Is There A Cost To Larval Begging In The Burying Beetle Nicrophorus Vespilloides?

Offspring of many animals signal their nutritional needs using conspicuous begging displays. Theoretical models for the evolution of begging suggest that costly begging signals provide an evolutionarily stable resolution to parent–offspring conflict because they provide parents with honest information on offspring need. However, other models suggest that cost-free or low-cost begging can evolve because parents and offspring have overlapping interests. Empirical studies on birds provide mixed and ambiguous evidence for begging costs. Here, we examine begging costs in the burying beetle Nicrophorus vespilloides. Larval begging may incur a growth cost as in birds or an opportunity cost because larvae cannot beg for food and self-feed at the same time. We used a novel experimental design, in which we controlled begging through the presence or absence of a dead parent simultaneously as we controlled the opportunity to self-feed through the presence or absence of food. As intended, the presence of a dead parent stimulated larval begging, whereas larvae never begged when the dead parent was absent. However, the presence or absence of a dead parent had no effect on larval growth. Likewise, the interaction between the presence or absence of food and the presence or absence of a dead parent had no effect on growth. Thus, our study provides no evidence of either a growth cost or an opportunity cost of larval begging in N. vespilloides. The lack of evidence for any significant begging costs suggests that cost-free or low-cost begging could be more common than hitherto recognized. Key words: begging, burying beetles, cost-free signaling, parent–offspring conflict, signaling cost, signaling of need. [Behav Ecol 19:1111� (2008)]

In many birds and mammals, but also in some amphibians and insects, offspring use conspicuous begging displays to communicate their nutritional needs to the parents (Kilner and Johnstone 1997 Budden and Wright 2001 Wright and Leonard 2002). The conditions under which offspring beg- ging signals can be evolutionarily stable has been, and re- mains, a major issue in behavioral ecology. Parent–offspring conflict theory suggests that parents and offspring have diver- gent though overlapping interests concerning the allocation of parental resources and that offspring should be under se- lection to demand more than parents are prepared to provide (Trivers 1974). However, if offspring use begging to exagger- ate their true need, parents should be under selection to ignore offspring begging displays, in which case offspring beg- ging would be evolutionarily unstable because offspring would be under selection to cease begging. Thus, the key issue has been to understand the conditions under which offspring begging signals can be evolutionarily stable given that parents and offspring have conflicting evolutionary interests. Evolutionary game theory is the principal theoretical tool for examining the conditions under which offspring begging and parental responsiveness to begging can be evolutionarily stable (Godfray 1995a). The vast majority of such models have been based on the assumption that begging incurs some form of cost to the offspring (Johnstone and Godfray 2002 Moreno- Rueda 2007). Both honest signaling (Godfray 1991, 1995b Johnstone 2004) and scramble competition models (Rodr ́ıguez- Girone ́s et al. 1996 Parker et al. 2002), which are the most widely cited models for the evolution of begging, suggest that costly begging provides an evolutionarily stable resolution to parent–offspring conflict. The reason is that begging costs effectively punish offspring misrepresenting their true need, thereby allowing parents to obtain honest and reliable infor- mation on the offspring’s needs by monitoring offspring beg- ging signals (Godfray 1991, 1995b Parker et al. 2002). However, not all models for the evolution of begging are based on the assumption that begging is costly. Maynard Smith (1991, 1994) and Bergstrom and Lachmann (1997, 1998) showed that cost-free or low-cost offspring begging might be evolutionarily stable because parents and offspring have over- lapping interests. Thus, empirical information on the costs of begging are needed to assess the relevance of alternative the- oretical models for the evolution of offspring begging signals.

Empirical studies, all of which have been conducted on birds, have provided mixed and ambiguous evidence regarding the costs of offspring begging (Chappell and Bachman 2002 Haskell 2002 Moreno-Rueda 2007). Such studies have fo- cused mainly on energy costs (Chappell and Bachman 2002) and predation costs (Haskell 2002). Begging is thought to be energetically costly because higher begging levels increase the offspring’s metabolic rate, which in turn decreases the off- spring’s growth rate (Kilner 2001). Studies on energy expen- diture suggest that begging nestlings increase their metabolic rate by less than 30% of their baseline metabolic rate (Chappell and Bachman 2002). Although such an increase in metabolic rate may seem insignificant, there is evidence that begging is associated with a substantial growth cost (Kilner 2001 Rodr ́ıguez- Girone ́s et al. 2001). Studies on canaries and magpies sug- gest that begging incurs an energy cost that translates into reduced growth (Kilner 2001 Rodr ́ıguez-Girone ́s et al. 2001), although a study on collared doves found no evidence of such a growth cost (Rodr ́ıguez-Girone ́s et al. 2001). In birds, beg- ging is also thought to incur a predation cost because preda- tors could use begging calls to locate nests. However, studies on altricial birds have so far provided limited and ambiguous evidence for a predation cost (Haskell 2002). For example, anexperimental study on artificial nests suggests that begging calls might increase predation risk in ground-nesting birds but that this is not the case in tree-nesting birds (Haskell 1994).

In order to advance our understanding of the role and na- ture of begging costs, it is now timely to extend empirical re- search to include nonavian species in which the offspring beg for food from their parents. One such species is the burying beetle Nicrophorus vespilloides. This species has recently at- tracted interest as a nonavian study system for the evolution of offspring begging and parental care (Smiseth and Moore 2002, 2004a, 2004b, 2007 Smiseth et al. 2003 Lock et al. 2004 Smiseth, Lennox, and Moore 2007 Smiseth, Ward, and Moore 2007 Crook et al. 2008). Conveniently, this species breeds readily in the laboratory, where confounding factors can be effectively controlled, and generally behaves in the laboratory as it does in the field (Eggert and Mu ̈ller 1997). Like all burying beetles, N. vespilloides breeds on carcasses of small vertebrates, which is the sole food source for the developing larvae (Scott 1998). Parents provide care by creating an open- ing in the carcass within which the larvae feed, directly pro- visioning the larvae with predigested carrion, cleaning the carcass of bacterial and fungal growth, and defending the brood against predators and congeneric competitors (Eggert and Mu ̈ller 1997 Eggert et al. 1998 Scott 1998 Trumbo 2007). The larvae can feed independently but will also beg for food from their parents (Smiseth and Moore 2002 Smiseth et al. 2003). The larvae beg by raising their head toward the parent while waving their legs or touching the parent with their legs (Rauter and Moore 1999). The larvae beg to signal their hunger levels (Smiseth and Moore 2004b, 2007), and the parents respond to begging by adjusting their resource allocation (Smiseth and Moore 2002, 2004b).

The aim of this study was to test for evidence of begging costs in N. vespilloides. Larval begging may incur energy costs, which in turn decrease the offspring’s growth rate as reported for some birds (Kilner 2001 Rodr ́ıguez-Girone ́s et al. 2001). How- ever, it is unlikely that larval begging would incur predation costs because begging is tactile and short ranged, making it unlikely that it would attract attention from predators. In- stead, begging might incur an opportunity cost because larvae cannot self-feed and beg at the same time. Thus, begging larvae may suffer a cost through a loss in the time spent self- feeding. To test whether larval begging incurs an energy and/ or an opportunity cost, we used a novel experimental design, in which we independently manipulated the presence or ab- sence of parents and the presence or absence of food. Pre- vious studies show that larvae only beg in the presence of a parent (Rauter and Moore 1999 Smiseth and Moore 2002). Thus, to stimulate larval begging without introducing confounding effects on growth due to food obtained from the parent, we provided the larvae with a dead parent. A pilot experiment confirmed that larvae would indeed beg to dead parents. If larval begging incurs an energy cost, we expected larvae to grow less well in the presence of a dead parent than in its absence. We also manipulated the presence or absence of food to test for an opportunity cost of begging. If there was such a cost, we expected that larvae with access to food should grow less well when presented with a dead parent than when not presented with a dead parent. In other words, we ex- pected an effect of the interaction between the 2 treatments on larval growth.

MATERIALS AND METHODS

We used beetles from an outbred laboratory population de- rived from over 100 wild-caught N. vespilloides females trapped in a deciduous forest in August 2003 at Sunbank Wood, Man-

chester, England. Beetles were housed individually in clear plastic containers (17 3 12 cm area and 6 cm high) under a 16:8 h light:dark cycle at 20 6 1 #176C. The beetles were fed scraps of meat ad libitum twice a week. We randomly selected pairs of nonsibling virgin males and females for breeding. Each pair was placed in a new container filled with about 2 cm of moist soil and provided with a previously frozen mouse carcass (range 20㪱 g) supplied from Livefoods Direct Ltd, Sheffield, England. Two days after the female had started lay- ing eggs and before the eggs hatched, the female and the carcass were transferred to a new container filled with 2 cm of moist peat. The male was removed at this stage because male assistance in food provisioning has no detectable effect on larval growth or survival (Mu ̈ller et al. 1998 Smiseth et al. 2005). The eggs were left to hatch in the old container, which was checked for the presence of newly hatched larvae 4 times a day. The newly hatched larvae were used to establish exper- imental broods comprising 15 larvae, which is well within the natural variation with respect to brood size in N. vespilloides (mean 6 standard deviation brood size: 21 6 10 offspring, range 2㫇 larvae Smiseth and Moore 2002). Broods were al- ways established so that they contained larvae of mixed ma- ternity. We provided females with broods only after their own eggs had started hatching because females exhibit temporal kin recognition, killing larvae that arrive before but accepting larvae that arrive after their own eggs have started to hatch (Mu ̈ ller and Eggert 1990).

We conducted the experiments exactly 24 h after the larvae had been placed on the carcass, which corresponds to the age at which the larvae had reached the second instar and the peak in larval begging (Smiseth et al. 2003). We excluded broods where more than 5 out of the 15 original larvae placed with a female had died (n 1𔊬 8), thus restricting our manipulations to those broods where at least 10 larvae had survived (n 1𔊬 120). The female was removed 30 min before the start of the experiment and was killed by being placed in a 220 #176C freezer. Five min before the start of the experiments, the fro- zen female was taken out of the freezer to thaw. The larvae were then removed from the carcass and placed in a small transparent container lined with moist paper. The broods were randomly assigned to the 4 treatment groups: 1) with a dead parent and with food, 2) with a dead parent and with- out food, 3) without a dead parent and with food, and 4) without a dead parent and without food. The broods that were given access to food were provided a small piece (ca., 1מ g) of carrion from a prepared mouse carcass. The broods that were provided with a dead parent were always provided with the female that previously had provided them with care.

At the start of the experiment and exactly 24 h after the lar- vae had been placed on the carcass, we weighed the whole brood at once to the nearest 0.1 mg and recorded the number of larvae in the brood. We later calculated the average larval body mass in the brood by dividing the brood mass by the num- ber of larvae. Five minutes later, we recorded larval begging by instantaneous scan sampling (Martin and Bateson 1986) every 1 min for 10 min. This procedure was repeated after 55 min and after 105 min. At each scan, we counted the number of larvae that were begging. A larva was considered to be begging when it raised its head toward the parent while waving its legs or touching the parent with its legs (Rauter and Moore 1999). We calculated the average percentage of time spent begging by each larva in the broods during each 10-min observation period as B 1𔊬 (Rb/n) 3 (100/10), where Rb is the total num- ber of begging events during an observation session and n is the number of larvae in the brood. At the end of the exper- iment and exactly 2 h after the larvae had been weighed for the first time, we weighed the whole brood again and re- corded the number of larvae in the brood. Statistical methods

We used repeated-measures general linear models (GLM) to test whether larvae changed their begging behavior through- out the experiment. In this analysis, we used time of observa- tion as a within-subject factor with 3 levels (i.e., each of the three 10-min observation periods), whereas the presence or absence of food was entered as a between-subjects factor with 2 levels. We used GLM to test for effects of the presence or absence of food and the presence or absence of a dead parent on the weight change during the experiment. All variables used in the statistical analyses were either normally distributed or subject to square root transformations to achieve a normal distribution. All tests were 2 tailed, and the significance level was set at P 1𔊬 0.05.

RESULTS

Larvae that had not been provided with a dead parent were never observed begging. These broods were therefore ex- cluded from further analyses on larval begging. In contrast, lar- vae that had been provided with a dead parent begged throughout the treatment period (Figure 1). The time of ob- servation had no significant effect on the amount of time spent begging, implying that larval begging behavior re- mained at a fairly constant level throughout the 2-h treatment period (repeated-measures GLM, within subjects: F1,58 1𔊬 2.59, P 1𔊬 0.11). The presence or absence of food had a significant effect on the amount of time spent begging by the larvae (repeated-measures GLM, between subjects: F1,58 1𔊬 34.30, P , 0.001). Larvae spent less time begging when they had access to food than when they had no access to food (Figure 1). There was no significant effect of the interaction between time of observation and the presence or absence of food (repeated- measures GLM, within subjects: F1,58 1𔊬 2.69, P 1𔊬 0.072), al- though visual inspection of the data suggests that larvae that had no access to food may have increased their begging be- havior somewhat during the treatment period while larvae that had access to food begged at a fairly constant level throughout the treatment period. As expected, the presence or absence of food had a highly significant effect on larval growth (GLM: F1,116 1𔊬 185.33, P , 0.001). Larvae with access to food grew about 0.7 mg during the 2-h treatment period, whereas larvae without access to food lost a similar amount of body mass (Figure 2). In con- trast, the presence or absence of a dead parent had no signif- icant effect on larval growth (GLM: F1,116 1𔊬 1.17, P 1𔊬 0.28 Figure 2). Thus, there was no evidence that larvae that were stimulated to beg through the presence of a dead parent grew less well than larvae that were not presented with a dead par- ent. Finally, there was no significant effect of the interaction between the presence or absence of food and the presence or absence of a dead parent (GLM: F1,116 1𔊬 0.42, P 1𔊬 0.52 Figure 2). Indeed, larvae that were provided with food and a dead parent grew just as well as larvae that were provided with food but not with a dead parent (Figure 2). Thus, there was no evidence that larval begging incurred an opportunity cost.

DISCUSSION

Our study is the first to test for begging costs in a nonavian species. If begging incurred an energy cost translating into re- duced larval growth, we expected larvae to grow less well when they had access to food and to lose more weight when they had no access to food when stimulated to beg through the presence of a dead parent. However, we found no significant difference in the change in larval body mass in the presence or the ab- sence of a dead parent. If anything, visual inspection of Figure 2 suggests that there was a nonsignificant trend for larvae without access to food to lose more weight when not pre- sented with a dead parent, which is in opposite direction of what we expected if begging incurred an energy cost. We also tested for an opportunity cost of begging. Such opportunity costs would not be found in altricial birds, which receive all their food from the parents, but may occur in partially beg- ging species, such as N. vespilloides, in which the offspring obtain some food by self-feeding and some by begging (Smiseth et al. 2003). If there was an opportunity cost of begging, we expected an effect of the interaction between our 2 treatments because larvae with access to food should grow less well in the presence than in the absence of a deadparent. However, we found no effect of the interaction be- tween our 2 treatments, and larvae that were provided with food and with a dead parent grew just as well as larvae that were provided with food but not with a dead parent. Thus, our study provides no evidence in support of the suggestion that larval begging in N. vespilloides incurs energy or opportunity costs.

Although we found no evidence in support of begging costs in our study, we cannot completely exclude the possibility of undetected begging costs in N. vespilloides. First, our study may have had a relatively low statistical power because we measured growth over a short period of 2 h. We settled for a treatment period of 2 h because a previous pilot experiment suggested that cannibalism of dead or live larvae might some- times occur when larvae are kept without food over a period of 4ע h (Smiseth PT, unpublished data). Thus, keeping in mind that N. vespilloides larvae grow extremely rapidly at this stage in their development, a treatment period of 2 h provided the best possible balance between recording data on weight changes without introducing problems due to mortality and cannibalism. Average larval growth over 2-h period at this stage in development is 1.33 mg when larvae receive care from their parents (Smiseth and Moore 2004b) and 0.7 mg when larvae forage by self-feeding only (Figure 2). We estimate that the minimum detectable difference for the presence or ab- sence of a dead parent was equal to a change in body mass of 0.24 mg, assuming a statistical power of 0.8, a sample of 60 broods in each treatment level, and a within-group variance of 0.38 as estimated from our data (Zar 1984 Equation 13.36). Thus, our 2-h treatment period would have been sufficient to detect a substantial growth cost in N. vespilloides, although it would not have been sufficient to detect a small growth cost.

Second, although our study shows that the presence of a dead parent stimulates larval begging, larvae may beg less fre- quently and/or less intensively than when cared for by a live parent. Indeed, the larvae in our experiment spent only around 3ע% of their time begging, which is somewhat lower that the 7㪤% reported for broods cared for by a live parent (Smiseth et al. 2003 Smiseth, Lennox, and Moore 2007 Smiseth, Ward, and Moore 2007). Thus, we cannot exclude possibility that there might a begging cost in natural broods cared for by a live parent where begging levels are higher. Nevertheless, we believe that our method of stimulating larval begging through the presence of a dead parent provides the best available method for detecting begging costs because it prevents confounding effects on larval growth due to parental food provisioning, which would have been inevitable had we used a live parent.

The lack of evidence for any significant costs of begging lends some support to cost-free or low-cost models of begging (Maynard Smith 1991, 1994 Bergstrom and Lachmann 1997, 1998). This suggestion is supported by additional indirect evidence suggesting that larval begging in N. vespilloides is cost free or has a low cost. First, begging signals in this species appear to be discrete (i.e., larvae either beg or not beg Smiseth and Moore 2004b) rather than graded as they are in birds (i.e., nestling begging varies in intensity Kilner and Johnstone 1997 Budden and Wright 2001). Theoretical con- siderations suggest that only costly begging signals can pro- vide graded information on offspring need, whereas cost-free begging signals are discrete and consequently less informative (Johnstone and Godfray 2002). Second, because larval beg- ging in N. vespilloides is tactile (Rauter and Moore 1999 Smiseth and Moore 2002), larval begging will be short ranged and therefore unlikely to attract attention from predators. Models of cost-free and low-cost begging have so far received less atten- tion from empiricists than models of costly begging (Kilner and Johnstone 1997 Budden and Wright 2001 Wright and

Leonard 2002). In birds, where offspring begging signals do appear to provide graded information, there is some evidence that begging is costly (Kilner 2001 Rodr ́ıguez-Girone ́s et al. 2001). Nevertheless, discrete and cost-free begging signals may be more common than hitherto recognized, in particular among nonavian species. Thus, we encourage empiricists and specially those studying nonavian species, to take cost-free and low-cost models into consideration.

Our study also shows that larval begging in N. vespilloides is stimulated by the presence of a dead parent, although the larvae beg less frequently than when cared for by a live parent, presumably because the dead parent provides no food in re- sponse to begging. Nevertheless, the use of a dead parent provides a valuable research tool for stimulating larval beg- ging while preventing confounding effects of parental food provisioning on larval growth. Interestingly, the finding that larval begging is stimulated by the presence of a dead parent suggests that the larvae somehow recognize their parents as appropriate stimuli independently of the parents’ behavior. Instead, the larvae may respond to other cues from their pa- rents, such as olfactory or gustatory cues based on cuticular hydrocarbons or the physical shape of the parent. We encour- age further research to investigate these issues.

In conclusion, our study suggests that neither energy nor op- portunity costs of begging have significant effects on larval growth in N. vespilloides. The issue of begging cost is essential to our understanding of the evolution of offspring begging signals, and we strongly encourage further empirical work on the potential costs of begging in both avian and nonavian species to further advance our understanding of the nature and role of begging costs. Indeed, insects such as the burying beetle N. vespilloides (Smiseth and Moore 2002, 2004a, 2004b, 2007 Smiseth et al. 2003 Lock et al. 2004 Smiseth, Lennox, and Moore 2007 Smiseth, Ward, and Moore 2007 this study) and the earwig Forficula auricularia (Ko ̈lliker 2007) may pro- vide particularly valuable model systems in this respect because these species are well suited for large-scale experi- ments and can be studied under standardized conditions in the laboratory.

FUNDING

Natural Environment Research Council (NE/C002024/1) The University of Manchester.

We thank the Mersey Valley Countryside Warden Service and Alan Barton, the Mersey Valley ecologist, for permission to collect beetles on their property at Sunbank Wood, Manchester. We thank Michelle Scott and two anonymous reviewers for valuable comments on the manuscri pt.

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