.) that she sensed

that there was a wasp at the rear edge of her egg

mass, she never turned to assume a new orientation over the eggs. That is, the bugs never turned

so as to bring their front legs to bear on the unprotected back side of the mass. To do so of course

would result in leaving another side of the mass

open to attack, and the lack of turning implies a

sacrifice of the back eggs in order to insure the

relative safety of the others. This failure to turn

was probably an important factor in keeping T.

bodkini rates at relatively low levels in some

situations.

P. semiflaviventris: Attacks by P. semiflaviventris females were quite different. The general

tactic of this species was to move to about a body

length from the edge of the egg mass (generally

within range of the bug's antennae), quickly turn

180°, and then extend the abdomen to about

twice its normal length and back in slowly toward

the mass, attempting to contact an egg with the tip

of her abdomen (Figures 1, 106, 10c). Upon reaching the mass, the wasp laid in the first bug egg she

touched, then moved to lay in an adjacent egg in
24 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

the edge of the mass or to thread her abdomen between two edge eggs and parasitize an interior egg

(Figure lOd). Wasps attacked from all sides of the

bug, not just the rear. This species also seemed to

attack especially often just after I disturbed the

bug.

DEDUCTIONS FROM PATTERNS OF PARASITISM WITHIN EGG MASSES AND WITHIN TREES.—The patterns of

parasitism in empty (hatched) egg masses with the

common "compact" shape (Figure 12) confirmed

the direct behavioral observations of wasp-bug

interactions. Since defending female bugs nearly

always positioned themselves over such groups in a

standard way, detailed analyses of the directions

from which the wasps attacked could be made.

For instance, the eggs in position C in Figure

126 formed the rear, more poorly protected edge

of the mass, and eggs in these positions were parasitized by T. bodkini approximately four times

more heavily than those in any other part of the

mass. Parasitism by P. semiflaviventris on the

other hand was not confined to the rear edge, but

was distributed on all sides of the group. The central eggs were seldom parasitized by either species.

The patterns of parasitism of these groups also

brought out several more subtle details of the

interactions between P. semiflaviventris and the

defending bugs. Excepting the back edge, edge

eggs (A, B, and D in Figure 126) were generally

more heavily attacked than eggs on the first interior row (E, F, and G, but not H—see below)

(p<0.05 excluding H). Since attacking wasps arrived first at edge eggs and only later at interior

eggs, the difference between the two positions

a

FIGURE 12.—Pattern of parasitism of "compact" egg masses: a, parasitism rate for each position

(hatched = T. bodkini, black = P. semiflaviventris, white = no parasitism); b, positions grouped

according to similarities in parasitism rates.
NUMBER 205 25

probably results from the bugs interrupting some

attacks by the wasps.

The two eggs farthest from any edge (J in Figure 12b) were least parasitized by P. semiflaviventris (p<0.01). Probably the wasps were unable

to extend their abdomens far enough to reach

these eggs. Eggs in position K were more heavily

parasitized than the central eggs (p<0.01), but less

heavily parasitized than other first row interior

eggs (E, F, G, and H) (p<0.01). The wasps were

probably capable of reaching these eggs with their

extended abdomens, but perhaps often failed to

curve them so as to reach this position.

Anterior lateral edge eggs (A) were less parasitized than posterior lateral edge eggs (B)

(p<0.05). This difference may result from the

bug's more consistent and efficient scraping along

the front edge of the egg mass with her front legs.

In addition, first row interior eggs at corners

(I, E, and H) were more heavily parasitized than

other first row interior eggs (F, G) (p<0.01). Such

corner eggs were probably more accessible to wasps;

for instance, a wasp could reach position E by

going between the bases of either A and D or A

and A, but would have access to F only between A

and B. The position with the highest rate of parasitism, H, had three access routes, in addition to

being accessible from the poorly guarded rear edge

of the mass.

The bugs were clearly less successful in defending

the eggs at the front and sides of their groups

against P. semiflaviventris than against T. bodkini, probably as a result of several factors. Female

P. semiflaviventris kept their bodies out of range

of the bug's scraping legs while ovipositing, exposing only the small tips of their extended abdomens. The bug thus had a smaller target to hit,

and one which offered much less purchase for its

legs. The tip of the wasp's abdomen may have

been difficult for the bug to see (it was darker than

the rest, and I had trouble seeing it), and this,

combined with the ability of the female P. semiflaviventris to lay eggs very quickly, also meant

that just a moment's lack of vigilance could cost

the bug one or more eggs. Often bugs responded to

the presence of an attacking P. semiflaviventris

by continually scraping along the edge of the egg

mass, even when the wasp was not near enough to

oviposit. Once a wasp succeeded in getting her extended abdomen between two edge eggs and was

TBODKINI ON £ DJiLCE

20

io

-TREES WITH TOTAL RATE OHO.0%

TREES WITH TOTAL RATE 10.1-20.0%

—•—TREES WITH TOTAL RATE 20.1-30.0%

5 10 15 20 25

Number of eggs parasitized in groups with 28 eggs

E.SEMIFLAVIVENTRIS 0N £ DULCE

20

10

-TREES WITH TOTAL RATE 0-10.0%

TREES WITH TOTAL RATE 10.1-20.0%

TREES WITH TOTAL RATE 20.1-30.0%

5 10 15 20 25

Number of eggs parasitized in groups with 28 eggs

T.BODKINI ON TREES WITH 10-20% PARASITISM

-P. DULCE

CASSIA SP

TCATAPPA

20

15

£ 10

I

S 10 15 20 25

Number of eggs parasitized in groups with 28 eggs

FK.URE 13.—Number of eggs parasitized/mass as a function of

the total parasitism rate of the tree.
26 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

ovipositing in an interior egg, she was well braced

by the eggs and not easily moved; on several occasions I saw a bug scrape right over a wasp in this

position without dislodging it.

Several additional details of bug-wasp interactions can be deduced from Figure 13, which

shows how the numbers of eggs parasitized in

masses of 28 eggs varied according to the total

parasitism rate in P. dulce trees. The total rate for

a tree is probably a fair indication of the density of

wasps which were searching for eggs there and thus

what is said below concerning total parasitism

rates probably also applies to the density of searching wasps in a tree.

In both wasp species the number of egg masses

missed declined as the total parasitism rate for the

tree rose (it should be kept in mind that my assumption that unparasitized egg masses were never

found by wasps was undoubtedly incorrect in some

cases in which the bug succeeded in repelling a

wasp before it laid a single egg; such interactions

may have been more common in the case of P.

semiflaviventris); at the same time, the number of

eggs parasitized per group rose for both species.

The curves for T. bodkini show strong peaks in

the region of five eggs, almost certainly due to the

fact that the back edges of egg masses, the usual

site of T. bodkini parasitism, usually consisted of

about five eggs; the curves for P. semiflaviventris

show no such tendency.

The low numbers of eggs per group parasitized

by P. semiflaviventris in trees with low total rates

are surprising, indicating that the defense of the

bugs against single attacks by P. semiflaviventris

was quite effective, perhaps more so than that

against single attacks by T. bodkini females. The

higher rates of parasitism which P. semiflaviventris

achieves on some trees would thus seem to be due

to multiple attacks, a conclusion supported by the

shift to the right of the P. semiflaviventris curves

in trees with higher total rates. The curves for T.

bodkini also move to the right, but more slowly,

probably because each subsequent female wasp

tends to attack the same five eggs in the rear edge

of the egg mass; P. semiflaviventris females, not

being so restricted, probably attacked more efficiently, reparasitizing eggs much less often.

It was not uncommon to see more than one female wasp attacking a single bug (up to 10 female

P. semiflaviventris were seen around a single bug

in T. catappa trees), and it seems possible that a

sort of "social facilitation" may occur in such situTABLE 15.—Patterns of parasitism of "compact" egg masses by P. semiflaviventris

in different species of tree (the numbers are the number of wasps from the given

position divided by the total number of wasps from eggs in that tree species not

counting those from position C; the positions are those indicated in Figure 126)

Position of egg P. dulce Cassia sp.

Canagium

odora turn

Cali Bucaramanga

T. catappa

A

B*

C

D

E

F

G

H»

I

J

K

Total wasps (not counting those

from position C)

Total number of egg masses

Total parasitism by T. bodkini

.20

.28

.23

.12

.08

.07

.08

.17

.06

.00

.03

208

87

.19

.22

.30

.16

.08

.05

.07

.16

.04

.01

.03

545

73

.22

.21

.23

.17

.08

.07

.08

.11

.0.")

.01

.03

1297

86

0%

.19

.22

.12

.15

.10

.07

.09

.11

.05

.00

.02

682

50

20%

.21

-21

.21

.16

.07

.09

.08

.11

.04

.01

.02

773

50

* Difference between P. dulce and T. catappa significant (p <.O5).
NUMBER 205 27

ations, with a given wasp's presence aiding other

attacking females by distracting the bug's attention.

EFFECT OF TREE SPECIES.—Battles between bugs

and P. semiftaviventris wasps for "compact" egg

masses were only slightly influenced by the species

of tree where they occurred. Since the rates of parasitism by T. bodkini differed in different tree species, the eggs at the back edges of the masses

(position C in Figure 12), where the great majority of T. bodkini parasitism occurred, were excluded from the analysis to avoid the effects of

interspecific competition. The percentage contribution from each position in the mass was calculated by placing the total parasitism in a given

position over the total number of P. semiflaviventris produced in compact masses in that particular tree species minus those from position C.

When the resulting patterns of parasitism in different tree species are compared as in Table 15, it

is clear that the general pattern was very similar.

Two differences are significant, however; the numbers of wasps from the two posterior lateral positions B and H are higher in P. dulce than in the

other trees. These differences may stem from a

wasp's being able to "surprise" the bug more easily

on small leaves by hiding for several minutes on

the other side of the leaf, then peeking over the

edge and quickly beginning to lay before the bug

sees her. This tactic might be more effective on

smaller leaves and in the rear part of the egg mass

where the bug's antennae and eyes would be less

likely to sense the wasp.

A detailed analysis of this type was not possible

in the case of the T. bodkini, but Figure 13c indicates that the tree species also failed to substantially modify the bug's interactions with this species

of wasp.

EFFECT OF SHAPE OF EGG MASS.—The effect of the

shape of an egg mass on its susceptibility to wasp

attack was determined by counting the numbers of

eggs parasitized in already vacated egg masses of

different shapes. Of 209 "compact" masses from 17

P. dulce trees, 124 had fewer than the median

number of T. bodkini wasps for masses of 28 eggs

in their respective trees (p<0.01, all trees had a

median parasitism greater than 0). Presumably

this reduction in parasitism resulted from the bugs

being better able to defend a smooth-sided, compact group than more irregular, strung-out masses

which had more "edge" eggs and more nooks to

protect attacking wasps from the bug's feet. The

form of the mass did not have a significant effect

on parasitism by P. semiflaviventris, however.

WASPS VS. OVIPOSITING BUGS

DIRECT OBSERVATIONS.—On three occasions I

found wasps (three T. bodkini and one P. semiftaviventris) parasitizing eggs while the bug was

still ovipositing. Except for kicking at the wasp

when it touched her, and perhaps moving farther

back over the eggs between ovipositions, none of

the bugs appeared to modify her oviposition behavior. The bugs were apparently unable to see the

wasps (which were always behind them) and in

two cases did not appear to sense the wasp's

presence during the early part of the interaction.

The kicks of the bugs at the wasps were essentially

blind, evidently directed mainly by contact. For

instance, on one occasion the bug moved forward

to lay an egg, then back, and kicked at the side

where she had touched a wasp just before moving

forward, but meanwhile the wasp had changed

sides; later the bug also kicked several times more

after she succeeded in kicking the wasp clear of the

eggs. Although the bugs finally kicked away all four

wasps before finishing ovipositing, their defensive

behavior was poorly organized; several times a bug

brushed or kicked an ovipositing wasp repeatedly

and, failing to dislodge it, ceased responding to it.

The behavior of the two species of wasp was

quite distinct in this situation. The P. semiflaviventris female behaved very much as if attacking a

group with a female bug in normal defensive position; she stayed on the leaf, backed in and probed

with her extended abdomen, and laid several eggs

in succession without inspecting them with her

antennae. She showed no response to the bug's

periodic moves forward and back over the egg

mass.

The behavior of the T. bodkini females differed

from both that of P. semiftaviventris and from that

of T. bodkini females attacking eggs with a bug in

normal guarding position. They stayed on the tops

rather than the sides of the eggs, and moved over

them antennating the cap of each. All three wasps

appeared to try to avoid touching the bug. Although each wasp spent the majority of her time

on the rearmost eggs (which were not covered by
28

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

the bug's abdomen), she did not oviposit there—

presumably because she had already parasitized

those eggs. When the bug moved forward to lay

another egg, the wasp also moved to the front part

of the group, inspected, and then turned and oviposited in an egg there. Since the bug laid an egg

in less time than it took T. bodkini to oviposit, the

bug sometimes moved back over the mass while a

wasp was still ovipositing. The bugs often sensed

the wasps at this time, and two of the wasps were

kicked clear of the eggs after being discovered at

this stage. In other cases, the wasp crouched low

and stayed very still under the bug's thorax, only

moving again when the bug moved forward to lay

its next egg. On one occasion I was sure that the

wasp marked the egg it had just parasitized, but on

several other occasions the marking was either very

limited or did not occur. One of the T. bodkini

females, kicked clear of the eggs by the bug, landed

on my hand holding the branch, and after cleaning

herself briefly, she flew away.

DEDUCTIONS FROM PATTERNS OF PARASITISM WITHIN

EGG MASSES.—Attacks made during the bug's oviposition may explain one additional pattern of

parasitism of the "compact" group form. The interior eggs in the anterior part of the mass (positions E, F, and I) were more heavily parasitized by

T. bodkini than those in the posterior part (G, J,

and K) (p<0.05, H is omitted since the high rate

of parasitism by P. semiflaviventris may influence

the T. bodkini rate). Interior eggs are probably

nearly inaccessible for T. bodkini once the bug

finishes ovipositing, and the eggs in the front part

of the group are laid first (e.g., Figure 4) and are

thus both exposed longer to attacks during oviposition and more poorly defended by the ovipositing bug.

Competition between Species of Wasps

WITHIN BUG EGGS

Comparisons of the patterns of P. semiflaviventris parasitism of "compact" groups from sites

with different rates of T. bodkini parasitism showed

(assuming that wasp-bug battles were essentially

the same in all sites—see Table 15) that the two

wasp species compete for eggs. The sites chosen for

their different T. bodkini parasitism rates were

these: Cassia sp. trees in Bucaramanga (T. bodkini

absent), P. dulce tree leaves in Cali (7\ bodkini

in moderate numbers), and P. dulce branches in

Cali (T. bodkini in high numbers). In all cases,

the parasitism by T. bodkini was concentrated in

the rear edge of the egg mass (position C in Figure

126). As shown in Table 16, parasitism by P. semiflaviventris in these rear eggs was significantly reduced where T. bodkini was more common.

The complementary comparison of patterns of

T. bodkini parasitism of "compact" masses in tree

species with high and low P. semiflaviventris rates

(T. catappa vs. P. dulce) showed no difference.

This probably results from the tendency noted

above for P. semiflaviventris to attack all sides of

the mass more or less equally, and in turn indicates

that the lower rates of P. semiflaviventris in rear

eggs on T. catappa and Cassia sp. (Figure 12a)

probably also resulted from competition with T.

bodkini.

In general, these data show conclusively that T.

TABLE 16.—Influence of interspecific competition on patterns of parasitism in

"compact" egg masses (all samples from Cali, Colombia, unless otherwise indicated)

Wasp species

P. semiflaviventris

Total parasitism rate

Percent of total that came from

position C

T. bodkini

Total parasitism rate

Rate of parasitism of eggs in

position C

Number of masses

••

 b Pairs differ significantly (p<.01)

Cassia sp. in T. catappa

Bucaramanga

P. dulce trees

Leaves Branches

70%

23%»

0%

0%

86

68%

17%-

9%

32%

50

11%

18%'

15%

54%

87

6%

9%'

41%

90%

69
NUMBER 205 29

bodkini sometimes displaces P. semiflavivenlris,

but not vice versa. The fact that neither species

dominated consistently over the other when both

laid into the same, otherwise virgin, eggs indicates,

however, that each species sometimes displaces the

other in nature.

FIGHTS BETWEEN MALES

Since the first wasps to emerge were nearly

always males, it was possible to deduce the results

of interspecific fights which had occurred in nature.

In masses from which at least one wasp of both

species had emerged, but from which some wasps of

both species had yet to emerge when the mass was

collected (all wasps and eggs were immediately

killed with alcohol to prevent additional emergals

before I counted them), the numbers of males of

both species were significantly reduced (p<0.01,

Table 17). Thus, males of each species significantly

displaced those of the other.

It appears that T. bodkini males may be superior fighters. The total rates for those egg masses

parasitized by both species of wasp were 18% T.

bodkini and 45% P. semiflavivenhis. Assuming

the sex ratio in Table 5, this would imply an average of 1.3 T. bodkini males/egg mass, and 2.4 P.

semiflaviventris males/egg mass. If the two species were equally good fighters, the results of the

20 cases in which only one male was left on the egg

mass (Table 17) would have been 7 T. bodkini

and 13 P. semiflaviventris, rather than the observed 11 and 9 (0.05<p<0.1).

In addition, P. semiflaviventris males were more

tolerant of the presence of conspecific males than

were T. bodkini males. Of 48 masses which had T.

bodkini males, only 4 had more than one, while

9 of 33 masses had more than one P. semiflaviventris male (p<0.05). On several occasions I saw

a P. semiflaviventris male avoid an attack by an

advancing conspecific by behaving like a female,

lowering his antennae to the substrate, and remaining motionless. Such "feigning" behavior

might be more effective in P. semiflaviventris

than in T. bodkini since P. semiflaviventris females usually stay clustered around egg masses

after emerging while T. bodkini females disperse.

There was no indication that males search out

egg masses other than those where they emerge, as

males were never found on masses from which at

least one wasp of that species had not emerged

(Table 17). Thus the exclusion of males of a given

species by the other eliminated the chances of females of that species to mate near that egg mass,

although the possibility remains that they mate

away from the eggs.

Experimental Removal of Bugs Guarding Eggs

Both the patterns of parasitism of egg masses by

the wasps and my repeated observations of bugs

repelling attacking wasps show that the defensive

behavior of the bugs lowers the number of eggs

parasitized by wasp females which have found the

egg mass. The observations reported in the sections

on the oviposition and hunting behavior of the

wasps suggest, however, that both species, and especially P. semiflaviventris, use the presence of guarding bugs to locate egg masses. The possibility thus

arises that the net influence of the guarding bug

on her eggs is negative—that her betrayal of their

position by standing over them outweighs the

benefits she confers on them with her defensive

behavior.

This possibility was tested by removing bugs

from some young egg masses (eggs without visible

embryonic eyes and thus less than about four days

old and still susceptible to parasitism), and leaving

TABLE 17.—Male wasps present on egg masses from which some but not all of

the xoasps had emerged

Species

Masses from which

had emerged

Masses from which

emerged

Masses from which

had emerged

emerged

males of both species

only T. bodkini had

only P. semiflaviventris

T. bodkini

11

30

0

P. semiflaviventris

<)

0

38

Both

8

0

0

None

o

1

3

Total

30

31

41
30 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 18.—Results of removal of female

A. tripterus guarding eggs on antless trees

Wasp species

Parasitism by T. bodkini

Control

Without female

Parasitism by P. semiflaviventris

Control

Without female

Number of control egg masses

Number of experimental egg masses

T. catappa Cassia sp.

4.5%

72%

64.4%

27

22

11.8%

18.1%

61.4%

46.4% *

23

39

• Experimental differs from control

coxon's "Sum of Ranks Test").

(p <.O5, using Willor less excluding ants from one T. catappa tree

and one Cassia sp. tree (twigs harboring Pseudomyrmex colonies were removed and a ring of

"Tack Trap" was laid around the trunk to prevent

other species from climbing into the tree) and

then repeating the experiment just described.

The results, presented in Table 18, show that the

net effect of the presence of the bugs is indeed

negative; it aids rather than hinders P. semiflaviventris and has no significant effect on T. bodkini.

Thus the bugs were "wasting their time" with respect to botli species of wasp, since they could have

been investing it in feeding to produce more eggs.

the females guarding other similar masses in the

same trees to serve as controls. Both test and control groups were identified by marks placed on adjacent leaves, and parasitism rates were determined

1-2 weeks later. The first test of this kind was conducted in two P. dulce trees, and a total of 48 test

and 41 control groups were recovered. Nearly all

of the experimental egg masses had vanished, however, when I recovered the leaves; in most cases

there was nothing but a greasy stain remaining on

the leaf. Of those few eggs recovered, not one produced a bug (most failed to develop). I observed

several species of insect feeding on undefended eggs

in this species of tree (Table 22), and they (perhaps especially the ants) were probably responsible

for the losses.

These results show that the defense of the bugs

against generalized egg predators is highly effective

and that the overall effect of their defense is undoubtedly positive. The possibility remained, however, that the effect of the bugs with respect to the

parasitic wasps is negative. This was tested by more

Other Factors Affecting A. tripterus Survival

UNHATCHED EGGS

Often some eggs in a mass failed to produce

either bugs or wasps. In some cases it was possible

to determine whether a young bug or a wasp had

died before emerging; in others, where it was not

possible, the egg was termed "undeveloped." Some

such eggs may have been infertile, while others

probably contained dead bug embryos or parasites

which died before discoloring the egg's vitelline

membrane. The frequencies of both failures of

identifiable bugs and wasps to emerge and of undeveloped eggs were correlated with the site of the

egg mass.

DIFFERENCES BETWEEN SPECIES OF TREE.—Eggs

laid during the same four-week period failed to develop more often on the leaves of a P. dulce tree

than on those of two nearby Cassia sp. trees (Table

19). The frequency of undeveloped eggs was also

correlated with tree species when data taken from

TABLE 19.—Frequencies of deaths within the bug eggs on leaves of different tree

species during the same four-week period (A) and during various periods (B)

Died within the egg (A)

Bugs

T. bodkini

P. semiflaviventris

"Undeveloped"

Frequencies of

"undeveloped" (B) ...

P. dulce

5.2% (N = 3262)

19.7% (N = 761)

42.2% (N =491)

6% (N=4777)

4.9% (35,099 eggs,

18 trees)

Cassia sp.

.9%(N = 1063)

.9%(N = 327)

2.7% (N= 1251)

1% (N=2778)

1.2% (18,411 eggs,

10 trees)

Canagium

odor alum

2.1% (3,215 eggs,

8 trees)

T. catappa

2.7% (26,302 eggs

21 trees)
NUMBER 205 31

various trees at different periods were compared

(Table 9). Hatching was consistently poorer on

P. dulce than any other species of tree, but the

level of significance cannot be determined since the

effects of parasitism on the production of "undeveloped" eggs are unknown.

DIFFERENCES BETWEEN LEAVES AND BRANCHES.—In

P. dulce trees, eggs laid on branches failed to develop more frequently than those on leaves. Thus,

in 12 samples from 14 trees, the frequency of

undeveloped eggs in branch egg masses was higher

than that in leaf masses in 13 cases, lower in 7, and

equal in 3 (p<0.1), and the total frequencies of

undeveloped eggs were 7.7% on branches (N =

7463) and 4.3% on the leaves (N = 13,313) of

these trees. Data from eggs on T. catappa trees did

not follow this pattern: 2.4% of the eggs on

branches (N = 3845) and 3.2% of those on leaves

(N = 15,735) of six trees were undeveloped. In

this case at least, the differences in developmental

failures are not due to differences in parasitism,

since the differences in parasitism rates on leaves

and branches of both tree species are similar

(Table 10).

LEAVES AND EGG MASSES THAT FELL FROM TREES

Substantial losses of entire egg masses were observed during weekly checks in several trees. Each

leaf which had an egg mass on it was marked (in

the case of P. dulce, an adjacent leaf was usually

marked), and the mass was collected after all bugs

and wasps had left it. In a span of five weeks, 290

leaves marked on three P. dulce trees were recovered; 31% had lost their eggs. On two Cassia

sp. trees, 16% of 145 marked leaves recovered during the same period were without eggs, indicating

that this type of egg loss was less common

(p<0.01) in Cassia sp.

These figures show a clear difference between

the tree species, but they are only approximations

of the true rates of loss because of several complications in taking the data: (1) marked leaves lacking eggs were probably less easily noticed, and

therefore underrepresented; (2) some egg masses

probably fell after the last bugs and wasps left, but

before I returned to search the tree—these losses

would be biologically insignificant; and (3) in the

case of P. dulce, the entire leaf rather than just the

egg mass may have fallen in some instances, leaving

only the adjacent marked leaf. (Repeated observations of new eggs on yellow, ready-to-fall leaves on

P. dulce and Cassia sp. trees [these trees continually shed a few scattered leaves] suggest that the

bugs did not distinguish such unsatisfactory sites

from others.) In balance, the data on losses by falling are probably somewhat below the true rates.

One other factor appeared to influence the loss

of egg masses by falling. In all four study species of

tree (and especially in P. dulce), a greater proportion of the older masses were on branches than

on leaves (Table 20; guarded masses differ from

unguarded masses, p<0.01) indicating that eggs

stayed stuck to branches longer before falling. Egg

masses also -appeared to stay glued to T. catappa

and Canagium odoratum leaves longer than to P.

dulce and Cassia sp. leaves, perhaps due to the

greater mechanical protection afforded by the

larger size of the leaves (Figure 2).

LOSSES OF FIRST INSTAR NYMPHS

VARIATION WITH SITE.—The numbers of first instar nymphs lost from groups at different sites were

determined in two ways. Direct measurements of

losses during the entire first instar period were determined in cases where the nymphs were found

just moulting to the second instar by comparing

TABLE 20.—Distribution of young and old egg masses on branches and leaves of

P. dulce trees (total of 18 samples from 16 trees; the ages of unguarded masses

were judged by the accumulations of dirt and fungus on them)

Ages of eggs

Guarded egg masses

Unguarded and empty.but relatively new eggs ..

Old, weathered, empty eggs

Percent of masses found on— Total number of

Branches Leaves egg masses

18 82 832

51 49 334

58 42 283
32

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

for each mass the numbers of eggs that had produced bugs with the numbers of nymphs present;

indirect measures were obtained by comparing the

numbers of hatched eggs and the numbers of first

instar nymphs and then (assuming that on the

average these nymphs were halfway through the

first instar and that the rate of loss throughout the

instar was uniform) multiplying the losses by 2.

The results of both types of counts are presented

in Table 21. It should be kept in mind that "losses"

did not necessarily mean deaths of nymphs, but

only that the nymphs were no longer near the egg

mass. The general low activity of the first instar

nymphs suggests that vanished nymphs had not

walked away, but had either fallen or been eaten.

Falling nymphs clung readily to surfaces which

they struck but, even so, the chances of survival of

the nymphs probably decreased greatly if they fell.

There were again significant differences in losses

from different species of tree and from different

sites within a given species (Table 21). The directly measured rate of loss from P. didce leaves

was not quite significantly greater than that from

Cassia sp. leaves (0.06>p>0.05), but was greater

than that from T. catappa leaves (p<0.05). The

indirectly measured rate of loss from branches was

greater (p<0.01) than that from leaves in P. dulce.

Although none of the differences between direct

and indirect measurements were large enough to

be significant, the consistent tendency for indirect

measurements to be larger suggests that the assumption that the rate of loss is constant throughout the instar may be incorrect and that younger

nymphs may be more frequently lost.

It seemed that mechanical agitation, which

would be greater on smaller-leafed trees such as

P. dulce, might be a principal cause of loss, but

comparisons of losses (determined indirectly) on

one P. dulce just after a period of heavy daily rains

and after periods of milder weather were not significantly different. First instar nymphs (as well as

older ones) were capable of clinging very strongly

to a substrate; when I tried to lift nymphs away

from their egg masses in captivity, some individuals

clung to and suspended groups of eggs and nymphs

corresponding to up to ol) times their own weight.

EXPERIMENTAL REMOVAL OF FEMALES GUARDING

FIRST INSTAR NYMPHS.—The effects of the bugs'

defense of first instar nymphs were measured by

removing defending females. The number of

nymphs was counted when the female was removed

and again two days later, and the total number

which would have been lost in seven days, the approximate duration of the first instar, was then

calculated by multiplying the observed losses by

3.5. The results of these observations (Table 21)

were that losses rose significantly (p<0.01, calculated on the basis of losses/day) on both P. dulce

and Cassia sp. when the female was removed. The

defense of the females, at least in P. dulce trees,

had the effect of especially reducing the likelihood

of losses of large numbers of nymphs from any

given group. Thus, of 39 unguarded groups on P.

dulce which lost nymphs during the 48-hour experimental period, 13 or 33% lost three or more

nymphs; of 108 control groups which had lost

nymphs (the average age of these nymphs was assumed to be 3.5 days), only 24% had lost three or

TABLE 21.—Losses of first instar A. tripterus nymphs from guarded and unguarded groups in 7 days at different sites (methods used in arriving at these

numbers are explained in the text; numbers in parentheses are number of egg

masses and total number of nymphs hatched)

Nymphs lost

Measured

Measured

Nymphs lost

groups

from defended groups

directly

indirectly

from undefended

P. dulce

Leaves

6.3%

(41,808)

11.7%

(245,4802)

44.1%

(51,1078)

Branches

32.2%

(56, 726)

Cassia sp.

Leaves

3.4%

(23,353)

9.3%

(146,1969)

40.2%

(22, 332)

T. catappa

Leaves Branches

2%

(10,99)

3.5% 8%

(79,665) (20,170)
NUMBER 205 33

more nymphs (p<0.05 after adjusting for different

time spans).

reared from both adults and large nymphs of A.

tripterus.

OTHER ENEMIES OF A. tripterus

The animals observed preying on various stages

of A. tripterus in nature and captivity are listed in

Table 22. In addition to the species listed, a fungus

of the genus Penicillium attacked and killed both

nymphs and adults in Palmira and Cali (Eberhard,

in press). A parasitic wasp, Hexacladia sp. n. (?)

(Encyrtidae) (det. C. M. Yoshimoto), was also

Discussion

HUNTING BEHAVIOR OF THE WASPS

Precise descriptions of the searching behavior of

parasitic insects are of great interest, but are rare

(DeBach and Hagen, 1964). Several aspects of the

hunting behavior of the two wasps are clear from

the data of this study.

TABLE 22.—Other enemies of A. tripterus (all attacks on eggs and first instar

nymphs occurred in unguarded groups unless otherwise noted; e=egg, n1=first

instar nymph, n = other nymphs, a=adults, P.d.=Pithecelobium dulce, C.sp.=

Cassia sp., T.c.= Terminalia catappa)

Predators

Hymenoptera

Sphecidae

Bicrytes variegata

Vespidae

Polistes canadensis

Fonnicidae

Ectatomma ruidum

Crematogaster sp

Pseudomyrmex spp

Campanotus sp

Hemiptera

Reduviidac

Zelus sp

Pentatomidae

Loxa sp

Podisus cloelia

Supputius sp. near typicus3

Coleoptera

Coccinellidae

Olla abdominalis Say (?)

Curinus colombianus Chapin

Neuroptera

Chrysopidae (1 species)

Araneae

Theridiidae

Achaearanea tesselata*

Anelosimus sp

Salticidae

Species 1

Species 2

Stage (s) of A. tripterus attacked Trees in which

In captivity In nature enemy was found

n P.d., Csp.

n

1

 P.d., Csp.

e P.d., Csp., Tx.

e P.d., Tx.

e Tx.

e P.d.

«„ n P.d., Tx.

e P.d.

e,nlTn iV.n.a P.d.

e,n1(n e'.n^.a P.d., Tx.

e Pd.

e P.d., Csp.

cnj P.d., Csp., Tx.

n,a P.d., Csp., T.c.

n* P.d.

n Tx.

a

1

 Tx.

1

 Recently moulted.

'Female A. tripterus present.

3

 Also preys on adult Phanuropsis semiflaviventris in nature.

4

 Also preys on Bicyrtes variegata in nature.
34 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Females of P. semiflaviventris, but not T. bodkini, tend to stay and hunt in the tree where they

emerge; experimental predation on unemerged

wasps in given trees significantly reduced the parasitism by P. semiftaviventris, but not T. bodkini.

Both wasps almost certainly use the presence of the

defending female bugs to locate host eggs, and

their responses to male and dead bugs suggest that

the location and immobility of the bug are important. Both wasps hunt their host visually, and P.

semiflaviventris hunts during the day.

Both species seem to be primarily aerial hunters.

The lack of correlation between the relative isolation (both natural and experimental) of the leaf

with the eggs and the parasitism rates on the pinnate leaves of Cassia sp. trees imply that most

searching is not carried out on foot. A further, indirect indication that the wasps find bug eggs from

the air is the tendency of the bugs to face the leaf

tip rather than its base while guarding their eggs.

It is not easy to reconcile the tendency of the

wasps to hunt in flight with the tendency of P.

semiflaviventris to stay in the trees where they

emerge. The wasps are very small, and relatively

weak fliers, so that even moderate winds probably

tend to wash them out of trees where they are

flying. The wind in Cali is usually very weak in the

mornings, but is often moderate to strong in the

afternoons, sometimes reaching 15-20 kmph as

early as 2:30-3:00 PM. Perhaps moderate or

stronger winds cause P. semiflaviventris to stop hunting, perhaps the wasps do not normally hunt later

than about 2:00 PM, or perhaps hunting flights consist of many short hops.

It is possible that hunting for eggs on branches

involves behavior distinct from that of hunting on

leaves, as on several occasions females of T. bodkini

were seen walking along branches and responding

to bugs as if they were searching for eggs.

It is clear that the species of tree somehow influences the hunting behavior of P. semiflaviventris. Parasitism by this wasp shows a general

correlation with leaf size, being highest in eggs

laid on larger leaves. Even though the defensive behavior of the bugs may be somewhat less effective

against P. semiflaviventris on the small-leaved P.

dulce, eggs on this tree are much less heavily parasitized than those in other trees. The relatively

constant rates of T. bodkini in different tree species

on the other hand suggest that its hunting behavior is not influenced by the tree species.

The rate of parasitism in a given tree species

must be a function of both the facility with which

a wasp finds egg masses (hunting efficiency) and

the time it spends looking for them there (hunting

effort). The relative weights of these two factors

are unknown. It would seem that trees with larger

and fewer leaves would, a priori, be easier to

search; this would explain the variations in P.

semiflaviventris rates, but would imply that T.

bodkini hunts more in trees which are harder for

it to search. Without more knowledge of the

natural habitats of the wasps and bugs and of

alternate hosts of the wasps, it is not possible to

weigh these factors.

Although T. bodkini tends to disperse more

randomly among different species of tree than does

P. semiflaviventris, parasitism rates by T. bodkini

were far from uniform, even in trees of the same

species, and significant differences occurred in

given trees at different times. These differences

could be explained by (a) more wasps arriving to

hunt in some trees than in others, (b) individual

wasps searching more in some trees than in others,

and/or (c) some trees being more easily searched

than others of the same species. The most likely of

these is (a), at least in those cases in which a given

tree's parasitism rates varied over time.

COMPETITION BETWEEN THE WASPS

The two species of wasps compete with each

other at two points in their life cycle; the males

tend to exclude each other from egg masses and,

probably as a result of larval competition within

the egg, only one wasp grows from any egg parasitized by both species. It appears that neither

species is completely dominant in either type of

competition, although T. bodkini males may be

somewhat superior fighters. Both types of competition are common in Cali.

The result of interspecific competition between

males is that, at least on some trees, substantial

numbers of females are left unfertilized. Analyses

of the sexes of wasps from egg masses showed that

unfertilized females seldom lay eggs (assuming

that unfertilized eggs produce males, as is generally

true for Hymenoptera). Whether unmated females

mate away from the egg masses where they emerged

(laboratory observations indicate that this is pos-
NUMBER 205 35

sible, at least in T. bodkini), or whether they never

oviposit is not known. In any case, interspecific

competition among males probably causes appreciable reductions in the rates of parasitism by both

species in at least some situations.

It should be noted that this host-parasite system

is somewhat unusual in that the bug's defense of

its eggs probably buffers the competition between

the wasps to some extent. By more or less excluding

T. bodkini from most parts of the egg mass, the bug

makes some eggs avilable to P. semiflaviventris

even in areas of relatively high T. bodkini density.

The bug's defense also lowers the premium on the

searching ability of the wasps, since a wasp's

ability to outmaneuver the bug once she has located an egg mass is also a factor in her competitive

success. Thus the superiority of one species in

hunting might be such that it would displace the

other under different circumstances, but would fail

to do so in this system because of its difficulty in

overcoming the defenses of the bugs.

Net influence of the guarding behavior of the

bugs on the total effectiveness of the wasp population's ability to parasitize eggs is not known. The

bugs certainly delayed and repelled some wasps and

caused many others to waste time trying to attack

unsuitable eggs. But they also acted as beacons indicating the location of the eggs, and the balance of

these factors is unknown.

EVOLUTIONARY RELATIONSHIPS OF THE WASPS

F. Wilson (1961) described various characteristics which are common to most wasps of the family

Scelionidae. On comparing the two species of this

study against his scheme (Table 23), it is clear that

T. bodkini is less specialized (closer to the family

norm) than P. semiflaviventris and that the main

points of difference in both species are associated

with oviposition.

The differences of both species from the family

pattern are probably due to the unusual circumstances they encounter while ovipositing. They

must overcome the defensive behavior of the guarding bugs, while at least some of the scelionids considered by Wilson attack unguarded eggs (Wilson,

pers. comm.). It seems likely that characteristics

#6, 7, and 8 would be disadvantageous during

battles with defending bugs since they would slow

the wasp's oviposition and thus give the bug more

TABLE 23.—Characteristics of T. bodkini and P.

semiflaviventris as compared with those of other

scelionids (F. Wilson 1961)

Family norm for Scelionidae

1. Males emerge before

females

2. Males stay on egg mass

where emerged, fight with

other males there

3. Copulation occurs as female

emerges from host egg...

4. More females than males...

5. Each male can fertilize

many females

6. Females fight each other

while attacking an egg

mass

7. Female marks host egg

after ovipositing into it..

8. Female distinguishes

already parasitized eggs

from others

Same characters found in—

T. bodkini P

yes

7

yes

yes

yes

probably

almost never

sometimes

yes, at least

sometimes

. semiflaviventris

yes

J

yes

yes

yes

probably

no

no

no

time to kick it away. This idea is supported by the

fact that T. bodkini females perform more marking and inspection when on undefended eggs than

when battling a bug.

F. Wilson (1961) also describes several other

characteristics of Asolcus basalis, which he does not

attribute to the rest of the family, and the species

of this study share several of these, including the

method of cutting the cap of the bug's egg on

emergence, and the predominance of emergences

in the morning (at least in P. semiflaviventris).

They differ in that they oviposit much more

quickly—approximately 4 seconds in P. semiflaviventris and 20-30 seconds in T. bodkini as against

3-4 minutes in A. basalis. Oviposition times of

other scelionids which attack undefended eggs are

also relatively long: 2.5 minutes in Telenomus

gifuensis (Hidaka, 1958), 6-8 minutes in T. fariei

(Lima, 1928), 5-20 minutes in Hadronotus ajax

(Schell, 1943), and 0.5-2 minutes in Platytelenomus sp. (?) hylas (Moutia and Courtois, 1952).

Egg marking behavior by T. bodkini is also much

shorter (1-2 seconds) than that of A. basalis (about

20 seconds—F. Wilson, 1961). Again these differences appear to represent adaptations to overcome

the bug's defense of her eggs. One other small dif-
36

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

ference is the rubbing movement made occasionally by P. semifiaviventris males mounted on females before mating.

P. semifiaviventris is more specialized to overcome the bug's defenses than is T. bodkini: in each

case in which the two species differ from the

scelionid norm, P. semifiaviventris is farther from

the norm than T. bodkini and the ability of P.

semifiaviventris to extend and curve its abdomen,

an unusual feature for the family (Scelio pembertoni, a parasite of buried grasshopper eggs—

Pemberton, 1933—also extends its abdomen when

ovipositing), is also clearly an aid in penetrating

the bug's defense. P. semifiaviventris' combination

of "advanced" characters enables it to parasitize

relatively well-defended areas of the egg mass,

while the "less specialized" T. bodkini is more or

less restricted to one poorly defended edge. T.

bodkini attacks appeared to be more efficient in one

situation, however—when the wasps parasitized eggs

as they were being laid by the bug.

F. Wilson interpreted the various characteristics

he described as being adaptations favoring the

species, but it is possible and thus preferable (see

Williams, 1966, for example) to explain them as

adaptations to benefit the individual. Each female

would be favored by the ability to distinguish and

refrain from ovipositing into eggs already parasitized, and by her aggressiveness toward other females on a given egg mass. The same would hold

for aggressiveness between males on egg masses.

Aggressive males emerging early and staying to

copulate with females from the same mass would

avoid having to hunt for females, and thus benefit

from the likely high concentration there, and they

would give their mates a maximum amount of

time to hunt for hosts. Females which mated as

soon as they emerged would have more time to

search for hosts. And within this framework, a female would maximize the reproductive potential of

her offspring by producing more female than male

eggs, laying only the minimum number of male

eggs necessary to insure the fertilization of the females in that egg mass.

SELECTION PRESSURES ON THE BEHAVIOR

OF THE BUGS

THE CHOICE OF SITES FOR EGG MASSES.—The data

relating the sites of egg masses to variations in

parasitism, failure to hatch, losses from the tree by

falling, and losses of first instar nymphs reflect the

workings of natural selection on the bugs' choices

of oviposition sites. The balance of these factors

was not always the same in different trees, and the

bugs did not always act in their own best interests.

Natural selection clearly favored laying eggs on

branches rather than leaves in T. catappa, while

losses were nearly even in P. dulce (Table 24). In

both species of trees, however, the bugs laid on

leaves much more often than on branches, and the

difference between the tree species was the reverse

of what survivorship data would predict, with T.

catappa leaves being more heavily favored than

those of P. dulce (Table 24). These data suggest

TABLE 24.—Percent losses of A. tripterus offspring in different trees, on leaves

and branches of the same trees and frequency of oviposition in these sites

Cause of loss

Parasitism by—

T. bodkini

P. semifiaviventris

Failure to develop

Eggs fall from tree

Loss of first instar nymphs

Total average survival

Frequency of oviposition .

Number of egg masses ..

Number of trees

T. catappa P. dulce

Leaves

8%

64%

5%

very small

2-3%

3 1 %

92.5%

519

15

Branches

13%

32%

3%

very small

8%

52%

7.5%

Leaves

2 1 %

10%

4%

3 1 %

10%

49%

87%

Branches

3 5%

7%

8%

very small

20%

4 5 %

1 3%

1221

14
NUMBER 205 37

the hardly surprising conclusion that the bugs

evolved in circumstances very different from those

in present-day urban Cali, and that they are probably presently evolving new behavior to adjust to

this environment. Modified selective regimes in

urban areas are probably common for many organisms (e.g., Ford, 1955; Waldbauer and Sternburg, 1967). Just what the original conditions were

in which A. tripterus evolved a preference for ovipositing on leaves is a matter of conjecture.

Survivorship data also permit comparisons between species of tree. Thus the total survivorship

through the first instar on P. dulce was about 48%

(49% of the 87% on leaves plus 45% of the 13%

on branches), that on T. catappa was about 33%

(31% of 92.5% plus 52% of 7.5%), and that on

Cassia sp. was about 45% (branch masses were almost nonexistent; average rates were 54% parasitism, 1% failure to hatch, 16% falling from the

tree, and 5% loss of first instar nymphs). Natural

selection on eggs and first instar nymphs favored

bugs ovipositing in Cassia sp. and P. dulce trees

over those laying eggs in T. catappa, but in fact

trees of the latter species commonly had large populations of bugs and eggs.

DEFENSE OF EGGS BY FEMALES.—The striking fact

that the defense of their eggs by the female bugs,

which in various respects appears to be specifically designed to combat the parasitic wasps,

nevertheless causes a net loss of eggs to at least one

of the wasp species, suggests the following possible evolutionary history. The bugs are certainly

descended from an ancestor that did not guard its

eggs, although at least four other Antiteuchus

species are presently subsocial. This ancestor's eggs

were probably strong enough to withstand attacks

by generalized predators such as ants, but were

relatively defenseless against parasites such as

scelionids, which were able to oviposit through

hard shells. Bugs began guarding their eggs because

of the selective advantage of repelling parasites.

Their existing responses to disturbances (as seen

in present-day nymphs and males)—antennating

toward the source of disturbance, shaking the body,

and perhaps kicking toward the disturbance—combined with suppression of the tendency to flee,

served to drive away enough of the parasites to

make guarding worthwhile, and incidentally drove

off generalized predators also.

Over time the defensive responses of the bugs

became more finely adjusted to the attack behavior

of the parasites: they acquired the defensive movements of scraping and leaning toward the source of

disturbance, perhaps later suppressing scraping

after the nymphs had hatched out; they suppressed squirting defensive liquid, feeding, and the

tendency to turn and face disturbing stimuli; and,

perhaps, they modified several details of oviposition behavior, and began laying more compactly

arranged egg masses, and facing toward the tips of

such masses and toward the tip of the leaf. At the

same time, the egg cuticle became thinner, as the

eggs were now guarded from attacks of generalized

predators as well as from parasites, and this material could be more advantageously used in other

ways.

The wasps, especially P. semiflaviventris, evolved

in response to the changes in the behavior of the

bugs, modifying several aspects of their oviposition

behavior to speed it up, and also beginning to use

the presence of the bug as a cue to the location of

egg masses. P. semiflaviventris also evolved a greatly

extendible abdomen. The advances of the wasps

have been such that at the present time the bug

loses more eggs to parasites than it saves from them

by guarding. The production of thinner egg shells,

however, has trapped the bugs into remaining on

their eggs, which are now susceptible to many other

predators in addition to the parasites.

DEFENSE OF FIRST INSTAR NYMPHS BY FEMALES.—

Since losses of unguarded nymphs were not prohibitively high (Table 21), the possibility arose

that female bugs lost more than they gained by

guarding nymphs. The cost of guarding behavior

was calculated by comparing the lengths of time

until the next oviposition in two cases: females

taken from newly hatched (<12 hours old) first

instar nymphs, and females from second instar

nymphs (these had spent about a week guarding

first instar nymphs and 0.5-1 day guarding second

instar nymphs). The females from the new first

instars reoviposited on the average 19 days later

(giving a rate of egg production of 28/19 or 1.47

eggs/day), while the others averaged 17 days until

reoviposition (1.65 eggs/day). Comparing the two

tactics—desertion or nondesertion of first instar

nymphs—in terms of time, deserters would spend

7+19 = 26 days between ovipositions, and nondeserters 7 + 7+17 = 31 days between ovipositions.

The time difference multiplied by the rate of egg
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

production by deserters (5 X 1.47) gives the actual

cost in eggs of guarding behavior—7.4 eggs each

cycle.

The savings, in terms of nymphs, resulting from

guarding behavior amount to about 30% of the

nymphs hatched in both P. dulce and Cassia sp.

trees (Table 21). For unparasitized masses of 28

eggs, this would amount to 8.4 nymphs per cycle.

Thus, even without taking into account the advantages of protecting nymphs as they moult to the

second instar (their bodies are soft and for a short

while they are without defensive odor) and the

possible dangers to the female before she oviposited

again, the benefits outweigh the costs of guarding

first instar nymphs. This should be equally true for

situations of high and low parasitism, unless parasitism rates are declining steadily.

Desertion rates were higher in P. dulce than in

Cassia sp., even though the rates of loss of nymphs

from unguarded groups were about the same in

both species. Thus, at least in urban Cali, the

stimuli which cause the bugs to desert their nymphs

do not accurately reflect the likelihood of losses of

unguarded nymphs.

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Blatchley, W. S.

1926. Hemiptera or True Bugs of Eastern North America. Indianapolis, Indiana: Native Publishing Co.

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1944a. A Note on Phanuropsis semiflaviventris Cirault

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