Anim. Behav., 1992,44,1021-1027
Lifelong patterns of forager behaviour in a tropical swarm-founding wasp: effects of specialization and activity level on longevity
SEAN O'DONNELL & ROBERT L. JEANNE Department ofEntomology, University of Wisconsin, Madison, W153706, U.S.A.
(Received 22 November 1991; initial acceptance 30 January 1992; final acceptance 20 February 1992; MS. number: A6223)
Abstract. The relationships between foraging tenure and specialization on materials, and foraging tenure and foraging activity were measured for marked, known-age workers ofthe social wasp Polybia occidentalis. The purpose ofthe study was to assess differences in cost to foragers, in terms ofrisk ofmortality, associated with material specializations and activity level, and determine whether ontogenetic changes in forager beha viour reflect these differences in cost, such that more risky patterns of behaviour are postponed until later in adult life. Polybia occidentalis workers terminated foraging at an average of5·9 days after their first trip, independent of their age at first foraging, suggesting that this task entailed a high risk of mortality. Lifetime foraging activity was calculated as foraging rate (mean number oftrips per hour), foraging effort (mean number of time-weighted trips per hour), and as the proportion of observation days that an individual was active during her foraging tenure. Foraging tenure was not related to foraging rate or effort, but had a strong negative relationship with the proportion ofobservation days during which an individual foraged. By the latter measure, risk of mortality increased with foraging activity. The length of foraging tenure was negatively correlated with the proportion of foraging effort devoted to food materials (nectar and insect prey), supporting the hypothesis that gathering food was riskier than gathering nest materials (water and wood pulp). Foragers that switched between food and nest materials exhibited no tendency to specialize on nest materials first and therefore foraging for riskier materials was not always performed later in adult life. These results are discussed in terms of possible factors regulating task performances at the individual level in social insects.
Recently some authors have suggested that behav in which foragers have been found to specialize ioural specialization by workers increases efficiency on materials for longer periods (Forsyth 1978; and reliability at the colony level in eusocial insects Strassmann et al. 1984; Post et al. 1988), foraging (Jeanne 1986; Franks 1987) and therefore increases may be subdivided into distinct roles based on colony fitness. However, in some eusocial insects, individual material specializations, workers that adopt certain behavioural roles have Few studies have addressed the possibility of been shown to suffer high costs or risks. Foraging, differential costs to foragers that specialize on in particular, entails a high risk of mortality rela different materials (Strassmann et al. 1984; Post tive to other roles (Sakagami & Fukuda 1968; Porter et al. 1988). The cost we consider is the likelihood & Jorgensen 1981; Schmid-Hempel & Schmid of mortality, hereafter called risk, associated with Hempel 1984; Strassmann 1985). We examined the foraging for particular materials. Within colonies, notion of behaviour-specific costs to workers foragers also frequently differ in rate of work through studies offoraging in the advanced eusocial or activity level, and several studies have sought wasp Polybia occidentalis. a correlation between worker longevity and Even within behavioural roles, specialization foraging activity (Schmid-Hempel & Wolf 1988; by eusocial hymenopteran workers can be striking. Calabi & Porter 1989; Wolf & Schmid-Hempel In some species, forager specializations have 1989). The goal of this study was to learn whether been shown to persist for at least several days certain material specializations or high activity (Heinrich 1976; Rissing 1981; Schmid-Hemr.~l levels involved greater risks for P. occidentalis 1984; O'Donnell & Jeanne 1990). In other species, foragers.
0003-3472/92/121021 +07 $08,00/0 © 1992 The Association for the Study ofAnimal Behaviour 1021 ~;"~ 1022 Animal Behaviour, 44, 6
....~ METHODS 2 days. Observation periods at each colony lasted 20-90 min (X= 73 min) in the morning, and 30 Study Site and Colonies 90 min (X= 61 min) in the afternoon. Two colonies The study was conducted between 26 June and 8 were observed each day. No observations were made August 1989 (rainy season) near the town ofCafias during periods of heavy rain. All occurrences of in Guanacaste Province, Costa Rica. The study site marked forager arrivals were noted by recording is a mixture of gallery forest, seasonally deciduous time oflanding and material carried. forest, and open pastures with scattered shrubs. Polybia occidentalis foragers gather fourmaterials. Polybia occidentalis nests are most abundant in the Nectar and insect prey are referred to collectively as last of these habitats, where many colonies nest 'food materials'. Wood pulp and water, used in nest within I· 5 m ofthe ground. A more detailed descrip construction and maintenance, are referred to as tion of the site is found in Daubenmire (1972). We 'nest materials'. Methods used to identify materials studied four colonies ofmoderate size (adult popu carried by foragers are detailed in Hunt et al. (1987). lation of several hundred individuals), with all In some cases, returning foragers entered the nest or brood stages present, and located within a I-ha left again before their load could be identified; when area. this occurred we recorded material as unknown. Two ofthecolonies (numbers 4 and 5) wereexper Trips made by foragers carrying unknown material imentally manipulated periodically during the study were not included in our analysis. by removing a portion of the outer nest envelope. The four colonies were collected after the termin The effects of these manipulations have been pub ation of behavioural observations, and all adult lished elsewhere (O'Donnell & Jeanne 1992); the wasps were placed in Kahle's fixative solution or manipulations had no significant effect on the frozen. Collections were performed after sunset to behavioural variables addressed here or on ensure that all workers were captured; no workers longevity and will not be considered further. were observed returning to the nest sites the morning following collections.
Introduction of Known-age Workers Data Analysis Combs containing pupae were removed from two P. occidentalis nests located more than 100 m We defined foraging tenure as the number of from the nearest observation colony and incubated days between a worker's first and last observed for at ambient temperature in the laboratory. These aging trips. This estimate represents a lower bound combs served as sources of known-age workers for on true foraging tenure, since workers could have introduction into the observation colonies. Adult foraged on days preceding or following those on wasps eclosing from the source combs were indi which they were observed. vidually marked with paint on the thorax and were In an effort to analyse exposure to risk, we exam released within 24 h ofeclosion into the observation ined two attributes offoraging behaviour measured colonies. Cohorts of known-age wasps were intro for the duration of individual foraging tenures: duced at2- to 5-day intervals from 26 June to 9 July. activity level and material specialization. Forager The total numbers of known-age workers and activity level was quantified in three ways: (I) cohorts added were: Colony 4: 88 workers in six Foraging rate: the mean number of trips made per cohorts; Colony 5: 105 workers in seven cohorts; hour ofobservation, under the assumption that risk Colony 10: 80 workers in five cohorts; Colony 13: accumulates incrementally with each trip, regard 105 workers in seven cohorts (mean cohortsize = 15, less of trip duration and of what material was range = 8-20). Introduced workers were accepted collected. (2) Foraging effort: each trip for a given into the worker populations of the observation material was weighted by a factor equal to the mean colonies. time to collect that material divided by the mean time to collect water, which required the least time. This activity measure was used under the assump Behavioural Observations tion that risk of mortality bears some relation to Behavioural data were collected between 28 how long the forager spends in the field. Mean time June and 8 August 1989. With few exceptions we spent in the field on a foraging trip differed widely collected data from each observation colony every among the four materials (O'Donnell & Jeanne O'Donnell & Jeanne: Forager behaviour andlongevity in wasps 1023
1990). (3) Proportion ofdays that an individual was tenure did not vary with the age at which workers observed foraging during her tenure. The final first foraged (univariate log-rank test, X2=0·58, measure allowed us to assess the effect of long P>0·25). periods of inactivity on forager longevity. We used life table methods of survival analysis Relationship Between Activity Level and Foraging (SAS Institute 1985) to study the effects of material Tenure specialization and activity level on the length of Survivorship statistics for foragers were calcu foraging tenure. By definition, behavioural attri lated at 5-day intervals. Survival analysis of forag butes associated with shorter foraging tenures ing tenure showed no significant difference among involved greater risk. We assumed that the colonies (log-rank test for equality among colonies, observed termination of foraging was due to mor d/=3, X2=3·58, P>0·3). The risk of mortality tality, rather than to changes in worker behaviour increased over foraging tenure, since the hazard such as switching to other tasks. Therefore marked function, the probability that a worker last foraged workers present when the colonies were collected in a given age interval, rose with the number ofdays were presumed not to have completed their forag since first foraging (Fig. 3). Foraging tenure was not ing careers and were censored in the survival analy significantly associated with foraging effort (mean sis. Censoring permits inclusion in the survival weighted trips per observation hour; univariate log analysis of individuals whose true longevity is rank test, d/= I,X2= I '39,P>0'IO)orwithforaging unknown because observations were terminated rate (the unweighted number of foraging trips per before their demise (for further discussion see SAS observation hour; univariate log-rank test, d/= I, Institute 1985). The log-rank test was used to assess X2 =4-4, P>O·IO). However, the proportion of differences in survivorship distributions among observation days during a forager's tenure on which colonies and to test for effects of behavioural vari she was observed foraging was negatively associated ables on forager longevity. This test is appropriate with the length of her tenure (workers with tenures when examining censored data (D. Heisey, per greater than 3 days, univariate log-rank test, d/= I, sonal communication). The hazard function, the X2=8'14, P<0·005). probability that a worker last foraged in a given age interval, was used to examine changes in risk of Specialization on Materials mortality over time. Foraging for food materials was riskier than for aging for nest materials: considering all foragers, RESULTS tenure was negatively correlated with the proportion of foraging effort (weighted trips) devoted to food Approximately half of the workers (N= 191) added (Spearman correlation, r= -0,39, P
Table I. Fates of known-age marked workers added to P. occidentalis observation colonies
Colony
4 5 10 13 Total
Number added 88 105 80 105 378 NumberC%)*thatforaged 45 40 45 61 191 (51 %) (38%) (56%) (58%) (51%) Ofthose foraging, number (%) that foraged for Food materials only 37 25 36 43 141 (82%) (63%) (80%) (70%) (74%) Food and nest materials 5 10 I 8 24 (11%) (25%) (2%) (13%) (13%) Nest materials only I I 2 4 8 (2%) (3%) (4%) (7%) (4%) Total gathering known materials 43 36 39 55 173 (96%) (90%) (87%) (90%) (91%) Unknown materials only 2 4 6 6 18 (4%) (10%) (13%) (10%) (9%) Number surviving to collection 21 16 22 27 86 Number not recorded (never seen)t 36 56 27 33 152
"Percentage of wasps added. tWasps that never foraged and were not present when the colony was collected. Their behavioural histories were unknown because only foraging was recorded; some of these workers may have died soon after marking and introduction.
30 30
It! '" ~ '" 20 '"0> ~ .g~ 20 '0 r- r- '" C £ 0> c'" '" 10 E'" '"~ 10 a.'" ~ a.'"
0 InoOrLD o 4 8 12 16 2 4 6 8 10 12 14 16 18 20 22 Foraging effort (weighted trips/h) Foraging tenure (days) Figure 1. Distribution of total lifetime foraging effort for Figure 2. Distribution of foraging tenure, the number of P. occidenlalis workers from four colonies. To calculate days elapsed from the first to the last time each individual effort, the number of trips for each material was multi was observed foraging, for P. occidentalis. plied by the average trip duration divided by the aver age duration of a trip to collect water, the most rapidly collected material. to obtain materials. As has been reported for was gathered first by these individuals did not other eusocial Hymenoptera (Sakagami & Fukuda differ from equiprobability (binomial test, P> 0,15, 1968; Porter & Jorgensen 1981; Schmid-Hempel N = 24). There were 14 individuals (58 % of24) that & Schmid-Hempel 1984), most P.occidentalis switched types more than once. workers disappeared soon after the onset of forag ing. Furthermore, the duration of foraging tenure DISCUSSION did not depend on the age at which a worker began foraging; once they entered the forager role, Foraging behaviour is especially risky for social workers were exposed to high risk of mortality. insect workers because it involves leaving the nest Predators on foraging P. occidentalis observed at O'Donnell & Jeanne: Forager behaviour and longevity in wasps 1025
"0 Relationship Between Activity Level and Longevity > .~ 0·40 Foraging is one of the few tasks that involve .5 u <1> flight, which is both energetically expensive and E'" 0·30 exposes workers to increased risk of predation. .E High foraging activity might therefore be expected 1;; .'2 0·20 to have a negative impact on longevity. When Cl. measured as the proportion of days a worker for <1> 65 aged during her tenure, activity level was negatively "0" 0·10 " correlated with the duration of foraging tenure in 'E ::l P. occidentalis. Schmid-Hempel & Wolf(1988) also 0 :;:: 0 5 10 15 20 found a negative relationship between the proportion Days since first foraged oftime spent active and longevity for foraging honey Figure 3. Mean (±SE) hazard function value, the prob bee workers. However, work rate (foraging rate ability oflast foraging in a given 5-day age interval, based and foraging effort) did not vary significantly with on the number of days elapsed since first foraging for foraging tenure in P. occidentalis. Results from P. occidentalis (no standard error could be calculated for other research relating work level to longevity in the last interval since all foraging tenures terminated by this point). Numbers on graph indicate how many workers insects are inconsistent. Studies on the fire ant last foraged in each age-interval; a total of 51 wasps were Solenopsis invicta (Calabi & Porter 1989) and diverse censored in the survival analysis (see Materials and non-social insects (Collatz & Sohal 1986) support Methods section). the notion of a trade-off between high foraging activity and longevity. Wolf & Schmid-Hempel our study site are many, including dragonflies, (1989) noted a decrease in life span for artificially mantids, robber flies, predaceous Hemiptera, and weighted honey bees, but only the individuals spiders (Forsyth 1978; personal observations). receiving the heaviest weights (23 mg) were affected. Schmid-Hempel & Wolf(l988) found that longevity Forager Longevity ofhoney bee workers was notaffected by experimen tally induced changes in foraging rate and time away The mean worker life span ofP. occidentalis (X= 24·0 days), measured during the ergonomic or from the nest. There may be advantages that accrue growth phase ofcolony development, falls between with foraging experience in P. occidentalisand other the shorter life spans (X= 17·9 days, three species) species that offset the increased costs ofhigh activity of highly eusocial vespine wasps and the longer life level; these advantages could obscure a negative spans (X=27·5 days, five species) of primitively relationship between activity level and longevity. eusocial polistine wasps (reviewed by Strassmann Forexample, experienced foragers may be less likely 1985). Foraging tenures often vary widely among to lose their way, or better able to a void predators by individuals, but are generally short in social insects. using direct flight routes. Such factors may explain the lack Porter & Jorgensen (1981) found a life expectancy of a predictable negative relationship of 14 days for Pogonomyrmex ant foragers; forager between activity level and longevity in social insects. life expectancy was 6·1 days in the desert ant Cataglyphis bicolor (Schmid-Hempel & Schmid Long-term Specialization on Materials and Hempel 1984), similar to the value of 5·9 days Longevity obtained for P. occidentalis. The increased risk of mortality with time after initiation of foraging The earlier finding that some P. occidentalis may be due to an elevated effect of senescence on foragers exhibit lifelong specialization or 'fixation' P. occidentalis foragers with more time spent forag on materials (Forsyth 1978) was supported in this ing. In this context it is interesting to note again that study. However, since some foragers collected both foraging tenure did not decrease as age of first for food and nest materials, fixation was not universal. aging increased, suggesting that mortality is not Long-term specialization by hymenopteran workers fixed at a certain age. It is possible that partici can take a variety offorms. Gordon (1984) measured pation in foraging involves some physiological strong task fidelity of approximately 1 month cost, manifested as accelerating senescence, in duration in harvester ant, Pogonomyrmex badius, addition to the hazards ofpredation or getting lost. exterior workers. Sommeijer et al. (1983) noted 1026 Animal Behaviour, 44, 6
15r------~ • • • • • • • • . ". • • o 10 20 30 Foraging effort for food materials (weighted trips/h) Figure 4. Total lifetime foraging effort devoted to nest materials plotted against lifetime effort devoted to food materials for the 24 workers that made trips for both types (foraging effort = number of trips for each material weighted by the ratio between mean foraging time for that material and for water). The dashed line indicates values expected ifequal effort was devoted to both types ofmaterials. specialization (nectar versus pollen) by foragers of et al. 1983; G. Robinson, personal communi the stingless bee Melipona favosa; 75% of 85 cation), but in these cases it was not known whether observed foragers collected only one material in the materials gathered differed in risk to foragers. their lifetimes. In some social insects, tasks usually Our data are consistent with the hypothesis that considered together as parts of a behavioural role selection to maximize worker longevity has shaped such as foraging may actually represent distinct age-based task sequences on a coarse scale because roles in themselves. foraging, which is risky behaviour, is the last role Specialization on food as opposed to nest materials performed (Jeanne et al. 1988). The hypothesis was was correlated with decreased foraging tenure in not supported on the finer scale of within-role P. occidentalis. A comparable result was found in specialization. Our results suggest that foraging in the primitively eusocial wasp Polistes exclamans, P. occidentalis comprises two roles, both of which where worker longevity was negatively correlated are based on material specialization. with foraging effort devoted to prey and pulp That some P.occidentalis foragers are more (Strassmann et al. 1984). Similarly, Gordon & flexible, gathering both food and nest materials, Holldobler (1987) found that Pogonomyrinex ant raises the question of how material specializations workers engaged in different exterior tasks, on are maintained at the individual level. Why do some which they specialized for long periods (Gordon individuals enter and remain in specializations on 1984), were at different risk. the more risky materials? Reeve & Gamboa (1987) showed that dominance interactions, especially with the queen, directly and indirectly induced foraging Ontogenetic Sequenee of Specializations behaviour in P.fuscatus. Dominance interactions Ifcolony-level selection to maximize worker life with workers have been shown to bring about span is strong, risky tasks should be performed later worker- versus queen-like behaviour in Metapolybia in life by social insect workers (Jeanne 1986). The aztecoides, a swarm-founding wasp (West -Eberhard lack ofa consistent ontogenetic sequence ofspecial 1977). The freq uency ofdirect reproduction by active izations on materials by P. occidentalis foragers workers, in this case foragers, in P. occidentalis is does not match the prediction that the foraging role unknown. It is possible that subordinate individ should be divided into a set of specializations per uals, or those with the lowest opportunity for direct formed in sequence as a worker ages. Rather, most reproduction, are compelled to engage in riskier foragers gathered only one material type, and tasks (West-Eberhard 1981) such as food foraging. foragers that switched between food and nest If this is the case, detailed studies relating ovary materials showed no consistent pattern with respect development or related physiological character to which type was gathered first. Stingless bee and istics with worker behaviour should yield insight honey bee foragers are similarly inconsistent in their into the mechanisms governing task specialization sequence of material specializations (Sommeijer in eusocial wasps. O'Donnell & Jeanne: Forager behaviour and longevity in wasps 1027
ACKNOWLEDGMENTS O'Donnell, S. &Jeanne, R. L. 1990. F oragerspecialization and the control of nest repair in Polybia occidentalis Olivier (Hymenoptera: Vespidae), a tropical swarm We thank Werner and Lilly Hagnauer for their founding wasp. Behav. Bcol. Sociobio/., 27, 359-364. ongoing support of our research, especially for O'Donnell, S. & Jeanne, R. L. 1992. The effects ofcolony permission to work on their land. Larry Phelps pro characteristics on longevity and foraging behavior of vided valuable assistance in the field. Jose Arturo individual wasps (Polybia occidentalis, Hymenoptera: Vespidae). insects Soc., 39, 73-80. Leon and the Costa Rican office of the Organiz Porter, S. D. & Jorgensen, C. D. 1981. Foragers of the ation for Tropical Studies were helpful in obtaining harvester ant Pogonomyrmex owyheei: a disposable field supplies. Dennis Heisey's advice on statistical caste? Behav. Bcol. Sociobiol., 9, 247-256. analysis of survivorship data was greatly appreci Post, D. c., Jeanne, R. L. & Erickson, E. H. Jr. 1988. ated. Thanks to Susan Bulova, Emilia Martins, Variation in behavior among workers ofthe primitively social wasp PolistesJuscatus variatus. In: Interindividual Joan Strassmann and an anonymous referee for Behavioral Variability in Social insects (Ed. by R. L. reading and commenting on earlier versions of the Jeanne), pp. 283-319. Boulder, Colorado: Westview manuscript. Our research was funded by NSF grant Press. BNS-85l7519, R.L.J. principal investigator; and Reeve, H. K. & Gamboa, G. J. 1987. Queen regulation of worker foraging in paper wasps: a social feedback the University of Wisconsin College ofAgriculture control system. Behavior, 102, 147-167. and Life Sciences. Rissing, S. W. 1981. Foraging specializations of indi vidual seed-harvester ants. Behav. Ecol. Sociobiol., 9, 149-152. Sakagami, S. F. & Fukuda, H. 1968. Life tables for REFERENCES worker honeybees. Res. Pop. Ecol., 10, 127-139. SAS Institute. 1985. SAS Users Guide: Statistics. Version Calabi, P. & Porter, S. D. 1989. Worker longevity in the 5 edn. Cary, North Carolina: SAS Institute. fire ant Solenopsis invieta: ergonomic considerations of Schmid-Hempel, P. 1984. Individually different foraging correlations between temperature, size and metabolic methods in the desert ant Cataglyphis bicolor rates. J. insect Physiol., 35,643-649. (Hymenoptera, Formicidae). Behav. Ecol. Sociobiol., Collatz, K. G. & Sohal R. S. (Eds) 1986. Insect Aging. 14,263-271. New York: Springer Verlag. Schmid-Hempel, P. & Schmid-Hempel, R. 1984. Life Daubenmire, R. 1972. Phenologyand other characteristics duration and turnover of foragers in the ant Cata of tropical semi-deciduous forest in North-Western glyph!s bicolor (Hymenoptera, Formicidae). insectes Costa Rica. J. Bcol., 60,147-170. Soc., 31, 345-360. Forsyth, A. B. 1978. Studies on the behavioral ecology Schmid-Hempel, P. & Wolf, T. 1988. Foraging effort and of polygnous social wasps. Ph.D. thesis, Harvard life span ofworkers in a social insect. J. Anim. Ecol., 57, University, Cambridge, Massachusetts. 509-522. Franks, N. R. 1987. The organization ofworking teams in Sommeijer, M. J., De Rooy, G. A., Punt, W. & De social insects. Trends Ecol. Evo!., 2, 72-75. Bruijn, L. L. M. 1983. A comparative study offoraging Gordon, D. M. 1984. The persistence ofrole in workers of behavior and pollen resources ofvarious stingless bees the harvester ant, Pogonomyrmex badius. Psyche, 91, (Hym., Meliponinae) and honeybees (Hym., Apinae) in 251-265. Trinidad, West Indies. Apido!., 14,205-224. Gordon, D. M. &Holldobler, B. 1987.Worker longevity in Strassmann, 1. E. 1985. Worker mortality and the harvester ants (Pogonomyrmex). Psyche, 94,341-346. evolution ofcastes in the social wasp Polistesexclamans. Heinrich, B. 1976. The foraging specializations of indi Insectes soc., 32, 275--285. vidual bumblebees. Ecol. Monogr., 46,105-128. Strassmann, J. E., Meyer, D. C. & Matlock, R. L. 1984. Hunt, J. H., Jeanne, R. L., Baker, I. & Grogan, D. E. 1987. Behavioral castes in the social wasp, Polistes exclamans Nutrient dynamics of a swarm-founding social wasp (Hymenoptera: Vespidae). Sociobiology, 8, 211-224. species, Polybia occidentalis (Hymenoptera: Vespidae). West-Eberhard, M. J. 1977. The establishment ofrepro Ethology, 75, 291-305. ductive dominance in social wasp colonies. Proceedings Jeanne, R. L. 1986. The evolution of the organization of oj the VllI Congress on International Union Study oj work in social insects. Monitore Zoologieo italiano Social insects, pp. 223-227. N.S.,20,119-133. West-Eberhard, M. J. 1981. Intragroup selection and the Jeanne, R. L., Downing, H. A. & Post, D. C. 1988. evolution of insect societies. In: Natural Selection and Age polyethism and individual variation in Polybia Social Behavior (Ed. by R. D. Alexander & D. W. occidentalis, an advanced eusocial wasp. In: inter Tinkle), pp. 3·\7. New York: Chiron Press. individual behavioral variability in social insects (Ed. Wolf, T. J. & Schmid-Hempel, P. 1989. Extra loads and by R. L. Jeanne), pp. 323-357. Boulder, Colorado: foraging life span in honeybee workers. J. Anim. Eco!., Westview Press. 58,943-954.