Ecological Entomology (2000) 25, 262±266

Bene®ts of communal breeding in burying : a ®eld experiment

1,2 1 ANNE-KATRIN EGGERT andSCOTT K. SAKALUK 1Behavior, Ecology, Evolution and Systematics Section, Department of Biological Sciences, Illinois State University, U.S.A. and 2Institut fuÈr Zoologie der Albert-Ludwigs-UniversitaÈt, Freiburg, Germany

Abstract. 1. The ultimate causes of communal breeding and joint parental care in various species of Nicrophorus burying beetles have not been resolved satisfactorily. One hypothesis suggests that females remain on the carcass for extended periods of time because joint defence affords them improved probabilities of retaining the carcass successfullyin the face of intense competition from intra- generic competitors. 2. In a ®eld experiment designed to test this hypothesis in N. defodiens (Mannerheim), breeding associations of two females and a male were no more successful at retaining their carcass than were monogamous pairs, lending no support to the hypothesis. 3. Intra-generic intruders that usurped already-buried carcasses were typically much larger than the original residents. 4. The bodysize of original residents affected both the burial depth and the probabilityof a takeover. Larger beetles buried the carcass deeper and were more likelyto retain possession of the carcass. Group composition also did not affect the depth at which carcasses were buried. 5. Severe and even fatal injuries incurred bysome residents indicated the occurrence of violent and damaging ®ghts between competitors over carcasses in the ®eld. Key words. Burying beetles, communal breeding, competition, co-operation, nest defence, Nicrophorus defodiens.

Introduction their developing young (Pukowski, 1933). Carcasses are frequentlydiscovered bymultiple individuals of both sexes Communal breeding occurs in a varietyof vertebrate and but aggressive interactions typically lead to the monopolisation species. In manysuch breeding associations, reproduc- of the carcass bya single male±female pair. Communal tive skew (Keller & Vargo, 1993; Reeve & Ratnieks, 1993) is breeding occurs, however, on carcasses that are large for the high, involving reproductive suppression of some individuals respective species. Communal breeding in these instances or even acts of infanticide (e.g. see Hrdy& Hausfater, 1984). encompasses two distinct behavioural components: tolerant Bene®ts associated with communal breeding are frequently behaviour towards individuals of the same sex and species less obvious, at least for some of the individuals involved. during carcass burial and preparation; and extended presence Thus, relatedness to the dominant breeders or environmental on the carcass bytwo or more females that mayfeed the brood constraints limiting singular breeding attempts of subordinate jointlyand even simultaneously(Eggert & Mu Èller, 1997). group members have been invoked as adaptive explanations When burying beetles reproduce in polygynous associations, for communal breeding (e.g. see Brown, 1987). reproductive output per female has been found to be Burying beetles (Coleoptera: : Nicrophorus) inter consistentlylower than in monogamous pairs in ®eld and small vertebrate carcasses that serve as the sole food source for laboratorystudies conducted byvarious researchers ( N. vespilloides Herbst: MuÈller et al., 1990; Eggert & MuÈller, Correspondence: A. Eggert, Behavior, Ecology, Evolution and 1992; N. defodiens: Trumbo & Fiore, 1994; N. tomentosus Systematics Section, Department of Biological Sciences, Illinois State Weber: Scott, 1994a, 1997). This reduction in individual University, Normal, IL 61790-4120, U.S.A. E-mail: [email protected] reproductive success even on large carcasses raises the obvious

262 # 2000 Blackwell Science Ltd Communal breeding in burying beetles 263 question of how selection has maintained communal breeding hammered into the soil ¯ush to the top of the surrounding behaviour over evolutionarytime. One possibilityis that forest litter. The carcass and the experimental beetles were communal breeding reduces the probabilityof takeovers of the placed gentlyon top of the soil and prevented from escaping carcass byintra- and inter-speci®c competitors, a bene®t that bysecuring an inverted metal strainer (mesh size 2 mm) so that might ultimatelyrender the expected reproductive output for it ®tted snuglyaround the upper rim of the metal cylinder. co-breeders higher or equal to that of single or monogamous Carcasses were revisited the next morning between 09.00 and breeders (Eggert & MuÈller, 1992; Trumbo, 1992; Trumbo & 10.00 hours to determine whether the carcass had been buried. Wilson, 1993; Scott, 1994a; Robertson et al., 1998). This The strainer covering a cylinder was removed 48 h after the hypothesis was tested in a ®eld experiment on N. defodiens,a carcass had been found buried, allowing experimental beetles species subject to intense competition for carrion by to abandon the carcass and competitors to gain access to it. conspeci®cs and congeners. Possible earlier takeovers were of little interest because the objective of the experiment was to identifypotential bene®ts of extended care bymultiple females. Methods Cylinders were left open for 4 days before they were retrieved and transported to the ®eld laboratory, where their The studywas conducted in a tract of mixed forest (mostly contents were carefullyunearthed and inspected. The retrieval deciduous with some conifers) on Wolfe Lake, a small lake in time was selected on the basis of an earlier ®eld studyof northern Ontario, Canada (46°02¢N, 79°32¢W). Beetles were takeovers in N. orbicollis Say, which had shown that > 90% of collected in traps baited with 30±40 g carcasses of laboratory takeovers occur during the ®rst 6 days after carcass burial mice that had been obtained frozen from a commercial supplier (Robertson, 1993). For each soil core recovered, the burial and thawed as needed. Field-collected beetles were separated depth and condition of the carcass, the number and develop- bysex and maintained on chicken liver for a minimum of mental stage of anylarvae present, and the identityand species 8 days before being used in experimental trials. Mouse of beetles present on the carcass were recorded. When carcasses used in the experiment weighed 30±35 g and were unmarked beetles of larger species were found near the thawed in a refrigerator overnight before being placed in the carcass, it was scored as a successful takeover, unless some or ®eld the following afternoon. A length of dental ¯oss was tied all of the original residents and their brood were still present on to the hind leg of each carcass to facilitate its recoveryonce the carcass. Unmarked conspeci®cs discovered on retrieval buried. Beetles were processed (measured, weighed, marked) were considered successful intruders if the same-sex original between 09.00 and 11.00 hours on the daya trial was initiated resident had disappeared and the stage of the brood suggested and were assigned to either of two treatments: monogamous (a that the original brood had been supplanted bya replacement single female and a male) or polygynous (two females and a brood. male) associations. Bodysize was measured as the width of the pronotum at its widest point at 123 magni®cation using a stereomicroscope (Wild, Heerbrugg, Switzerland) equipped Results with an ocular micrometer, and bodymass was determined to the nearest milligram on an analytical balance. Individuals Seventycarcasses were placed in the ®eld between 12 Julyand were assigned to treatments such that the bodysize of 20 August 1996. Of these, 11 were missing at the time of individuals in both treatments was similar. The bodysize of retrieval, probablydue to the interference of larger mammalian the largest female in polygynous groups (mean pronotum scavengers, most likelyracoons. Such failed broods occurred width 6 SE = 4.82 6 0.06 mm, n = 36) was similar to that of with similar frequencies in monogynous (6/34) and poly- monogamous females (4.82 6 0.06 mm, n = 34; t-test, t = 0.046, gynous (5/36) trials, and were not included in subsequent P > 0.5), and the size of the males was also similar between analyses. One additional trial in which no burying beetles were treatments (monogamous: 4.61 6 0.08 mm; polygynous: found on the carcass at the time of retrieval was also excluded. 4.57 6 0.07 mm; t = 0.418, P > 0.5). The pronotum width of Burying beetles were present on each of the remaining 58 the largest on a carcass varied between 4.19 and carcasses. On 36 of these, at least one of the original N. 5.71 mm. Beetles were marked individuallybypiercing the defodiens residents was still present, while all the original elytra with small insect pins (size 00) in speci®c number- residents on the other 22 carcasses were missing or found dead, encoding patterns. Holes in the orange-coloured areas of the and these carcasses were occupied bylarger congeners. In 20 elytra are readily visible under the stereomicroscope because of these 22 takeovers, the carcass was well-maintained their rims turn black, creating the appearance of distinct black (rounded, solid) and would probablyhave supported another spots. brood: N. orbicollis were present on 13 carcasses, N. Beetles were initiallyplaced on the carcass in transparent tomentosus on another six, and both N. orbicollis and N. 0.5-l plastic containers between 14.00 and 15.00 hours to tomentosus were found on one carcass. In the remaining two acclimate them to the carcass; the beetles along with the takeovers, carcasses had manyholes chewed into them, were carcass were placed in the ®eld between 16.00 and 17.00 hours stretched out, and did not appear ®t for another reproductive on the same day. Beetles were induced to bury carcasses inside attempt. All the beetles present on these carcasses were male open metal cylinders (coffee cans with the tops and bottoms (two N. sayi Laporte and one N. defodiens on one carcass, and removed: diameter 15.5 cm, height 17 cm) that had been one N. tomentosus and one N. defodiens on the other), and they

# 2000 Blackwell Science Ltd, Ecological Entomology, 25, 262±266 264 Anne-Katrin Eggert and Scott K. Sakaluk were probablyusing the carrion as food for themselves rather than their broods. In addition to these 22 unambiguous takeovers, there was one trial in which onlyone of the original residents disappeared and was replaced bya same-sex conspeci®c. When the carcass was retrieved, the original male was still present but the resident female (of a monogamous pair) had disappeared and another, signi®cantlysmaller female (18% smaller pronotum width, 38% smaller bodymass) was present on the carcass. This maynot have been a true takeover involving anyagonistic encounters; the original female may not have been reproductivelycompetent and left the carcass, and the new female mayhave been attracted bythe resident male via pheromone emission. Even when this instance was counted as a successful takeover, there was no impact of group composition (monogamous vs. polygynous) on the probability of takeovers (monogamous: 16 carcasses retained, 13 lost; polygynous: 19 carcasses retained, 10 lost: log-likelihood ratio, G = 0.650, P > 0.2). The bodysize of resident females appears to affect the risk that a carcass is lost to intruders. A logistic regression of takeover probabilities against the bodysize of residents (for polygynous groups, only the size of the largest female was included in the analysis) revealed that larger females were more likelyto retain the carcass than were smaller females (log-likelihood ratio, G = 5.60, P = 0.018). Nearlyall the newly arrived beetles (intruders) were larger and heavier than the original residents. The pronotum width of intruders was on average 34.4 6 4.7% (6 SE) greater than that of the residents (see Fig. 1a), and their bodymass was on average Fig. 1. Distribution of relative bodysize and bodymass advantage 159.3 6 22.4% greater (see Fig. 1b). for successful intruders (n = 23 takeovers). (a) Pronotum width of On ®ve carcasses, original residents and their brood were largest intruder minus pronotum width of largest resident, as a present along with larger congeners. In one of these cases, the percentage of the resident's pronotum width. (b) Bodymass of carcass had produced a large N. defodiens brood but was not heaviest intruder minus bodymass of heaviest resident, as a suitable for another brood. The two individuals of larger percentage of the resident's bodymass. species (N. orbicollis, N. sayi) that were present were probably feeding on the remaining carrion. In the remaining four cases, intruding beetles mayrelocate the carcass further into the soil the intruders were N. tomentosus (three single individuals and to prevent another takeover. In contrast, when the carcass is a pair), all of which were similar in size to the largest original removed bya scavenging mammal, the original location of the resident (between 8% smaller and 14% larger). These are best brood chamber is clearlyvisible, and such cases were included interpreted as unsuccessful takeover attempts in which in the analysis. A multiple regression showed that burial depth residents defended their carcass successfully. Including these depended on the size (pronotum width) of the largest resident instances in the analysis as takeovers would not alter the beetle and on the time of season (days after the start of the conclusion because four of these ®ve carcasses were originally study) at which the carcass was buried, but not on group 2 controlled by polygynous groups. composition (F3,42 = 4.32, P < 0.01, R = 0.24). Larger residents Some of the original N. defodiens residents had attempted to buried carcasses deeper [partial r (6 SE) = 1.43 6 0.52, defend the carcass to their death. Remains of one male and two t = 2.75, P < 0.01], and the depth at which carcasses were female residents and another beetle's abdomen were found in buried decreased over the course of the season (partial r = the vicinityof three carcasses that had been taken over. On ®ve ±0.036 6 0.016, t = 2.25, P < 0.05), but the breeding association carcasses that had been retained bytheir original owners, some (the number of resident females) did not affect burial depth or all beetles were found to be severelyinjured at the time of (partial r = ±0.08 6 0.41, t = 0.20, P > 0.5). carcass retrieval. Most injuries involved the extremities, and each of these beetles had lost at least the tibia from one leg. Bodysize also appeared to have an important effect on the Discussion depth at which the carcass was buried. Burial depth was measured as the distance of the bottom of the brood chamber The results of this studydo not support the hypothesisthat the or crypt to the soil surface. Any carcasses that had been taken presence of a second reproductive female N. defodiens on a over byintruders were excluded from the analysisbecause large carcass reduces the risk that the carcass is lost to other

# 2000 Blackwell Science Ltd, Ecological Entomology, 25, 262±266 Communal breeding in burying beetles 265 burying beetles. Polygynous groups were as likely to lose their original residents in the studyreported here, with few carcass to larger congeners as were monogamous pairs, and exceptions (Fig. 1). There is an important asymmetry between takeovers byconspeci®cs were extremelyrare or absent. These resident and intruder that probablycontributes to the scarcity results are consistent with those of a ®eld studybyTrumbo and of intraspeci®c takeovers: the expected bene®t of winning Fiore (1994), who found that carcasses buried by polygynan- aggressive interactions, or the cost of surrendering, is not the drous groups of N. defodiens (two males, two females) same for both opponents. If the resident wins, its current brood attracted an equal number of competitors as those buried by can complete development on the carcass; the intruder, on the monogamous pairs. Both results argue against improved other hand, can onlywin the remaining amount of carrion, carcass defence as a bene®t to co-operative breeding in which is smaller and of lower qualitythan it was when the burying beetles. Scott (1994a) staged encounters with intruders resident started her reproductive attempt. Some residents byadding potential intraspeci®c or interspeci®c competitors to defended the carcass successfullyagainst larger intruders, established broods of N. tomentosus that had either male± and some suffered severe or even fatal injuries in the process; female pairs or foursomes (two males, two females) as original such evidence of fatal ®ghting in the ®eld previouslyexisted residents. She found no signi®cant advantage for foursomes for N. orbicollis (Trumbo, 1990b) but not for anyother species. against any particular type of intruder, but a re-analysis of the The results of this studyfail to resolve the adaptive overall takeover rates reported in her studysuggests that such signi®cance of co-operative breeding in female burying an advantage maystill exist in N. tomentosus (pairs retained 33 beetles. The onlyprogress theyoffer is that improved carcasses, lost 14, foursomes retained 59 carcasses, lost 10; concealment or defence of the carcass is an unlikely G = 3.92, P < 0.05). explanation for the tolerant behaviour of females or their Takeover rates appeared to be related to the bodysize of extended presence on large carcasses. One remaining possibi- resident females, with larger residents experiencing a lower lityis that communal breeding reduces competition for carrion takeover risk than smaller residents. Two factors may by¯ymaggots, as suggested byScott (1994a) and Trumbo contribute to this effect: larger residents maysimplybe (1994). Large carrion ¯ies cannot access carcasses once they superior competitors in actual aggressive interactions with are buried, however, which makes competition with ¯ies an other beetles, or theymaybe better able to conceal the carcass unlikelycandidate for the explanation of the prolonged successfullyfrom beetles searching activelyfor carrion, and presence of multiple females on the carcass. thus to prevent aggressive encounters. The observation that Trumbo (1995) suggested that for small species like N. burial depth was also related to the bodysize of resident defodiens, successful reproduction on large carcasses maybe beetles suggests that the latter effect mayat least partially so rare that even in the absence of bene®ts to communal mediate the observed effect of bodysize on takeover rate, breeding, the cost of ®ghting is not offset bythe bene®ts that because burying the carcass deeper presumably affords better accrue in the event of successful monopolisation of the carcass. protection against discoveryof the buried carcass byfree- In the present study, however, N. defodiens retained a much ¯ying competitors. Interspeci®c differences may be due to a greater proportion of carcasses (50%) than reported byTrumbo similar advantage conferred bylarger bodysize: N. orbicollis (1995) in his summaryof several earlier studies in the U.S.A. buries carcasses deeper than does N. defodiens (Wilson & (on 16±35 g carcasses: 16% 6 8%). More northerlypopula- Fudge, 1984) and is less likelyto lose them (Trumbo, 1995). tions of this presumablycold-adapted species (Wilson et al., The effect of season on burial depth is probablymediated by 1984) mayexperience lower rates of nesting failure on larger soil properties that mayhave changed over the 2-month course carcasses, but females from these populations still exhibit of the study; later in the season, carcasses are buried less tolerance towards conspeci®cs. deeply, possibly because the soil is drier and harder for the On small carcasses, where aggressive interactions are beetles to manipulate. In addition, manyof the individuals that frequent and intense, the smaller of two competing females are reproductivelyactive late in the season are teneral adults gets onlylimited access to the carcass, departs much sooner, whose exoskeleton maystill be relativelysoft, which could and produces fewer offspring than does her larger rival (MuÈller also hamper the ef®cient and deep burial of carcasses. et al., 1990; Eggert & MuÈller, 1992; Scott & Williams, 1993). Takeovers byintraspeci®c competitors from established N. In communal associations on large carcasses, however, a defodiens residents appear to be rare in general, especiallyon female's genetic contribution to the joint brood need not be large carcasses. In the present study, this occurred at most in associated with her relative bodysize and the duration of her onlyone of 23 observed takeovers. Two other studies provide stayon the carcass (Eggert & MuÈller, 1992, in press; but see information on the frequencyof intraspeci®c takeovers in N. Scott & Williams, 1993). There are situations in which defodiens; only®ve of 69 takeovers from male±female pairs reproductive skew is largelyshaped byacts of larval and single females in Michigan (Trumbo, 1990a), and one of infanticide committed byco-breeding females; occasionally, 14 takeovers from pairs in New Hampshire (Scott, 1994b), entire broods are eradicated (Eggert & MuÈller, in press). were byintraspeci®c competitors. It is possible but not likely Females will then produce replacement clutches if the carcass that N. defodiens maynot be as good at locating buried is still suitable for reproduction (MuÈller, 1987). The prolonged carcasses as its larger congeners. A better explanation is that presence of two or more females on a large carcass maythus large bodysize differences maybe necessaryfor successful have less to do with bene®ts of joint care than with both takeovers. The bodysize, and especiallythe bodymass, of females' sel®sh attempts to bias the composition of the brood successful intruders was considerablylarger than that of in favour of their own offspring.

# 2000 Blackwell Science Ltd, Ecological Entomology, 25, 262±266 266 Anne-Katrin Eggert and Scott K. Sakaluk

Acknowledgements the , (Coleoptera: Silphidae). Journal of Zoology (London), 231, 583±593. This studywas supported bya research grant from the Robertson, I.C., Robertson, W.G. & Roitberg, B.D. (1998) A model of Deutsche Forschungsgemeinschaft to Dr Josef K. MuÈller (Mu mutual tolerance and the origin of communal associations between 1175/2-1) and bygrants from the National Science Foundation unrelated females. Journal of Insect Behavior, 11, 265±286. Scott, M.P. (1994a) Competition with ¯ies promotes communal (IBN-9601042) and Illinois State Universityto S.K.S. We breeding in the burying beetle, Nicrophorus tomentosus. thank S. T. Trumbo and an anonymous reviewer for comments. Behavioral Ecology and Sociobiology, 34, 367±373. Thanks also to the Toeppner familyfor allowing us to place Scott, M.P. (1994b) The bene®t of paternal assistance in intra- and dead rodents in their stretch of forest at our leisure, Donna Sr, interspeci®c competition for the burying beetle, Nicrophorus Donna Jr, John and Marion Sakaluk for logistic support, and defodiens. Ethology, Ecology and Evolution, 6, 537±543. Wayne Riddle for an abundant supply of coffee cans. Scott, M.P. (1997) Reproductive dominance and differential ovicide in the communallybreeding buryingbeetle Nicrophorus tomentosus. Behavioral Ecology and Sociobiology, 40, 313±320. References Scott, M.P. & Williams, S.W. (1993) Comparative reproductive success of communallybreeding buryingbeetles as assessed by Brown, J.L. (1987) Helping and Communal Breeding in Birds: PCR with randomlyampli®ed polymorphicDNA. Proceedings of Ecology and Evolution. Princeton UniversityPress, Princeton, the National Academy of Sciences of the United States of America, New Jersey. 90, 2242±2245. Eggert, A.-K. & MuÈller, J.K. (1992) Joint breeding in female burying Trumbo, S.T. (1990a) Interference competition among burying beetles beetles. Behavioral Ecology and Sociobiology, 31, 237±242. (Silphidae, Nicrophorus). Ecological Entomology, 15, 347±355. Eggert, A.-K. & MuÈller, J.K. (1997) Biparental care and social Trumbo, S.T. (1990b) Reproductive bene®ts of infanticide in a evolution in burying beetles: lessons from the larder. The Evolution biparental burying beetle Nicrophorus orbicollis. Behavioral of Social Behavior in and Arachnids (ed. byJ. C. Choe and Ecology and Sociobiology, 27, 269±273. B. J. Crespi), pp. 216±236. Cambridge UniversityPress, Cambridge. Trumbo, S.T. (1992) Monogamyto communal breeding: exploitation Eggert, A.-K. & MuÈller, J.K. (in press) Timing of oviposition and of a broad resource base byburyingbeetles ( Nicrophorus). reproductive skew in co-breeding female burying beetles Ecological Entomology, 17, 289±298. (). Behavioral Ecology. Trumbo, S.T. (1994) Interspeci®c competition, brood parasitism, and Hrdy, S.B. & Hausfater, G. (1984) Infanticide: Comparative and the evolution of biparental cooperation in burying beetles. Oikos, Evolutionary Perspectives. Aldine, New York. 69, 241±249. Keller, L. & Vargo, E.L. (1993) Reproductive structure and Trumbo, S.T. (1995) Nesting failure in burying beetles and the origin reproductive roles in colonies of eusocial insects. Queen Number of communal associations. Evolutionary Ecology, 9, 125±130. and Sociality in Insects (ed. byL. Keller), pp. 16±44. Oxford Trumbo, S.T. & Fiore, A.T. (1994) Interspeci®c competition and the UniversityPress, Oxford. evolution of communal breeding in burying beetles. American MuÈller, J.K. (1987) Replacement of a lost clutch: a strategyfor optimal Midland Naturalist, 131, 169±174. resource utilization in Necrophorus vespilloides (Coleoptera: Trumbo, S.T. & Wilson, D.S. (1993) Brood discrimination, nest mate Silphidae). Ethology, 76, 74±80. discrimination, and determinants of social behavior in facultatively MuÈller, J.K., Eggert, A.-K. & Dressel, J. (1990) Intraspeci®c brood quasisocial beetles (Nicrophorus spp.). Behavioral Ecology, 4, 332± parasitism in the burying beetle, Necrophorus vespilloides 339. (Coleoptera: Silphidae). Behaviour, 40, 491±499. Wilson, D.S. & Fudge, J. (1984) Burying beetles: intraspeci®c Pukowski, E. (1933) OÈ kologische Untersuchungen an Necrophorus F. interactions and reproductive success in the ®eld. Ecological Zeitschrift fuÈr Morphologie und OÈ kologie der Tiere, 27, 518±586. Entomology, 9, 195±203. Reeve, H.K. & Ratnieks, F.L.W. (1993) Queen±queen con¯icts in Wilson, D.S., Knollenberg, W.G. & Fudge, J. (1984) Species packing polygynous societies: mutual tolerance and reproductive skew. and temperature dependent competition among burying beetles Queen Number and Sociality in Insects (ed. byL. Keller), pp. 45± (Silphidae, Nicrophorus). Ecological Entomology, 9, 205±216. 85. Oxford UniversityPress, Oxford. Robertson, I.C. (1993) Nest intrusions, infanticide, and parental care in Accepted 26 October 1999

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