Behav Ecol Sociobiol(1994) 34:367 373

Behavioral Ecology and Sociobiology © Springer-Verlag 1994

Competition with flies promotes communal breeding in the burying beetle, Nicrophorus tomentosus Michelle Pellissier Scott Department of Zoology,University of New Hampshire, Durham, NH 03824 USA Received: 8 September 1993 / Accepted after revision: 20 February 1994

Abstract. Communal breeding through nest-sharing may benefit cooperating individuals indirectly, in increased inclusive fitness, or directly, when environmental constraints reduce the fitness of solitary breeders. Burying beetles provide extensive parental care and can breed either in pairs or in larger groups of unrelated males and females. Parentage of communally-reared broods is usually shared but is skewed in favor of the individuals of each sex that provide longer care. Females provide care longer than males, and two females are more likely to remain together in the brood chamber than two males are. Flies and other burying beetles are the major competitors for carcasses and this study suggests that it is competition with flies that promotes communal breeding in Nicrophorus tomentosus. On medium-size carcasses (35M0 g) the presence or absence of oviposition by flies had a significant effect on the size of the brood reared, and on large carcasses (55-60 g) the number of beetles present, two or four, had a significant effect on brood size. On both medium and large carcasses, pairs rearing broods on flyblown carcasses had fewer young than pairs on clean carcasses or foursomes on flyblown carcasses. There was a strong trend for an interaction effect between number of beetles and competition with flies (Table l). Duration of parental care was not affected by competition with flies except for that of the first male to depart, which provided care longer on flyblown carcasses (Table 2). Pairs and foursomes were equally able to defend the carcass and brood from conspecific intruders and from larger intruding Nicrophorus orbicoIlis (Table 3). Key words: Communal breeding - Parental care - Burying beetles - Nicrophorus

Introduction Reproductive cooperation has been important in the evolution of many aspects of social behavior. In communal breeding of birds and mammals, one form of repro-

ductive cooperation, nest-sharing or mate-sharing can lead to a polygynous, polyandrous or polygynandrous mating system when more than two adults provide care and are the parents of some of the young (Davies 1992). These adults are often not related and therefore do not gain indirect benefits through kin selection (Hamilton 1964). Similarly, the occurrence of mul'tiple foundresses of nests in some Hymenoptera results in the cooperative rearing of young. Frequently, but by no means always, foundress associations in wasps consist of close relatives (Metcalf and Whitt 1977; Queller et al. 1988), in which case there is a benefit through indirect fitness for a reproductively subordinate individual joining another female (West-Eberhard 1975; Noonan 1981). However, when there are ecological factors contributing to high rates of nest failure for solitary females, even unrelated females may gain from cooperation. The major selective factors may be defense against predators, parasites or usurpation by conspecific females, and for insurance that some adult members of the colony will survive when adult mortality is high (Strassmann and Queller 1989; Reeve 1991). Foundress associations may be mutualistic and all females may have a higher fitness than if they nested alone (Lin and Michener 1972). Usually, however, there is a strong asymmetry in the benefit of this reproductive cooperation; the dominant female may lay most of the eggs and enjoy the highest probability of survival, especially if she spends most of her time in the nest (Metcalf and Whitt 1977; Ross 1988; R6seler 1991). To understand the evolution of communal breeding, such as nest-sharing in birds and the social Hymenoptera, we must be able to separate genetic and environmental factors, identify the options open to each individual, and measure the trade-offs. Individuals may cooperate because it increases their direct or indirect fitness or they may be manipulated into doing so (Alexander 1974). Burying beetles (Silphidae, Nicrophorus) are an excellent model system for the investigation of reproductive cooperation. They are unusual among insects in that both males and females often provide extended parental care and sometimes more than one male or female rear a

368 single b r o o d (Eggert a n d Mfiller 1992; T r u m b o 1992; Scott a n d W i l l i a m s 1993). These i n d i v i d u a l s are a l m o s t c e r t a i n l y n o t genetically related, w h i c h e l i m i n a t e s a n y indirect benefits of c o o p e r a t i v e b e h a v i o r t h r o u g h inclusive fitness.

Natural history B u r y i n g beetles are a t t r a c t e d to small v e r t e b r a t e carcasses t h a t will b e c o m e f o o d for their young. If m o r e t h a n one m a l e o r female discover the carcass, t h e y u s u a l l y c o m p e t e i n t r a s e x u a l l y a n d the v i c t o r i o u s m a l e a n d female (usually the largest) b u r y a n d p r e p a r e the carcass ( P u k o w s k i 1933; W i l s o n a n d F u d g e 1984; B a r t l e t t a n d A s h w o r t h 1988). O n c e u n d e r g r o u n d , the carcass is rolled into a ball, the fur or feathers are r e m o v e d a n d it is t r e a t e d with o r a l a n d a n a l secretions. Nicrophorus tomentosus females lay eggs in the soil n e a r b y 2 4 - 6 0 h after b e g i n n i n g to b u r y the carcass a n d these h a t c h into altricial l a r v a e 3 d a y s later. A l t h o u g h some species require p a r e n t a l r e g u r g i t a tion at least at first, others, i n c l u d i n g N. tomentosus, can d e v e l o p n o r m a l l y w i t h o u t p a r e n t a l feeding ( p e r s o n a l o b s e r v a t i o n ; T r u m b o 1992). L a r v a e c o m p l e t e d e v e l o p m e n t in 6 - 8 days, leave the b r o o d c h a m b e r a n d disperse into the soil to p u p a t e . N. tomentosus e m e r g e as a d u l t s the following s u m m e r . U s u a l l y s m a l l e r carcasses are b u r i e d a n d each b r o o d is r e a r e d b y one m a l e a n d one female a n d t y p i c a l l y the female r e m a i n s with the b r o o d l o n g e r t h a n the male. H o w e v e r , l a r g e r carcasses are often b u r i e d a n d p r e p a r e d b y m o r e t h a n one m a l e a n d / o r female (Scott a n d Traniello 1990; T-rumbo 1992). These b r o o d s c a n h a v e m i x e d p a r e n t a g e a n d a d u l t s c a n r e m a i n with the b r o o d a n d p r o v i d e care to offspring w h i c h are n o t theirs (Eggert a n d Mfiller 1992; T r u m b o 1992; Scott a n d W i l l i a m s 1993). A carcass is a rich r e s o u r c e for m a n y o r g a n i s m s , including o t h e r b u r y i n g beetles, flies, fungi a n d microbes. In s o u t h e r n N e w H a m p s h i r e , there are two o t h e r b u r y i n g beetles, the l a r g e r N. orbicollis a n d the smaller N. defodiens, whose r e p r o d u c t i v e seasons o v e r l a p t h a t of N. tomentosus in August. Even after the carcass is buried, it can be d i s c o v e r e d b y o t h e r beetles which u s u r p the carcass, kill the b r o o d a n d p r o d u c e their o w n y o u n g (Scott 1990; T r u m b o 1990, 1991). This s t u d y seeks to identify e n v i r o n m e n t a l factors p r o m o t i n g c o m m u n a l breeding. I e x a m i n e the o u t c o m e of c o m p e t i t i v e i n t e r a c t i o n s between N. tomentosus a n d o t h e r b u r y i n g beetles a n d flies to assess the a d v a n t a g e s of g r o u p defense to the r e p r o ductively d o m i n a n t m a l e a n d female of a l l o w i n g a consexual to r e m a i n in the b r o o d c h a m b e r a n d share the p a r e n t a g e of the young.

Competition withflies. Beetles were given a carcass to bury in a pot 22 cm in diameter and 27 cm high that had been filled with a core of soil from the forest. In half the replicates there were a male and female, representing the option of the dominant individual to exclude consexuals from the burial chamber; in the other half there were two male and two female beetles, representing the option of cooperation. Consexuals differed in pronotal width by 10-25%. Half of these replicates had a 35-40 g (previously frozen) mouse carcass and half had a 55-60 g carcass, either a rodent or chick. Flies were prevented from ovipositing on half of these carcasses and the other half of the carcasses were exposed to flies on a warm, sunny day for about 4-5 h. Flyblown carcasses had visible clusters of eggs and six of these, which were set aside in a closed container, were completely consumed by maggots. Thus, there were three variables : beetle number, carcass size and the presence or absence of fly eggs (see Table 1). There were 30 replicates of each type. The pot was covered with Plexiglas until the carcass was buried, usually by the next morning, then the pot was placed inside a taller pot 30 cm in diameter that was covered with Plexiglas. When adults terminated parental care, they left the brood chamber and fell into the larger pot where they were captured. When all adults had left the brood chamber and larval development was complete (at least 16 days after burial), the brood chamber was exhumed and the larvae counted and weighed. The soil was checked for evidence of fly larvae and pupae and the condition and amount of remaining carcass (if any) was estimated.

Competition with burying beetles. Either a male and female or two males and two females were given a 35-40 g mouse carcass to bury on the forest floor. Replicates were 1-3 m apart. All beetles were individually marked with photo-reduced numbers glued to their elytra. A 30-cm piece of dental floss was tied to the rear leg of the carcass to facilitate its location after burial. The carcasses were covered by a 30-cm pot to discourage the immediate escape of the beetles and discovery by free-flying beetles. A male or female burying beetle intruder was introduced under the pot on the 4th day (N. tomentosus) or evening (N. orbicollis). The brood chamber was exhumed onthe 6th day; all beetles were caught and identified. The presence or absence of larvae was noted. Dynamics of groupformation. Two male and two female beetles were allowed to bury a 35-40 g mouse on the forest floor. Replicates were covered by a 30-cm pot and were 1-3 m apart. All beetles were individually marked. A male or female N. tomentosus was introduced under the pot after 24 h (before oviposition) or on the 4th day (before eggs hatched). The brood chamber was exhumed 24 h after the introduction of the intruder and all beetles were captured and identified.

Speed of burial. Either a male and female or two males and two females were released mid-day on a 45-50 g chick carcass on the forest floor. Replicates were covered by a 30-cm pot and were 1-3 m apart. They were checked every hour for the first 12 h and every 2 h thereafter. The carcass was scored "buried" when it was under soil and no part of the chick was visible. The carcass was exhumed 24 h later and the depth of the burial chamber measured.

Results Competition with flies

Methods Beetles used in these experiments were captured in Jaffrey, NH. They were usually kept for less than 2 weeks before being used in an experiment, fed meal worms and beef kidney ad libitum and maintained with like-sex individuals in natural temperature and day length. All experiments were performed outside.

Several types of 5 5 - 6 0 g carcasses were u s e d : large mice, small rats a n d chicks. T h e t o t a l weight of the b r o o d r e a r e d on chicks was significantly g r e a t e r t h a n those r e a r e d on the r o d e n t carcasses (9.9 _+ 3.2 g, n = 96 vs. 4.5 __ 3.9 g, n = 24 respectively, P -- 0.000). This difference p r o b a b l y o c c u r r e d b e c a u s e the q u a l i t y of m a n y of

369 Table 1. The total weight (g) of the brood reared by pairs or foursomes of Nicrophorus tomentosus on flyblown and clean carcasses (means_+ SD). The number of larvae reared are in brackets and sample sizes are in parentheses Pairs

Two males two females

35-40 g carcasses No flies Flies

5.9_+2.6 [28.4_+9.9] (n=28) 4.1_+2.8 [20.6--12.8] (n=30)

5.8_+2.0 [29.5_+9.5] (n=30) 5.4_+3.1 [25.9_+13.4] (n=30)

55-60 g carcasses Noflies Flies

9.3_+2.7 [36.5_+12.2] (n=24) 7.6-+3.6 [29.4-+14.6] (n=25)

11.7_+3.0 [50.7_+14.1] (n=24) 11.3-+3.5 [48.7-+15.8] (n=23)

Probabilities from a multifactor ANOVA on total brood weights

Pairs vs foursomes Flies vs no flies Carcass size Group size x flies Group size x carcass size Flies x carcass size Group size x flies x carcass size

35-40 g P

55-60 g P

All carcasses P

0.245 0.019

0.000 0.076

0.162

0.274

0.000 0.004 0.000 0.077 0.001 0.892 0.949

these rodent carcasses had been reduced by long storage and occasional partial thawing which dehydrated and degraded them. The 35-40 g mice and 55-60 g chicks had been stored for 1 m o n t h or less. Replicates using 55-60 g rodents were excluded from further analysis. Two 35 40 g carcasses were disturbed by a large m a m m a l and were also excluded from analysis. On small carcasses exposure to flies had a significant effect on the total weight of the b r o o d reared, and on large carcasses the n u m b e r of beetles had a significant effect. On 35-40 g carcasses the total weight of the b r o o d was significantly greater on clean carcasses than flyblown ones but was not different when reared by pairs or foursomes (Table 1). However, on 55-60 g carcasses the total weight of the b r o o d was significantly greater when reared by foursomes than pairs but was not significantly different on clean or flyblown carcasses. Analysis of the number of larvae rather than b r o o d weight produced similar results. (Total b r o o d weight is a better measure of reproductive success than n u m b e r of larvae because there is a trade-off between n u m b e r and weight of larvae.) My expectation was that only pairs would suffer in competition with flies, i.e. that there would be a significant interaction between group size and exposure to flies. There was a strong trend in this direction when all data were combined (P = 0.077, Table 1). The reduction of reproductive success suffered by beetles on flyblown carcasses was due to competition with flies. On large carcasses for which the presence of maggots and fly pupae was systematically noted when the b r o o d chamber was exhumed, 35% of those buried by foursomes produced at least some flies and 74% of those buried by pairs produced flies (G = 7.30, P < 0.01). Some beetles burying flyblown carcasses reared no young (3 of 30 by pairs and 1 of 30 by foursomes on 35-40 g carcasses; 2 of 25 by pairs and 0 of 23 by foursomes on 55-60 g carcasses) whereas no beetles burying

clean carcasses experienced b r o o d failure (G = 8.38, P < 0.01). In most cases it was clear that brood failure was due to competition with the flies: two of the three pairs on 35-40 g carcasses and both pairs on 55-60 g carcasses deserted on the first day and all five carcasses were partially or completely consumed by flies; the cause of b r o o d failure was unclear only for the 35-40 g carcass buried by a foursome, for which three beetles provided 5-7 days of care. All replicates of brood failures were included in the analysis presented in Table 1 because failure was the result of competition with flies. But even when failed broods were removed from the analysis of 35-40 g carcasses, the effect of exposure to flies was significant (P = 0.042). The male and female of a foursome that remained longer provided about the same duration of care as the male and female of a pair, respectively (Table 2). These data are pooled. As is the case with other burying beetles studied, females provided care longer than males on both large (t s = 4.24, P<0.001) and small (ts -- 10.0, P < 0.001) carcasses. Two females were more likely to remain together on a carcass than two males. On small carcasses, two females were present on the 5th day when eggs were expected to hatch in 55% of the b r o o d chambers and two males were present in 18% (G = 14.34, P<0.001). On large carcasses, two females were still present on the 5th day in 22% and two males were present in 12% (G = 1.40, P>0.05). For the most part, the duration of parental care was not affected by either group size or exposure to flies. Only the male of a foursome that provided shorter care remained significantly longer on flyblown carcasses than on clean ones and this relationship was stronger on smaller carcasses than larger ones (Table 2). All classes of parents except the male of a foursome that provided shorter care remained with the carcass and b r o o d significantly longer on smaller carcasses than larger ones. This

370 Table 2. Duration (days) of parental care (mean + SD) Pairs Female Male Two males, two females Female providing longer care Male providing longer care Female providing shorter care Male providing shorter care Exposed to flies Not exposed to flies

35-40 g carcass

55-60 g carcass

12.1_+3.9 (n= 53) 7.4_+2.0 (n=51)

7.4+_6.0 (n=43) 4.7 + 3.5 (n=47)

_+3.7 (n = 58) 7.0_+2.9 (n= 57) 4.4_+2.2 (n= 55) 2.9 _+1.9 (n = 44) 4.1_+1.6 (n=21) 1.7 +_1.3 (n = 23)

7.6 _+3.6 (n = 45) 5.1_+3.3 (n =44) 3.4 _+2.4 (n = 46) 2.2 -+2.3 (n = 34) 2.5_+2.2 (n= 15) 1.8-t-2.3 (n= 19)

11.0

Because there were no significant differences, results for flyblown and clean carcasses have been combined except for the male providing shorter care for which these data are broken down. Multifactor ANOVAs found no significant differences in the durations of care in any comparisons with the following exceptions: Single females and females providing longer care on small vs. large carcasses, P=0.000; single males and males providing longer care on small vs. large carcasses, P = 0.000; females providing shorter care on small vs. large carcasses, P = 0.024; males providing shorter care with flies vs. no flies, P = 0.000 and carcass size x flies, P = 0.054 Table 3. Probability of successful takeover by intruders of carcasses guarded by pairs and by two males and two females. Two-tailed probabilities from Fisher's exact tests are shown Intruder

Pairs

Foursomes

P

N. N. N. N.

0 (n = 12) 0.30 (n= 10) 0.33 (n=9) 0.50 (n = 16)

0.05 (n = 20) 0.11 (n = 19) 0.07 (n= 15) 0.40 (n = 15)

0.62 0.32 0.13 0.72

tomentosus female tomentosus male orbicollis female orbicollis male

difference in the d u r a t i o n of care is p r o b a b l y not caused by the difference in the size of the carcasses. Studies on other species have shown that the d u r a t i o n of parental care increases on larger carcasses (Scott and Traniello 1990). All replicates on smaller carcasses were done in early-mid August and those on large carcasses were d o n e in late A u g u s t and mid-September. Male and female N. orbicollis provide care longer for early, first b r o o d s which are also larger (Scott and Traniello 1990; unpublished data). It is likely that this is true for N. tomentosus as well and m a y explain the difference in duration of care.

Competition with burying beetles Pairs and foursomes were able to defend the carcass and b r o o d equally well against a male or female conspecific intruder or a male or female intruder of the larger competitor, N. orbicollis (Table 3). W h e n intruders successfully usurped the carcass, larvae from the original occupants where seldom present when the b r o o d c h a m b e r was exhumed. W h e n N. tomentosus was the potential intruder, larvae were present in 85% (n = 55) of the b r o o d chambers when the intruder was unsuccessful and 33% (n = 6) of the b r o o d chambers when the intruder was successful (Gadj = 6.65, P < 0.01). W h e n N. orbicollis was the intruder, larvae were present in 92% (n = 37) of the b r o o d chambers when the intruder was unsuccessful and 56% (n = 18) of the b r o o d chambers when the intruder was successful (Gaaj = 8.98, P < 0 . 0 1 ) . W h e n larvae were present even t h o u g h the intruder h a d successfully

Table 4. Probability that an intruder joins residents in the brood chamber when it is introduced 24 h and 4 days after burial

Female intruder Mate intruder

After 24 h'

After 4 days

0 (n = 12) 0.125 (n= 8)

0.05 (n = 20) 0.11 (n= 19)

usurped the carcass, there were usually only one or two newly hatched individuals. Successful intruders were never seen caring for y o u n g of the previous o c c u p a n t and, given m o r e time, p r o b a b l y would have killed all the larvae.

Dynamics of group formation Male or female conspecifics that were introduced under the pot 24 h after burial began (before oviposition) were just as likely to be repelled by the adults in the b r o o d c h a m b e r as conspecifics introduced on the 4th day (just before larvae hatched) (Table 4). The three successful male intruders were larger than the residents and in two cases, the late-joining male was the only male present when the c h a m b e r was exhumed. These males could be interpreted as successful intruders that w o u l d kill the larvae and reinseminate the females.

Speed of burial Carcasses were n o t buried faster by four beetles than by two (median = 15 h, n = 16, vs. 11 h, n = 16, respectively, U S = 142, P > 0.1). C o n t r a r y to expectation, carcasses were buried significantly deeper in 24 h by two beetles than by four (3.0 cm vs. 2.25 cm, Us = 176.5, P = 0.05) which suggests that burial is not a very c o o r d i n a t e d affair.

371 Discussion

A carcass is a rich, unpredictable resource and as such, promotes the evolution of parental care (Wilson 1971; Tallamy and Wood 1986). Finding and burying a carcass could literally be the chance of a lifetime (Scott and Gladstein 1993). Competition with other beetles can be severe and individuals may be injured or killed (Scott 1990; Trumbo 1991). Although the larger individuals of each sex can expel consexuals (Wilson and Fudge 1984) and do so on smaller carcasses (Trumbo 1992), they do not always do so on larger ones. Depending on the site and species of beetle, 30-70% of large carcasses (> 50 g) may be found and buried by more than one male and/or female (Scott 1990; Trumbo 1992; Scott unpublished data). As theory predicts (Trivers 1972), females are more likely to remain in the brood chamber together than are two males. In this study, smaller carcasses could be fully utilized by a single female. But larger carcasses could to some extent be shared by two females. As has been demonstrated in other species (Eggert and Mfiller 1992; Trumbo and Wilson 1993), the total reproductive output of two female N. tomentosus on larger carcasses is greater than that of a single female because females are limited in the number of eggs they can oviposit that will hatch more or less synchronously (Bartlett and Ashworth 1988; Miiller et al. 1990a; Scott unpublished data). Males, however, have no such limitation and cooperation between males is expected to be rare. When two males are simultaneously given access to a carcass, one often, but by no means always, leaves as soon as experimental design allows. The composition of cooperating individuals is established as the carcass is being buried. Intruders were not allowed to join a group any more readily after only 24 h than after 4 days. Females and males are infanticidal until a few hours before their eggs hatch (Mfiller and Eggert 1990). Therefore, communally-breeding females must begin to oviposit more or less synchronously. A late-joining individual would kill larvae which arrived at the carcass earlier than its own larvae would arrive. A laboratory study of N. vespilloides suggested that maternity of the brood was shared equally between two cooperating females (Eggert and Mfiller 1992) but the proportion may vary by species or population. DNA markers showed that maternity in this study was shared in only 70% of N. tomentosus broods communally reared on 35-40 g carcasses. (Ten of the parents and larvae from this study that were reared by foursomes on clean 3540 g carcasses were used for parentage analysis by randomly amplified polymorphic DNA, RAPD, using the polymerase chain reaction. Methods and data are presented in Scott and Williams 1993.) The reproductively dominant female was the mother of 50 100% (mean 80%) of the larvae. (Hereafter dominant and subordinate refers only to reproduction and implies nothing of the behavioral interactions.) The duration of care by the subordinate female was always less than that of the dominant female, but some were present for as long as 6-8 days even though they produced few or no young. Similarly, paternity of the larvae was shared in only 70% of

the broods. The dominant male always provided care longer than the subordinate male and was the father of 50 100% (mean 87%) of the young. Subordinate males may have inseminated one or both females as an '°extrapair copulation" and been excluded from the carcass or they may have assisted in its burial and preparation and left soon after (Bartlett 1988; Scott and Williams 1993). With foundress associations in social insects, the question of the identification of ecological constraints favoring communal breeding is usually posed from the subordinate's perspective: what factors favor a potentially subordinate individual joining another female (Brockman 1984; Reeve 1991)? But burying beetles form only temporary associations. Potential subordinates would be selected to join as long as the average number of offspring they produce as a subordinate is greater than the product of the probability that they will find and bury a carcass monogamously during that period and the number of resulting offspring. The availability of carcasses is probably very low (Scott and Gladstein 1993) and the subordinate individuals reduce their costs by remaining for a shorter time. The question of the benefits of communal breeding by burying beetles is better posed from the perspective of the dominant individuals: why don't the potentially dominant individuals, which are almost always the larger, expel consexuals? Also, in the study of social insects attention has recently turned to the question of the degree to which the dominant individual should monopolize reproduction and how much the subordinate should be allowed as an incentive to stay (Vehrencamp 1983a, b; Reeve and Ratnieks 1993). Communal breeding appears to reduce the reproductive success of the dominant because the principal determinant of reproductive success is carcass size, not the size of the parents or the duration of their care (Scott and Traniello 1990). Broods reared by one or two females on 3540 g carcasses in the absence of competition with flies are the same size. Parentage analysis indicates that the reproductive success of the dominant female is reduced by 20% when she allows a subordinate to remain. The subordinate's proportion of the total brood may be larger on larger carcasses which are 26% larger when reared by two females. Similarly, a second male reduces the reproductive success of the dominant male by 13% on smaller carcasses in the absence of competition with flies. However, when there is competition with flies, broods reared on small carcasses by foursomes are 32% larger than those reared by a pair. On larger carcasses, they are 49% larger. Although the intensity of competition with flies is expected to vary according to site, weather and time of the summer and may be quite different from the experimental conditions of this study, these results suggest that it is competition with flies that promotes communal breeding. That the subordinate males provide significantly longer care on flyblown carcasses also suggests that there is a benefit to assistance by both males and that the subordinate remains a few days longer to help eliminate maggots and eggs. Fly eggs may be destroyed by the phoretic mites carried by the beetles (Wilson and Knollenberg 1987) or eaten by the beetles themselves. They hatch quickly, per-

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haps even before the carcass is discovered by the beetles, and maggots enter the carcass through orifices where they are probably harder for the beetles to find and destroy. This forces the dominant female to allow a subordinate to remain well after oviposition by beetles if she is to gain the benefit of her assistance with the carcass which is not fully prepared for about three days. In this study the subordinate female remained for 3.4 and 4.4 days on large and small carcasses, respectively, which suggests that the dominant female usually allowed the subordinate to remain. In other laboratory studies I have seen both females together with the carcass 24 h after it was buried in about 75% of cases (Scott unpublished data). Females excluded from the carcass would be able to lay eggs as parasites only if they had had some access to it during its burial and preparation because oogenesis is triggered by the behavior of burying (Scott and Traniello 1987). So although brood parasitism by subordinate females may be fairly common in some Nicrophorus species (Mfiller et al. 1990b), communal breeding is common with N. tomentosus. The actual frequency of communal breeding in the field depends on the density of the beetle population as well as other factors, because a carcass must be discovered by several consexuals within 24 h. Both N. orbicollis and N. defodiens breed communally on large carcasses, at about a quarter and half the frequency, respectively, of N. tomentosus on similar-size carcasses (Scott and Traniello 1990; Trumbo 1992; Scott unpublished data). The European species, N. vespilloides, also breeds communally at lower frequency (Miiller et al. 1990b). N. tomentosus breeds in August and September whereas N. orbicollis and N. defodiens begin breeding in June and continue to bury carcasses through August. However, competition with flies is severe in August (Scott et al. 1987) and beetles locating carcasses in the field lose 31-79% of these to flies, depending on the species and time. At the same time, N. tomentosus loses only 14% (Scott and Traniello 1990; unpublished data). Cooperation does not reduce failure for N. defodiens in August (Trumbo and Fiore 1994); Scott unpublished data) and for this species the high rate of nest failure on large carcasses may promote the evolution of tolerance because there is little to be gained by excluding a rival (Trumbo 1994). N. tomentosus is a diurnal species and the other New Hampshire burying beetles are nocturnal. Diurnal activity, however, may increase the level of competition with flies only slightly if at all for N. tomentosus. Undiscovered carcasses eventually buried by N. tomentosus probably have no greater exposure to flies than those discovered at night by other burying beetles, because the carcasses are not always found within a few hours of their availability. Among the most serious competitors of burying beetles are other burying beetles. The threat of usurpation by conspecifics is the selection pressure driving extended paternal care in N. orbicollis (Scott 1990; Trumbo 1990, 1991). However, it seems not to be a major factor promoting communal breeding. Although the larger N. orbicollis can take over a carcass from N. tomentosus, four beetles are not significantly better at defending it than two. Furthermore, the importance of competition

from congeners in the evolution of communal breeding depends on the density of beetles. By August there are relatively few reproductive N. orbicolIis. Furthermore their motivational state may be low if there is insufficient time for N. orbicollis larvae to undergo metamorphosis, eclose and prepare for winter. (N. tomentosus overwinter as larvae.) N. tomentosus at 10 times the density, are the more important competitors, but they can be successfully repelled by a resident pair. Lastly, if there are more than two beetles the carcass is not buried faster or deeper (which would reduce the probability of discovery by other burying beetles). Fungi are also competitors for the carcass. Carcasses used in this study were well within the size range easily utilized by burying beetles (Trumbo 1992). The larger carcasses would be more difficult to preserve and keep clean but neither pairs nor foursomes had difficulty. Most of these carcasses were fully utilized by the beetles and if anything remained, it was free of mold. The behavioral nature of the cooperation among burying beetles is not clear. There is no recognition of kin. Broods can be experimentally exchanged between parents (Sherwood and Scott, unpublished data) and females feed young without regard to parentage (Trumbo and Wilson 1993). Presumably all come to the defense of the brood when it is discovered by a congeneric intruder. After the carcass is buried and prepared and the flies have been destroyed, there is only a small advantage in more than two adults remaining with the brood but a substantial advantage in two remaining to guard against conspecific intruders. Because there are no obvious asymmetries in expected future reproductive success between consexuals, i.e. future fecundity and probability of finding another carcass are expected to be the same for individuals of the same sex, game-theory models (Maynard Smith 1977) predict that the dominant and subordinate individuals of each sex might be equally likely to desert first leaving the other in a "cruel bind" (Trivets 1972). But the dominant individuals have more to lose than the subordinates and it may be that the subordinates' share of the brood is less than the minimum needed to balance the cost of longer duration of care. Alternatively, it is likely that the duration of parental care is hormonally mediated and the endocrine system is affected by behavior and experience (Lehrman 1965; Crews 1977). The behavior of burying causes ovarian development (Scott and Traniello 1987) which in turn causes parental behavior. Brood-care behavior is obviously strongly selected when a parent is unassisted. Continued parental care by communally breeding adults may be unselected (Jamieson 1989) rather than adaptive and the duration of their care may depend on how much access they have to the carcass or on the behavioral interactions of the adults. Acknowledgements. I thank Bob Taylor, the University of New Hampshire Agriculture Station and the Dana Farber Cancer Institute for supplying me with carcasses and the Daniel Shattuck family for allowing me access to their fields. This research was supported by National Science Foundation grant DEB 9222148.

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