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Behavioral Ecology Vol. 12 No. 3: 353-359
© 2001 International Society for Behavioral Ecology
Worker biting interactions and task performance in a swarm-founding eusocial wasp (Polybia occidentalis, Hymenoptera: Vespidae)
Department of Psychology, Box 351525, University of Washington, Seattle, WA 98195, USA
Address correspondence to S. O'Donnell. E-mail: sodonnel{at}u.washington.edu .
Received 10 April 2000; revised 31 August 2000; accepted 8 October 2000.
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ABSTRACT |
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Workers in many insect societies interact via body contact with their nest mates, and social biting and other forms of contact may play a general role in regulating task performance. Here I present evidence that social biting affects task performance without direct reproductive conflict in Polybia occidentalis, a swarm-founding eusocial wasp. Polybia occidentalis workers engaged in social biting with nest mates. Most workers that were active on the nest surface participated in biting interactions, but individuals differed significantly in their rates of biting and of being bitten. Rates of being bitten corresponded with nonreproductive task performance: more biting was directed at foragers than nonforagers, and foraging rates were correlated with rates of being bitten. Furthermore, some on-nest workers initiated foraging activity immediately after they were bitten. Together these patterns suggest that social biting influences foraging rates by increasing workers' probabilities of leaving the nest. Variation in biting rates did not correspond with differences in reproductive physiology: highly active biters and recipients did not differ in body size or in ovary development. In P. occidentalis and in other eusocial insects with large worker forces, biting and other types of social contact among workers may regulate task performance independently of direct reproductive competition.
Key words: body size, foraging, ovary development, polyethism, reproductive conflict, social organization.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Division of nonreproductive tasks among workers, or polyethism, is a key adaptation promoting the evolutionary and ecological success of eusocial insects (Wilson, 1990
). As
insect colony sizes have increased over evolutionary time, new challenges have
arisen for regulating the labor force. In small colonies of up to a few dozen
members, polyethism can be effectively regulated via central, hierarchical
control from the queen or other dominant individuals
(O'Donnell, 1998a;
Reeve and Gamboa, 1987).
However, centralized task organization is not possible in larger insect
societies, and instead the worker caste is self-organizing
(Nicolis and Prigogine, 1977;
Seeley, 1989;
Wilson and
Hölldobler, 1988). Self-organization
requires that workers share information about task performance needs
(Kaufman, 1991). Identifying
the communicative interactions among workers that regulate polyethism remains
as a central challenge to insect sociobiology
(Jeanne, 1986a;
Robinson et al., 1989;
Seeley, 1986).
Dominance status and aggression among group members have been shown to
affect division of labor in many animal societies (cooperatively breeding
birds; Brown et al., 1997;
primates, including humans; Drea and
Wallen, 1999; Hawley,
1999; but see Jacobs and
Jarvis, 1996 for a counter-example in naked mole rats).
West-Eberhard (1981; see also
Jeanne, 1991) hypothesized
that worker-like behavior will be performed by the losers of fights over
direct reproduction in animal societies. West-Eberhard's model predicts that
task performance decisions will correlate with variation in direct
reproductive value; more fecund, dominant individuals should avoid risky or
costly behavior such as foraging. This model is supported for some eusocial
insects by two observations. First, social aggression often determines
reproductive division of labor, and second, workers' aggressive status often
corresponds to their reproductive physiology (honey bees;
Hillesheim et al., 1989;
Ratnieks, 1993; bumblebees;
van Doorn, 1987; ants;
Cole, 1981;
Heinz and Oberstadt, 1999;
Powell and Tschinkel,
1999).
Other studies suggest that worker contact interactions can regulate task
performance independently of direct reproductive conflict. Biting and other
types of body contact occur in advanced insect societies. Contact interactions
have been noted in species where workers have reduced opportunities for direct
reproduction (Gordon and Mehdiabadi,
1999; Gordon et al.,
1993; Montagner,
1966). In these species, worker interactions may function in the
regulation of division of labor and task performance
(O'Donnell and Jeanne,
1995).
The goal of this study was to assess the relationships of contact
interactions (biting among nest mate workers) with task performance and with
reproductive physiology in the swarmfounding wasp Polybia occidentalis.
Polybia wasps are important subjects in studies of the regulation of
division of labor (Jeanne,
1986b; O'Donnell and Jeanne,
1992). Polybia workers have well-developed temporal
polyethism and exhibit a high degree of task specialization
(Jeanne, 1986b;
O'Donnell, 1998b). Polybia
occidentalis colonies build ovoid nests that are enclosed in a covering
envelope with a single entrance hole. At approximately 1 week of adult age,
most workers move from performing in-nest tasks to performing tasks outside
the nest. The older workers spend much of their time on the exterior nest
surface where they are visible to observers, and later they begin flying from
the nest to forage. Foraging workers nearly always arrive and depart from the
nest surface, and transfer the materials that they collect to workers on the
nest (Hunt et al., 1987;
O'Donnell and Jeanne, 1992).
Workers frequently engage in biting interactions with nest mates
(O'Donnell and Jeanne,
1995).
I quantified rates of giving and receiving social biting for individually marked P. occidentalis workers, and simultaneously quantified on- and off-nest task performance. I used these data to test for relationships between biting interactions and individual differences in task performance. I also measured variation in body size and ovary development to determine whether individuals' rates of biting and task performance were associated with morphology or reproductive physiology. I discuss evidence that biting regulates polyethism in P. occidentalis and in other large-colony eusocial species, and I suggest experimental manipulations to further test this hypothesis.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study site and observation colonies
Fieldwork was conducted from 12 to 23 July 1999 near Centro Ecologico La Pacífica, Guanacaste Province, Costa Rica (10°25' N, 85°07' W). Local habitats include savanna-like pasture with scattered shrubs, rice fields, and gallery forest, and the area is artificially irrigated throughout the year. Polybia occidentalis is abundant at this location. I selected three subject colonies based on ease of access (i.e., nesting within 2 m of ground) and of intermediate size for the population at La Pacífica (nests were approximately 12 cm in height). The subject nests were moved to covered, open shelters, shielded from rain and direct sunlight, and wired to a supporting frame. I moved the colonies at night to ensure that foragers would be present, and to minimize loss of adults during transport. I mounted a mirror behind each nest to facilitate observation of the entire nest surface, and to encourage foragers to approach the nest by flying toward the entrance hole. The subject colonies were not disturbed for at least 24 h after moving to allow the wasps to acclimatize to the new location. All colonies foraged on the day after they were moved.
I collected a subset of the workers from each subject colony and marked
them for individual identification on the day prior to starting behavioral
observations. To collect workers for marking, I placed a plastic bag
containing an ether-soaked cotton ball around each nest in predawn light at
0445 h, before foragers had begun to leave the nest. I mildly alarmed the
colony by tapping the bag, and I collected the adults that responded by flying
into the bag. Wasps were kept anesthetized with ether, and by cooling them in
a refrigerator, while they were marked. Each wasp was uniquely marked on the
dorsum of the thorax with paint pens
(O'Donnell and Jeanne, 1992).
After marking, wasps were returned to their nests and placed into the nest
entrance. I marked 250 female wasps in colony A, 353 in colony B, and 179 in
colony C. I noted when males were present (recognized by silvery pubescence on
the front of the face), but I did not mark them.
Behavioral data
I collected behavioral data while seated 0.5 to 1 m from the nests, facing
the entrance opening. For each colony, I conducted two daily continuous
observation sessions of 3 h duration on two consecutive days (12 h observation
total per colony). Morning sessions started between 0700 h and 0745 h local
time, and afternoon sessions started between 1200 h and 1240 h. These
observation times sampled the most active foraging period for P.
occidentalis at La Pacífica
(Jeanne et al., 1988;
O'Donnell and Jeanne,
1992).
I defined biting interactions as contact involving one wasp's mandibles
(the biter) chewing on a nest mate's body (the recipient), at any location
other than the mouth parts. Mutual mouth part contact occurs during food
exchange and solicitation (Hunt et al.,
1987). I distinguished three levels of intensity of biting
interactions. Mild biting was the lowest intensity of interaction, and
involved the biter slowly chewing on the recipient, without visibly moving the
recipient's body parts. Moderate intensity biting involved more vigorous,
rapid chewing, with part of the recipient's body being displaced or vibrated.
Severe biting was the highest intensity category, involving more rapid
movement and frequent changes in position by the biter. Severe biting was
often accompanied by the biter bending the tip of her gaster toward the
recipient in stinging movements, and recipients of severe biting were lifted
partly or totally off of the nest surface.
I recorded all occurrences of biting interactions on auditory cassette tape and later transcribed the tapes. For each interaction I noted the time to the nearest min, identity (including unmarked) of the biting wasp(s), identity of the recipient wasp, and whether the recipient flew from the nest within 3 s of the termination of the interaction. I simultaneously recorded all occurrences of arrivals of marked foragers at the nest onto a written data sheet, noting time to the nearest min, identity of the forager, and what material was carried by the forager. Every 15 min, I scanned the entire surface of the nest, noting the identity (including unmarked) of all individuals present.
Colony collections, wing length measurements, and ovary
dissections
I collected the subject colonies after sunset on the final day of
observations. Nests were placed in a plastic bag with ether and immediately
transferred to a freezer. When the adults ceased moving, the nests were
dissected and adult wasps were removed from the nest material. Marked adults
were sorted out. I placed all adult wasps in fixative (Kahle's solution, 18:
1:1 volumes 70% ethanol:glacial acetic acid:formalin). I noted the number of
brood combs and brood developmental stages.
After fixing in Kahle's solution for at least 4 weeks, the marked adults were transferred into 70% ethanol. I dissected the gasters (distal abdominal section) of females that had given or received significantly high rates of biting under a binocular microscope at x 40. I recorded workers' degree of ovary development relative to fully developed ovaries possessed by P. occidentalis queens from the subject colonies. Ovaries were assigned categorical scores from zero (no visible oocyte development, filamentous) to three (fully developed, queen-like ovaries). The dissections were performed blind to the behavior of the wasps. Unmarked wasps from the subject colonies that were preserved and dissected by the same methods showed the full range of ovary development from filamentous, undeveloped ovaries to ovaries with numerous large oocytes. There was no indication of distortion of oocyte shape or size relative to freshly collected wasps (personal observation).
I removed both of the mesothoracic wings from the bodies of the females
that had given or received significantly high rates of biting. The wings were
unfolded and mounted flat on microscope slides with transparent tape. I
scanned the mounted wings into computer image files at 600 DPI resolution, and
measured wing length using the ruler tool of Adobe Photoshop 5.0 software. I
measured the length of the rigid anterior wing vein (the costa vein) from its
proximal base to the proximal end of the pterostigma. I used a similar measure
of wing length in an earlier study, and found that it was strongly correlated
with dry body mass (O'Donnell and Jeanne,
1995). Wing length measurements were performed blind to workers'
behavior, and left wing measurements were performed blind to right wing
values. Individuals' left and right wing measurements were highly correlated
(r =.90, p <.0001), so I used the mean of costa vein
lengths as an index of body size.
Data analysis
All ranges presented are the range of values across the three subject
colonies. I tested the distribution of individuals' rates of biting and of
being bitten against the Poisson distribution of expected rates using a
G-test, pooling categories with expected frequency values less than three, and
estimating degrees of freedom as recommended by Sokal and Rohlf
(1981). Individuals that
engaged in biting interactions at significantly high rates were identified for
further analysis using a binomial test (p <.05); the null
hypothesis of the binomial test was that rates of behavior were equal for all
workers within colonies. For other analyses I used nonparametric tests when
the assumptions of parametric tests, such as equal variance among samples,
were violated.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Colony composition
Each subject nest contained four layers of brood comb upon collection. All stages of brood (eggs, larvae of various sizes, and pupae) were present in each colony. Adult males were present only in colony B. Total numbers of adult females present when the colonies were collected were: colony A, 321; colony B, 540; colony C, 348.
Colony-wide rates of biting behavior
On average, 14.3 to 18.7 wasps were visible on the nest surface during
scans (range five to 38). Most of the wasps present on the nest surface were
marked; unmarked wasps comprised 5.5% to 19.8% of individuals present during
scans. Biting interactions occurred at overall rates of 16.2 to 27.8 per h.
Averaging over the number of wasps present on the nest surface during scans
yielded estimates of 1.0 to 1.5 biting interactions per wasp per h on the
nest.
Intensity of biting behavior
Biting interactions typically lasted less than 30 s, but occasionally
extended for as long as 10 min. Biting interactions of mild and moderate
intensity occurred a higher rates than those of severe intensity in all
colonies (Table 1 and
Figure 1). The intensity of
biting occasionally increased during interactions (4.2% of mild and moderate
interactions increased in intensity), but intensity was never observed to
decrease. Most changes in intensity were from mild to moderate (n =
14), followed by changes from moderate to severe (n = 9). A
transition from mild to severe biting was observed once.
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Some interactions involved more than one individual simultaneously biting a single wasp (6% to 16% of interactions). In these instances, from one to five additional workers joined in biting a wasp after the first worker initiated contact. Furthermore, recipients were often bitten by several nest mates sequentially, being bitten by one or more new workers within 10 s after each interaction terminated. Recipients typically remained immobile while being bitten, then groomed themselves or walked over the nest surface in the 10 s immediately following an interaction (but see section on Nest departures following biting).
Individual variation in rates of biting and of being bitten
Marked wasps' behavior was consistent across the 2 days of observation. The
proportion of scans during which individuals were present on the nest was
highly correlated between days (colony A: r =.72, p <.01;
colony B: r =.75, p <.01; colony C: r =.64,
p <.01). Individuals' rates of biting other wasps were also
correlated between days, although this relationship was weaker in colony B
than in the other colonies (colony A: r =.98, p <.001; colony B:
r =.33, p <.01; colony C: r =.95, p
<.001).
Most marked workers bit, and/or were bitten by, other workers (58% to 64% of marked workers). Workers varied significantly in their rates of biting other workers, and in their rates of being bitten. For both biting and being bitten, workers that never performed the behavior, and workers that performed the behavior at exceptionally high rates, were more frequent than expected if biting rates were equal among workers (Figure 2; test of goodness-of-fit to Poisson distribution, G3 to 5 = 19.4 to 92.0, all p <.005). From three to seven individuals in each colony initiated or received social biting more often than expected under the assumption of equal colony-wide rates (Figure 2; binomial test, p <.05). Single individuals in colonies A and C were exceptionally active biters on both observation days, biting nest mates at rates of over nine interactions per h (Figure 2). These individuals were biters in 57% and 42% of their colony's interactions, respectively. Adult males were present only in colony B. Males were bitten by their female nest mates (18.3% of biting interactions were directed toward males). Males were never observed to bite other wasps.
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Active biters interacted with many nest mates, rather than directing their biting at a few targets. For all colonies, the number of recipients of an individuals' biting correlated strongly with their total biting rates (only workers that bit nest mates more than once were included; colony A:r =.97, p <.0001, colony B: r =.82, p <.0001, colony C: r =.96, p <.0001). The maximum number of nest mates bitten by single workers ranged from 11 to 36. Frequent recipients were bitten by numerous nest mates, and the number of biters interacting with each wasp was strongly correlated with her rate of being bitten (only workers that were bitten more than once were included; colony A: r =.70, p <.001, colony B: r =.71, p <.001, colony C: r =.82, p <.0001).
Wing length and ovary development
Most of the highly interactive wasps survived until their colonies were
collected (significantly active biters collected: colony A: 3/3; colony B:
5/6; colony C: 3/3. Significantly frequent recipients collected: colony A:
4/6; colony B: 3/3; colony C: 6/7). Mean wing lengths did not differ among
colonies, and did not differ between active biters and recipients (two-way
ANOVA, all p >.50).
Excepting one female in colony C, no dissected females exhibited ovary
development. No opaque or swollen oocytes were visible in the ovaries, and the
ovaries were classified as filamentous. Wasp number 165 from colony C had
well-developed ovaries with many enlarged, opaque oocytes. However, her
ovaries appeared to be in decline (some distal oocytes were shrunken and
misshapen), and she had a heavy load of unidentified parasites (possibly
gregarines; Richards, 1978).
This female did not forage, and was recorded on the nest surface only on the
second day of observations, when she was bitten at a high rate.
Biting and foraging behavior
Workers foraged for two food materials, nectar and prey, and for two
building materials, water and wood pulp. Most workers collected a single
material (61% to 100% of marked foragers collected one material), and the
remainder of foragers collected two materials.
Foragers were bitten at higher rates than nonforagers (Figure 3; Kruskal-Wallis test, colony A: X2 = 13.1, df = 1, p <.001; colony B: X2 = 4.7, df = 1, p <.05; colony C: X2 = 16.0, p <.001). Workers that were bitten at higher rates also foraged at higher rates (Figure 4; colony A: r =.68, p <.001; colony B: r =.50, p <.001; colony C: r =.30, p <.005). High rates of biting were directed toward both food and nest material foragers. Both active biters and recipients foraged. Active biters were less likely to be foragers than recipients, although this difference was not significant (5/13 active biters foraged, 12/16 frequent recipients foraged; likelihood ratio X2 = 3.23, df = 1, 0.10 > p >.05). The two workers that bit nest mates at exceptionally high rates (colony A and colony C) were active as nectar and pulp foragers, respectively.
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Nest departures following biting
Biting interactions were sometimes immediately (i.e., within 3 s) followed
by departure of the recipient from the nest. More intense interactions were
more likely to be followed by the immediate departure of the recipient
(interactions followed by departure: n = 26, 21.5% of severe biting,
n = 14, 6.1% of moderate biting, n = 6, 1.7% of mild biting;
logistic regression after accounting for colony and individual effects,
X2 = 20.4, df = 2, p <.0001). In some cases,
workers that were already actively foraging left the nest immediately after
being bitten, and continued to forage (pooled across colonies, n = 13
nectar foragers, n = 1 pulp forager, n = 2 water foragers).
In other cases, workers began foraging following biting interactions (workers
that had not previously foraged during an observation session, and were
present on the nest for at least 1 h prior to biting interaction, n =
6 nectar foragers, n = 2 prey foragers, n = 2 pulp
foragers). Two workers departed after being bitten but did not subsequently
arrive carrying materials.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Social biting was a common and conspicuous feature of P. occidentalis worker behavior, and is apparently widespread among Epiponini. My observations of P. aequatorialis (O'Donnell, 1998b
), P.
emaciata, and P. sericea (unpublished data) demonstrate that
biting interactions among workers occur in other Polybia species, and
similar behavior has been noted in the swarm-founding wasp Parachartergus
colobopterus (Strassmann et al.,
1997). Most P. occidentalis nest workers and foragers
engaged in biting interactions. Biting interactions varied in intensity, and
in the responses they elicited from the recipient wasp. Three facts suggest
that biting interactions of different intensity are functionally similar.
First, behavioral transitions occurred from milder to more intense biting.
Second, workers that engaged in biting interactions at significantly high
rates, either as biters or recipients, exhibited a range of interaction
intensities. Finally, bitten workers departed the nest and began foraging
immediately after interactions of all intensities, although they were more
likely to do so after more intense interactions.
Individual differences in biting rates
Workers varied in their rates of biting. Both significantly active biters
and significantly frequent recipients were present in each colony. The fact
that rates of giving and receiving biting were not distributed randomly
indicates that workers differed in their relative social status. These
patterns raise the question of what factor or factors determine variation in
biting behavior. Highly active biters interacted with large numbers of nest
mates. Conversely, several workers often bit a single nest mate
simultaneously, and recipient wasps were often bitten by several nest mates
sequentially.
There may be a mechanism for common recognition of targets of biting, in
other words, an unknown factor that incites biting by nest mates. Some
eusocial wasps respond aggressively to nest mates that have well-developed
ovaries, possibly distinguishing them via chemical cues
(Downing and Jeanne, 1985;
West-Eberhard, 1977).
Aggression toward more fecund nest mates suggests that it functions as a form
of reproductive policing in some contexts
(Ratnieks, 1988). Polybia
occidentalis workers exhibit partial ovary development when young, up to
approximately 7 days of adult age, but workers' oocytes are typically resorbed
around the age at which they begin performing outside-nest tasks
(O'Donnell, in press). No
effects of worker body size or ovary development on biting behavior were found
in this study. Therefore, biting interactions among P. occidentalis
workers on the nest surface were not related to direct reproductive conflict.
Similarly, ovary development bore no relationship with biting interactions
among yellow jacket wasp workers (Vespula;
Montagner, 1966). In P.
occidentalis and yellow jackets, worker social biting occurs outside the
context of direct competition over reproduction.
Although P. occidentalis workers differed in social status, the
proximate mechanisms for these differences remain unclear. One possibility is
that propensity to give or receive biting changes predictably over the course
of adult development. Long-term observations of marked, known-age wasps are
needed to determine how biting behavior changes as workers age. Alternatively,
genotypically different nest mates may consistently vary in biting rates, and
biting may also be a form of genetic nepotism if it is directed at genetically
dissimilar workers. Polybia colonies possess multiple queens and
relatively high genetic diversity (Queller
et al., 1988), and genetic effects on foraging and in-nest task
performance have been demonstrated in P. aequatorialis (O'Donnell,
1996,
1998b). However, Strassmann et
al. (1997) found no genetic
evidence for nepotism in Parachartergus colobopterus biting
interactions.
The function of biting interactions and effects on task
performance
If P. occidentalis outside-nest workers were not competing for
access to direct reproduction, what evolutionary forces maintain biting
interactions? I propose that biting interactions play a role in regulating
P. occidentalis workers' task performance. Wilson
(1985; also see
Cole, 1981) predicted that
aggressive interactions could persist among workers of derived eusocial
species, even in contexts where the workers are sterile or nearly so. The data
in this study suggest that this was the case in P. occidentalis.
Biting was independent of ovary development, but was linked to foraging
behavior. Workers departed their nests after being bitten, and in nearly all
cases the departing workers began foraging. Recipient workers were more likely
to forage, and rates of being bitten were correlated with foraging rates.
Therefore, biting appeared both to initiate and to maintain foraging
activity.
Adult P. occidentalis workers exhibit strong temporal polyethism,
shifting from in-nest to on-nest, and finally to off-nest tasks as they age
(Jeanne et al., 1988;
O'Donnell and Jeanne, 1993).
The developmental onset of foraging may be stimulated in workers that receive
biting. Montagner (1966)
proposed a similar function for intense biting interactions (mauling) among
yellow jacket wasp workers (Vespula).
At the colony level, biting interactions could function both to maintain
P. occidentalis forager activity, and to adjust overall foraging
rates in response to changes in colony needs. If this is the case, then
experimentally decreasing the rate of biting interactions (e.g., by removing
the most active biters; O'Donnell,
1998a) would lead to a decrease in the rate of foraging.
Conversely, if biting interactions communicate information about colony needs
for task performance, then biting rates should change in response to
contingencies imposed on the colony. Experimental alterations of colony needs
for certain tasks, such as nest damage manipulations
(Jeanne, 1996;
O'Donnell and Jeanne, 1990),
should elicit effects on biting interactions.
The evolution of worker interactions and task performance
As eusocial insects evolve larger colony sizes, individual workers'
opportunities for direct reproduction decrease
(Bourke, 1999), yet division of
labor must still be achieved. As average colony size increases over
evolutionary time, worker interactions may become increasingly independent of
reproductive competition. The recent discovery of anarchistic honeybee
workers, which lay eggs in the presence of the queen but do not elicit
aggression, illustrates that worker interactions and reproduction can be
decoupled (Oldroyd et al.,
1999). Worker contact interactions in derived, large colony
species are likely to evolve from dominance interactions over egg-laying
rights in ancestral species. These interactions can become increasingly
ritualized over evolutionary time (Wilson,
1985).
In highly derived eusocial taxa, worker contact interactions may give
little indication of aggression or conflict, but retain the function of
affecting division of labor. The dorsoventral abdominal vibration or shaking
dance of honey bees (Apis mellifera) induces foraging behavior in
recipient workers (Schneider et al.,
1986; Seeley et al.,
1998). The shaking dance may represent ritualized aggressive
behavior, derived from dominance interactions that were ancestrally similar to
those of worker bumblebees (van Doorn,
1987). In some ants, brief contacts with nest mates have been
shown influence workers' task performance
(Gordon and Mehdiabadi, 1999;
Gordon et al., 1993). I propose
that ritualized contact interactions will continue to function in organizing
labor as larger, more complex societies evolve from smaller, simpler ones.
Support for this hypothesis requires demonstrating that worker contact
interactions influence task performance, but that they depend less on
variation in workers' capacity for direct reproduction in more derived
eusocial species. Within a eusocial clade, worker interactions will become
less associated with direct competition as colony size, social complexity, and
reproductive caste separation increase.
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ACKNOWLEDGEMENTS |
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Thanks to Adam Smith, Andy Bouwma, and Robert Jeanne for assistance in the field. The Hagnauer family was generous with hospitality and logistical support in Costa Rica. Daniel Markiewicz, Meredith Klacking, Melissa Nakanishi, and Tina Stremick assisted with dissections. David Westneat and two anonymous reviewers made helpful comments on earlier versions of the article. Research was conducted under permits from the Costa Rican government obtained with the help of the Organization for Tropical Studies. Financial support was provided by a U.S. National Science Foundation Grant, IBN-9904885.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Bourke AFG, 1999. Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12: 245-257.[ISI]
Brown JL, Brown ER, Sedransk J, Ritter S, 1997. Dominance, age, and reproductivesuccess in a complex society: a long-term study of the Mexican Jay. Auk 114: 279-286.
Cole BJ, 1981. Dominance hierarchies in
Leptothorax ants. Science 212:
83-84.
Downing HA, Jeanne RL, 1985. Communication of status in the social wasp Polistes fuscatus (Hymenoptera: Vespidae). Z Tierpsychol 67: 78-96.
Drea CM, Wallen K, 1999. Low-status monkeys
"play dumb" when learning in mixed social groups. Proc Natl
Acad Sci USA 96:
12965-12969.
Gordon DM, Mehdiabadi NJ, 1999. Encounter rate and task allocation in harvester ants. Behav Ecol Sociobiol 45: 370-377.
Gordon DM, Paul RE, Thorpe K, 1993. What is the function of encounter patterns in ant colonies? Anim Behav 45: 1083-1100.
Hawley PH, 1999. The ontogenesis of social dominance: a strategy-based evolutionary perspective. Devel Rev 19: 97-132.[ISI]
Heinz J, Oberstadt B, 1999. Worker age, size and social status in queenless colonies of the ant Leptothorax gredleri. Anim Behav 58: 751-759.[ISI][Medline]
Hillesheim E, Koeniger N, Moritz RFA, 1989. Colony performance in honeybees (Apis mellifera capensis Esch.) depends on the proportion of subordinate and dominant workers. Behav Ecol Sociobiol 24: 291-296.
Hunt JH, Jeanne RL, Baker I, Grogan D, 1987. Nutrient dynamics of a swarm-founding social wasp species, Polybia occidentalis (Hymenoptera: Vespidae). Ethology 75: 291-305.
Jacobs DS, Jarvis JUM, 1996. No evidence for the work-conflict hypothesis in the eusocial naked mole-rat (Heterocephalus glaber). Behav Ecol Sociobiol 39: 401-409.
Jeanne RL, 1986a. The evolution of the organization of work in social insects. Monit Zool Ital (NS) 20: 119-133.
Jeanne RL, 1986b. The organization of work in Polybia occidentalis: costs and benefits of specialization in a social wasp. Behav Ecol Sociobiol 19: 333-341.[ISI]
Jeanne RL, 1991. Polyethism. In: The social biology of wasps (Ross KG, Matthews RW, eds). Ithaca: Cornell University Press; 389-425.
Jeanne RL, 1996. Regulation of nest construction behaviour in Polybia occidentalis. Anim Behav 52: 473-488.
Jeanne RL, Downing HA, Post DC, 1988. Age polyethism and individual variation in Polybia occidentalis, an advanced eusocial wasp. In: Interindividual behavioral variability in social insects (Jeanne RL, ed). Boulder: Westview Press; 323-357.
Kaufman S, 1991. The sciences of complexity and "origins of order." PSA 1990 2: 299-322.
Montagner H, 1966. Le mechanisme et les consequences des comportaments trophallactiquez chez les guepes du genre Vespa. C R Acad Sci Paris 263: 785-787.
Nicolis G, Prigogine I, 1977. Self-organization in nonequilibrium systems. New York: John Wiley & Sons.
O'Donnell S, 1996. RAPD markers suggest genotypic effects on forager specialization in a eusocial wasp. Behav Ecol Sociobiol 38: 83-88.
O'Donnell S, 1998a. Effects of experimental forager removals on division of labour in the primitively eusocial wasp Polistes instabilis (Hymenoptera: Vespidae). Behaviour 135: 173-193.
O'Donnell S, 1998b. Genetic effects on task performance, but not on age polyethism, in a swarm-founding eusocial wasp. Anim Behav 55: 417-426.[ISI][Medline]
O'Donnell S, in press. Worker age, ovary development, and task performance in the swarm-founding wasp Polybia occidentalis (Hymenoptera: vespidae). J Insect Behav.
O'Donnell S, Jeanne RL, 1990. Forager specialization and the control of nest repair in Polybia occidentalis Olivier (Hymenoptera: Vespidae). Behav Ecol Sociobiol 27: 359-364.
O'Donnell S, Jeanne RL, 1992. Lifelong patterns of forager behaviour in a tropical swarm-founding wasp: effects of specialization and activity level on longevity. Anim Behav 44: 1021-1027.
O'Donnell S, Jeanne RL, 1993. Methoprene accelerates age polyethism in workers of a social wasp (Polybia occidentalis). Physiol Entomol 18: 189-194.
O'Donnell S, Jeanne RL, 1995. The roles of body size and dominance in division of labor among workers of the eusocial wasp Polybia occidentalis (Olivier) (Hymenoptera: Vespidae). J Kans Ent Soc 68: 43-50.
Oldroyd BP, Halling L, Rinderer TE, 1999. Development and behaviour of anarchistic honeybees. Proc R Soc Lond B 266: 1875-1878.
Powell S, Tschinkel WR, 1999. Ritualized conflict in Odontomachus brunneus and the generation of interaction-based task allocation: a new organizational mechanism in ants. Anim Behav 58: 965-972.[ISI][Medline]
Queller DC, Strassmann JE, Hughes CR, 1988. Genetic
relatedness in colonies of tropical wasps with multiple queens.
Science 242:
1155-1157.
Ratnieks FLW, 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132: 217-236.[ISI]
Ratnieks FLW, 1993. Egg-laying, egg-removal, and ovary development by workers in queenright honey bee colonies. Behav Ecol Sociobiol 32: 191-198.
Reeve HK, Gamboa GJ, 1987. Queen regulation of worker foraging in paper wasps: a social feedback control system (Polistes fuscatus, Hymenoptera: Vespidae). Behaviour 102: 147-167.
Richards OW, 1978. The social wasps of the Americas. London: British Museum (Natural History).
Robinson GE, Page RE Jr, Strambi C, Strambi A, 1989.
Hormonal and genetic control of behavioral integration in honey bee colonies.
Science 246:
109-112.
Schneider SS, Stamps JA, Gary NE, 1986. The vibration dance of the honey bee. I. Communication regulating foraging on two time scales. Anim Behav 34: 377-385.
Seeley TD, 1986. Social foraging by honey bees: how colonies allocate foragers among patches of flowers. Behav Ecol Sociobiol 19: 343-354.
Seeley TD, 1989. The honey bee colony as a superorganism. Am Sci 77: 546-553.
Seeley TD, Weidenmuller A, Kuhnholz S, 1998. The shaking signal of the honey bee informs workers to prepare for greater activity. Ethology 104: 10-26.
Sokal RR, Rohlf FJ, 1981. Biometry, 2nd ed. New York: WH. Freeman.
Strassmann JE, Klingler CJ, Arevalo E, Zacchi F, Husain A, Williams J, Seppa P, Queller DC, 1997. Absence of within-colony kin discrimination in behavioral interactions of swarm-founding wasps. Proc R Soc Lond B 264: 1565-1570.
van Doorn A, 1987. Investigations into the regulation of dominance behaviour and the division of labor in bumblebee colonies (Bombus terrestris). Neth J Zool 37: 255-276.
West-Eberhard MJ, 1997. The establishment of reproductive dominance in social wasp colonies. Proc 8th Int Cong IUSSI 164-168.
West-Eberhard MJ, 1981. Intragroup selection and the evolution of insect societies. In: Natural selection and social behavior: recent research and new theory (Alexander RD, Tinkle DW, eds). New York: Chiron Press; 3-17.
Wilson EO, 1985. The sociogenesis of insect colonies.
Science 228:
1489-1495.
Wilson EO, 1990. Success and dominance in ecosystems: the case of the social insects. Oldendorf/Luhe: Ecology Institute.
Wilson EO, Hölldobler B, 1988. Dense heterarchies and mass communication as the basis of organization in ant colonies. Trends Ecol Evol 3: 65-68.
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