Ins. Soc. 39:73-80 (1992)
1015-1621/92/010073-8 $ 1.50 + 0.20/0
© 1992 Birkhiiuser Verlag, Basel
The effects of colony characteristics on life span and foraging
behavior of individual wasps (Polybia occidentalis,
Hymenoptera: Vespidae)
S. O'Donnell and R. L. Jeanne
Department of Entomology, University of Wisconsin, Madison, WI 53706, USA
Key words: Behavioral control, behavioral development, contingency, life span.
Summary
We studied the effects of intrinsic colony characteristics and an imposed contingency on the life span
and behavior of foragers in the swarm-founding social wasp Polybia occidentalis. Data were collected
on marked, known-age workers introduced into four observation colonies.
To test the hypothesis that colony demographic features affect worker life span, we examined the
relationships of colony age and size with worker life span using survivorship analysis. Colony age and
size had positive relationships with life span; marked workers from two larger, older colonies had
longer life spans (X = 24.7 days) than those from two smaller, younger colonies (X 20.1 days).
We quantified the effects of experimentally imposed nest damage on forager behavior, to
determine which of three predicted behavioral responses by foragers to this contingency (increased
probability of foraging for building material, increased rate of foraging, or decrease in age of onset of
foraging) would be employed. Increasing the colony level of need [or materials used in nest
construction (wood pulp and water) by damaging the nests of two colonies did not cause an increase
in either the proportion of marked workers that gathered nest materials or in foraging rates of
marked individuals. when compared with introduced workers in two simultaneously observed
control colonies. Instead, nest damage caused a decrease in the age at which marked workers first
foraged for pulp and water. The response to an increase in the need for building materials was an
acceleration of behavioral development in some workers.
Introduction
Insect societies are inherently dynamic. Through the usual course of development,
colonies undergo intrinsic changes, such as fluctuations in adult and brood
populations. Colonies also face such extrinsic contingencies as predation and
changes in availability of food resources, to which they must respond appropriately if
they are to reproduce. If selection acts on colonies to enhance their efficiency and
reliability, workers should be sensitive to intrinsic and extrinsic changes in colony
conditions and alter their behavior accordingly (Jeanne, 1986; Calabi, 1988).
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O'Donnell and Jeanne
We studied the effects of the intrinsic properties of colony age and adult
population size and an extrinsic contingency, experimental nest damage, on forager
life span and behavior in the social wasp Polybia occidentalis (Olivier). Workers of
this species show age polyethism, yet within colonies, individuals show great
variability in life span and in the age of first performance of different tasks (Jeanne et
aI., 1988). The causes of this behavioral variability are poorly understood. The
purpose of this study was twofold: to determine whether forager life span was
dependent on colony age and size, and to determine how an experimentally imposed
contingency (nest damage) affected foraging behavior.
That colony demographic parameters influence the behavior and life span of the
colony's constituent members has long been recognized (Wilson, 1971). Since larger,
older colonies should be more buffered against contingencies, for example by virtue
of increased food stores or homeostatically superior nest structure, the predicted
relationship between colony size and individual life span is that workers in larger,
older colonies live longer. Studies on honeybees (Winston and Fergusson, 1985) and
primitively social wasps (Strassmann, 1985) have shown the predicted effects of
colony size on worker life span. The relationship between colony size and age with
worker life span has not been examined in swarm-founding wasps.
Previous work on P.occidentalis showed that a small number of workers
generates the increased rate of foraging for building materials at the colony level in
response to nest damage (O'Donnell and Jeanne, 1990). Here, we examine the
behavioral changes at the individual level which account for the increased rate of
building material input to the colony. There are three possibilities: (1) Workers are
recruited to foraging for building materials from other tasks. If this is the case, there
should be an increase in the proportion of building material foragers among the
marked workers in damaged colonies. (2) Building material foragers raise their
activity level. If this effect is important, there will be an increased rate of foraging for
building materials by marked workers in damaged colonies. (3) Behavioral develop­
ment is accelerated in response to damage. By acceleration of development we mean
that the performance of certain tasks, in this case foraging, begins at an earlier age in
workers in treated colonies than in their counterparts in control colonies. If this
occurs, building material foragers should become active at an earlier age in damaged
colonies.
Methods
Study Site and Organism
The study was conducted from 26 June through 8 August 1989 at Hacienda La
Pacifica in the province of Guanacaste, in northwestern Costa Rica. P. occidentalis is
abundant in open pastures at this site, where the wasps build enclosed, gourd-shaped
nests of wood-fiber carton. We chose four colonies nesting in low shrubs for
observation, based on ease of access. These colonies were in the ergonomic phase of
development for the duration of the study: all were rearing brood and producing
adult workers, but males (and presumably reproductive females) were not being
produced.
Foraging by Polybia occidentalis
75
Worker Introductions
Combs with pupae were removed from two P. occidentalis nests and maintained at
ambient temperature in mesh-covered containers as sources of known-age workers.
All adult wasps emerging from these combs were removed every 24 h, and a subset
was chosen unsystematically for introduction into the observation colonies; the
remainder were discarded. Wasps used for introduction were anesthetized with ethyl
ether, marked with paint for individual identification, and placed into the entrance of
an observation colony's nest. Introduced adults, if less than 24 h old, are accepted
into foreign colonies and enter the worker force (Jeanne et aI., 1988). Workers were
added to observation colonies at two- to five-day intervals over periods of 11 or 13
days. Cohorts of 8-20 wasps were added on a given day, the cohort size being
determined by how many adults had emerged from the source combs during the
previous 24 h. All marked adults were assigned an age of one day upon introduction
to the observation colonies.
Behavioral Observations
With few exceptions, we observed each colony every other day. Thus, two of the
colonies were observed twice per day, in the morning and afternoon. Colonies 4 and
10 were observed from 28 June to 30 July, colony 5 from 16 July to 3 August, and
colony 13 from 15 July to 8 August. Behavioral data were collected by an observer
seated approximately 1 m in front of the nest. Observation sessions lasted a mean of
73 min. in the morning and 61 min. in the afternoon. No observations were made
during periods of heavy rainfall. We did not record behavior of unmarked workers,
and did not measure colony-wide activity during this study. Each time a marked
forager arrived at the nest we recorded her identity, the material she carried, and time
of landing to the nearest minute. Foragers collect four materials: nectar and insect
prey (nutritional materials) and wood pulp and water (building materials).
P. occidentalis foragers nearly always transfer their loads to other workers on the
external nest surface where they are visible to observers (Jeanne, 1987); nectar and
water loads can be distinguished by observing the position of the forager's antennae
during transfer (Hunt et aI., 1987).
Experimental Manipulations
We manipulated colonies 4 and 5 by damaging the nests at 1800 h (sunset) on the
evenings preceding observation days. Damage consisted of removing a 5 cm x 7 cm
piece of the lowermost section of the nest envelope. This low-level perturbation
always induced nest repair the following morning. Nest repair by P.occidentalis
entails an increase in colony rates of foraging for water and wood pulp (O'Donnell
and Jeanne, 1990) and building behavior (Jeanne, 1987). Nest damage manipulations
were not performed on days when the colonies were engaged in nest expansion, which
involves the same foraging and building tasks as nest repair (Jeanne, 1987). Colonies
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O'Donnell and Jeanne
10 and 13 served as controls; these colonies were not damaged and did not engage in
nest expansion during the study.
Colony Collection
After the completion of behavioral observations, the four observation colonies were
collected in plastic bags containing ether-soaked cotton. The collections were
performed after 2000 h to ensure that all workers were present. The nest sites were
checked for returning workers the morning following collection; no remaining adults
were seen at any of the nest sites.
Colony age was estimated by counting the layers of pupal excrement (meconia) in
the older (uppermost) combs of the nest. The number of meconi a per cell provides a
record of the number of generations of brood raised. All adult wasps were preserved
in Kahle's fixative solution (Barbosa, 1974) or frozen and later counted for a measure
of colony size.
Data Analysis
The materials gathered by foragers require different amounts of field time for
collection ofone load; trips for water require the least time in the field (O'Donnell and
Jeanne, 1990). To compensate for these differences when analysing foraging rates, we
weighted the number of trips for each material by the mean time to collect that
material relative to the mean water trip time (see O'Donnell and Jeanne, 1990 for
details).
Patterns of worker lifespan and rates of behavioral development were analysed
using the life-table method of survival analysis (SAS Institute, 1985). The log rank
test was employed to test for differences in worker life span among colonies, as
reflected in the survival distribution functions (henceforth SDF) of marked workers.
Marked workers not present when the colonies were collected were assumed to
have died on the last day on which they were observed foraging. This estimate sets a
lower bound on life span, since workers may have foraged unobserved or engaged in
other activities at later dates. All marked workers present in the collected colonies
were censored in the survival analysis, which means that the fact that the study ended
before they died was taken into account when life span was analysed (SAS Institute,
1985).
Results
Effect of Colony Size and Age on Life Span
Survival analysis using life-table methods showed significant differences between
colonies in the distribution of adult age at termination of foraging (Fig. 1; log-rank
3,p < 0.01). The SDF
test for homogeneity ofSDF among colonies, X 2 = 15.9,
of the two smallest colonies, 4 and 10 (294 and 301 wasps when collected,
Foraging by Polyhia occidentalis
77
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Age (days) at beginning of interval
Figure 1. Survival distribution functions (SDF) of worker age at last observed foraging for four
P. occidentalis colonies. At the time of collection, colony population sizes and maximum layers of meconia
were as follows: Colony 4,294 adults, 3 layers; Colony 5, 964 adults, 4 layers; Colony 10, 301 adults, 2 layers;
Colony 13, 329 adults, 4 layers. Mean worker life span in colonies 4 and 10 combined = 20.1 days; mean life
span in colonies 5 and 13 combined = 24.7 days
respectively), did not differ statistically (X2 = 3.4, df = 1, p < 0.05; mean worker life
span 20.1 days); likewise, the largest colonies, 5 and 13 (964 and 329 wasps when
collected, respectively), had statistically indistinguishable SDF (X2 = 2.7, df = 1,
p > 0.05; mean worker life span = 24.7 days). Colonies 4 and 10 were also the
youngest, having a maximum of 3 and 2 (respectively) layers of meconia in the cells of
the oldest comb. Colonies 5 and 13 each had a maximum of 4 layers of meconia in the
upper combs, indicating that they were at least one brood generation time older (21­
35 days in the wet season; Forsyth, 1978).
Effects of Experimental Nest Damage on Foragers
The manipulated colonies (4 and 5) engaged in nest envelope building, either nest
repair or nest expansion, on all observation days. Envelope building was not
observed in control colonies; the wood pulp and water gathered by these colonies
were probably used for brood-cell heightening and nest cooling, respectively (SO'D
and RLJ, pers. obs.).
Experimental nest damage did not cause an increase in the proportion of
introduced workers that foraged (Damaged: Colony 4, 51 % of 88 introduced;
Colony 5, 38% of 105 introduced; Control: Colony 10, 56% of 80 introduced;
Colony 13, 58 % of 105 introduced). Of the workers that foraged, nest damage did
not consistently increase the proportional representation of nest material foragers in
the marked forager force (Damaged: Colony 4, 13 % of 45 foragers; Colony 5, 28 %
of 40 foragers. Control: Colony 10, 7% of 45 foragers; Colony 13,20% of 61
78
O'Donnell and Jeanne
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control
damaged
Treatment category
Figure 2. Box plots of the effect ofexperimental nest damage and nest expansion on age of first foraging by
building material foragers. Each box combines data from two colonies. The centralline represents the
median value, boxes enclose the interquartile (second to third quartile) range, whiskers enclose values within
1.5 interquartile ranges of the box, and the asterisk denotes a value outside the whiskers. In control
colonies, X age of first foraging 24.7 days; in treatment colonies, .¥ age of first foraging 19.0 days
foragers; Maximum likelihood analysis of variance estimate for contingency test,
= 1.97, df= 1, p > 0.10).
Nest material foragers in the damaged colonies did not collect wood pulp and
water at higher rates than those from control colonies (Building material foraging
rates: Damaged colonies, X = 4.3 time-weighted trips/hour; Control colonies,
X = 5.8 time-weighted trips/hour; Wilcoxon 2-sample test, Z = 0.07, P > 0.90).
Experimental damage did accelerate the rate of behavioral development of some
marked workers. Since few workers from each colony collected building materials,
data were pooled among the two colonies within each treatment category to increase
statistical power. The workers that collected nest materials made their first foraging
trips, regardless of material, at an earlier age in damaged colonies (Fig. 2; Wilcoxon
2-sample test, Z = 2.43, P < 0.05), and foraged for nest materials in particular at an
earlier age in damaged colonies (Mean control age 25.8 days, mean treatment
age = 21.4 days; Wilcoxon 2-sample test, Z = 2.20, P < 0.05).
Discussion
Effects of colony demography on worker life span have been noted in other species of
social Hymenoptera. Because we observed colonies in the field, we were unable to
separate the effects of colony size and age in this study; this was also the case in
Strassmann's (1985) study on Polistes. Winston and Fergusson (1985), working with
Apis, manipulated colony size experimentally, thus removing the confounding factor
Foraging by Polybia occidentalis
79
of colony age, and showed that workers in smaller colonies foraged at an earlier age
and had deereased life spans. From these few studies it appears that worker life span
generally increases with colony size, although the reasons for this are not clear.
Larger or older colonies may be expected to have greater stores of nutrients, more
homeostatic ally efficient nests, and well-established foraging routes and/or spe­
cialized foragers in place. Therefore, workers in large colonies may not work as hard,
and thus have greater life span. However, we did not find differences in the
distributions of foraging rates among workers from the four observation colonies
(O'Donnell and Jeanne, unpub. data), so by this measure, increased life span in the
older, larger colonies is not explained by differences in work load. Similarly, Wolf and
Schmid-Hempel (1990) found that workers from small honeybee colonies did not
adopt higher workloads than those from larger colonies.
Several studies have examined the short-term behavioral response of social
hymenopteran workers to various experimentally imposed colony contingencies (e.g.
Aron et aI., 1986; O'Donnell and Jeanne, 1990). Few have utilized the long-term
observations of identified, known-age workers that are necessary to distinguish the
three possible changes in worker behavior examined here (probability of task
performance, rate of task performance, and age of initiation of task performance).
Kolmes (1985) found that honeybee workers introduced into stressed (wax-deprived)
colonies raised their group activity level, but he did not analyse the behavioral effect
at the individual level. In this study, we showed that experimental nest damage
accelerated the rate of P. occidentalis behavioral development by decreasing the age
of first foraging in nest-material foragers. Neiter the probability that an individual
gathered nest materials nor the distribution of foraging rates for building materials
was affected.
Two studies on the ant Tapinoma erraticum (Lenoir, 1979; Meudec and Lenoir,
1982) demonstrated that the rate of behavioral development of workers, as indicated
by worker age at first foraging, can be accelerated under conditions of colony
starvation and of a shortage of older workers. Although it is too early to assess the
general importance of changes in the rate of worker behavioral development to insect
colony function, the fact that this pattern occurs in workers of an ant and a social
wasp suggests that it may be a common behavioral mechanism by which workers
respond to changing colony conditions.
Acknowledgements
Access to excellent wasp habitat on the property of Werner and Lilly Hagnauer greatly expedited our
field work. We thank Larry Phelps for his valuable suggestions and capable assistanee in the field.
Ken Glander helped with the storage and shipment of frozen wasps. Finaneial support was provided
by NSF grant BNS-8517519 (RLJ principalinvestigator), and by the University ofWisconsin College
of Agricultural and Life Seiences.
80
O'Donnell and Jeanne
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Received 10 July 1991;
revised 3 November 1991;
accepted 13 November 1991.