Regular articleUrinary C-peptide levels in male bonobos (Pan paniscus) are related to party size and rank but not to mate competition
Introduction
Competition among males over access to fertile females in group-living species often leads to the establishment of dominance hierarchies in the males (Hager and Jones, 2009), with those occupying higher ranks frequently enjoying priority of access to mates (Altmann, 1962). Although there is variation in male mating strategies between species and even within social groups, including coalition formation, queuing and sneaking copulations, a prominent strategy observed in many taxa is mate guarding (insects: Alcock, 1994; reptiles: Ancona et al., 2010; birds: Komdeur, 2001; mammals: Willis and Dill, 2007). Mate guarding, during which dominant males try to maintain sole mating access to fertile females, is one mechanism by which rank differences among males translate into skewed mating among those males. While representing a strategy that increases paternity success, mate guarding has been shown to be a trade-off with elevated metabolic costs due to higher rates of agonistic and sexual activities (Ancona et al., 2010) and due to constrained feeding behavior (Alberts et al., 1996, Komdeur, 2001). Although metabolic costs of mate competition can arise under different mating systems, they seem particularly high among high ranking individuals and in species that mate guard over extended periods as these factors lead to negative energy balances (i.e.: when energy intake is lower than energy expenditure; Lane et al., 2010). The resulting energetic stress may not only result in a substantial decrease in male body mass (Bernstein et al., 1989), but may even lead to a decrease of short-term reproductive success (Lidgard et al., 2005) and to increased male mortality (Hoffman et al., 2008). In some extreme cases (e.g. gray seals: Lidgard et al., 2005; Rhesus macaques: Higham et al., 2011b), termed “endurance rivalry”, male mating effort over extended periods is constrained by energy availability. Yet, the metabolic costs of mate guarding and high ranks are not consistent across species. While some studies in primates find that mate guarding and general mating effort are associated with reduced feeding time (Alberts et al., 1996, Georgiev, 2012), weight loss and nutritional stress in high ranking individuals (Bercovitch and Nürnberg, 1996, Higham et al., 2011b, Setchell and Dixson, 2001), others find neither an association with measurements of energy intake and expenditure (Huck et al., 2004, Mass et al., 2009, Weingrill et al., 2003) nor rank related patterns of nutritional stress during mating seasons (Schülke et al., 2014). Variation across studies might be explained by methodological differences (Alberts et al., 1996, Schülke et al., 2014) or by adaptive differences in energy allocation during mate competition across species (Georgiev, 2012, Girard-Buttoz et al., 2014b, Schülke et al., 2014). Another possibility is that the metabolic costs of mate guarding or high rank can be compensated by a reduction of energetically costly activities in another context such as vertical locomotion (Girard-Buttoz et al., 2014a). Nevertheless, males of species in which the maintenance of high rank depends on physical strength are expected to allocate energy differently than species in which social strategies such as pair-bonding or coalition formation are crucial for reproductive success (Schülke et al., 2014). While most primate studies have focused on metabolic costs in seasonal breeders, little is known about species with aseasonal breeding that might face more persistent costs over extended amounts of time with fewer opportunities for metabolic recovery (Emery Thompson and Georgiev, 2014). This study addresses the question of how male energy balance is affected by long lasting, aseasonal mate competition in bonobos (Pan paniscus), a species with fission–fusion dynamics and a lack of male priority of access to food.
Costs associated with mate competition, and with intragroup competition over food resources, are incurred by males living in groups containing several individuals of both sexes. Since feeding competition is hypothesized to have a stronger effect on female reproductive success, most studies focus on the metabolic costs of female gregariousness (e.g. Ebensperger et al., 2011, Emery Thompson et al., 2012a, Emery Thompson et al., 2012b, Pride, 2005; but Isbell and Young, 1993). However, rank related skew in access to food and the consequential costs of increased gregariousness may also lead to rank differences in energy balance among males. This phenomenon might be particularly prominent in species where females are dominant and therefore possess priority of access to food resources. It remains unclear as to whether or not high ranking males would have a more positive energy balance than low ranking males during periods of mate competition in such scenarios.
It has been hypothesized that some group-living species deal with decreases in food availability and increases in competition within groups by temporarily fissioning into smaller parties (Aureli et al., 2008). Consequently, in order to attenuate the effects of reduced food availability in the environment, party sizes are expected to be smaller during times of food scarcity. This function of fission–fusion dynamics has been supported in primates by findings that parties are small when fruit is scarce and large when fruit is more abundant (Anderson et al., 2002, Chapman et al., 1995, Cobden, 2014; but Rimbach et al., 2014, Smith et al., 2008). While a number of other factors have been shown to influence party size including the presence of females that exhibit visual signs of fertility (Anderson et al., 2002, Matsumoto-Oda et al., 1998) and predation pressure (Boesch, 1991), few attempts have been made to quantify the effects of different party sizes on the energy balances of males (Georgiev, 2012). This study explores links between male energy balance and grouping patterns in bonobos.
In wild living populations it is often difficult to quantify rank related metabolic costs or energetic stress. A classic approach to quantifying these costs has been by measuring glucocorticoid levels (e.g. Barrett et al., 2002, Goymann and Wingfield, 2004, Muller, 2004). This method however has the disadvantage that elevated levels can result not only from metabolic stress, but also from social or psychological stress (Abbott et al., 2003, Creel, 2001). For example, in baboons it has been proposed that during times of stable dominance hierarchies, high glucocorticoids in alpha males are primarily caused by energetic stress, whereas high glucocorticoids in low-ranking males are largely caused by social stressors (e.g., high rates of received aggression, a lack of a sense of control, and few coping mechanisms; Gesquiere et al., 2011). While several species seem to share the pattern with baboons, the generality of this notion is unclear and rank-related glucocorticoid levels are often still hard to interpret. A more specific approach to quantifying metabolic stress is by measuring urinary C-peptide levels (UCP levels; Sherry and Ellison, 2007). C-peptide is cleaved off from proinsulin during the activation of insulin which is produced when glucose levels are elevated in the blood. The C-peptide level of an individual therefore acts as a marker of energy balance, with high C-peptide levels indicative of a more positive energy balance than low levels. Several studies have already demonstrated the use of C-peptide in tracking energy balance in captive and wild living primates (bonobos: Deschner et al., 2008, Georgiev et al., 2011; orangutans: Emery Thompson and Knott, 2008; chimpanzees: Emery Thompson et al., 2009; macaques: Girard-Buttoz et al., 2011; gorilla: Grueter et al., 2014; guereza: Harris et al., 2010).
We measured the UCP levels of wild male bonobos to investigate how mate competition and party size affect the energy balance.
Bonobos live in multi-male, multi-female societies in which males normally remain in their natal community (Kano, 1992, Schubert et al., 2011). Females exhibit visual signs of fertility in the form of extended periods of genital swellings during interbirth intervals (Furuichi and Hashimoto, 2002). As changes of genital swellings do not always correlate with specific reproductive stages (Reichert et al., 2002), detectability of ovulation by males may be constrained, making intense efforts of mate guarding a costly strategy. Nevertheless, there are some indications that mate guarding is a male mating strategy in bonobos: Firstly, high ranking males spend more time in proximity to females with maximally tumescent swellings (Surbeck et al., 2012b). Secondly, staying in close proximity of maximally tumescent females is associated with an increase in male cortisol levels (Surbeck et al., 2012b). These elevated cortisol levels may be indicators of elevated metabolic stress due to mate guarding activity since the feeding time of bonobo males close to maximally tumescent females is also decreased (Surbeck et al., 2012b). While such a decrease in feeding time has been associated with increased vigilance and male aggression in other species (Ancona et al., 2010, Chuang-Dobbs et al., 2001), the latter does not apply to bonobos because the general presence of maximally tumescent females does not increase male aggression (Surbeck et al., 2012a). However, reduced aggression towards fertile females in the form of mate guarding without coercive mating may also result in decreased feeding opportunities (Surbeck and Hohmann, 2013). This “Metabolically costly mate guarding” hypothesis implies that energetically costly mate-guarding is a male mating strategy in bonobos and predicts rank related patterns of UCP levels only in the presence of maximally tumescent females with high ranking males having lower UCP levels.
Energetic costs of aggression have been demonstrated in several vertebrates (Southwick, 1967, Marler and Moore, 1989). In chimpanzees, energetically costly aggressive behavior is essential for the maintenance of high ranks even in the absence of maximally tumescent females (Georgiev, 2012). Aggressive behavior is more likely to explain differences in male energy balances than other energetically costly behaviors such as traveling (Emery Thompson et al., 2009). Results from one bonobo community indicate that high ranking males are also more aggressive than low ranking males and that the presence of maximally tumescent females that are close to conception (potentially fertile females) leads to an overall increase in male aggression (Surbeck et al., 2012a). The “metabolically costly aggression” hypothesis assumes that aggression is always energetically costly and, consequently, predicts that aggression negatively influences the energy balance of males. Therefore, we would expect permanently lower C-peptide levels in high ranking males. Given that the presence of potentially fertile females is associated with elevated levels of male aggression, a decrease in C-peptide levels in all males is predicted. Furthermore, as aggression frequency increases on mating days (Hohmann and Fruth, 2003), we would also expect copulation rates to correlate with C-peptide levels.
The energy balance of males may vary with changes in male gregariousness rather than mate guarding effort and a variety of scenarios concerning male grouping costs are possible.
If larger parties are due to the presence of maximally tumescent females, predation pressure, or proximity to neighboring communities and not to higher food availability, we would expect that males are more likely to experience higher metabolic costs and lower UCP levels when traveling in larger parties because per capita food availability decreases. The same pattern would emerge if overall individual energetic expenditure increases with party size. However, if larger parties are mainly formed during times of high food abundance, we would not expect a decrease in mean UCP with increasing party size because per capita food availability would remain constant. While the relationship between party size and energy balance in males allows for distinguishing some main hypotheses concerning the grouping dynamics of bonobos, data on energy expenditure such as travel distance, general food availability and female energy balance are necessary to explore these factors in more detail.
Male energy balance might also vary according to dominance rank independent of male mating strategies because high ranking males have priority of access to monopolizable food over low ranking males or occupy qualitatively better feeding spots (Kahlenberg, 2006). This would lead to observing rank related differences in UCP levels with higher ranking males having higher UCP levels. Furthermore, in bonobos, the presence of mothers has been shown to influence male mate access (Surbeck et al., 2011) and it is possible that the presence of mothers might also affect a son's access to other resources such as food. For an overview of the hypotheses and predictions see Table 1.
Section snippets
Ethics statement
Permits to conduct research at LuiKotale in Salonga National Park, Democratic Republic of Congo were granted by the Institut Congolais pour la Conservation de la Nature (ICCN) in Kinshasa, Democratic Republic of Congo.
Study site and subjects
Data collection was conducted on the Bompusa bonobo community between December 2007 and July 2009 at the LuiKotale field site in Salonga National Park, Democratic Republic of Congo. During the study period, the community consisted of 33–35 individuals, which included five adult
UCP levels of male bonobos
The medians of individual UCP levels ranged from 0.98–2.80 ng/mg Cr (overall range of UCP levels is from 0.18 to 57.65 ng/mg Cr). Although we only used early morning samples, we additionally included collection time into our analysis. The time of sample collection was not significant (daytime: GLMM estimate ± SE = 0.128 ± 0.06, P = 0.11). Furthermore, UCP levels did not exhibit significant seasonal variation (season as the simple sine shaped curve with the maximum at a previously undefined date: GLMM
Discussion
Measuring UCP levels in male bonobos, a species with linear male dominance hierarchies, we found no indication that mate competition negatively affects the energy balance of males. The positive correlation between mean monthly UCP levels and mean party size indicates a link between energy balance and fission–fusion dynamics in male bonobos, that is, males exhibit increased gregariousness when they can afford to do so. Comparing mean daily party sizes with UCP levels early next morning shows
Conclusion
Measures of UCP show that rank related differences in behavior during mate competition in male bonobos do not affect the energy balance. This suggests that mate guarding and other forms of mate competition by male bonobos are energetically neutral which might be linked to the low predictability of ovulation in females, which renders costly forms of mate competition ineffective and promotes alternative strategies which are independent of physical strength. When traveling in large parties high
Acknowledgments
The Institut Congolais pour la Conservation de la Nature (ICCN) granted permission to conduct field research and for exporting urine samples to Germany. The fieldwork of MS at LuiKotale was supported by the Max-Planck-Society, the L.S.B. Leakey Foundation (Award check no. 2507), Basler Stiftung für Biologische Forschung and the Swiss National Science Foundation (PBSKP3_145844). We thank Barbara Fruth for the inspiring discussions and support through the various stages of the project, Roger
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2020, Hormones and BehaviorCitation Excerpt :C-peptide is excreted at a consistent rate into urine and, in contrast to insulin, can be assessed from urine samples, enabling the repeated and non-invasive assessment of energetic condition (Emery Thompson, 2016), even in wild study populations. Associations between urinary C-peptide (uCP) and energy balance (or proxies thereof) have been demonstrated in various non-human primate species, including effects of body mass and experimentally induced weight change (e.g. fasting, provisioning) (e.g. Wolden-Hanson et al., 1993; Deschner et al., 2008; Girard-Buttoz et al., 2011), food and fruit availability and intake (e.g. Emery Thompson and Knott, 2008; Emery Thompson et al., 2009; Harris et al., 2009; Grueter et al., 2014), as well as energetic aspects of the social environment, e.g. dominance rank (Sherry and Ellison, 2007; Emery Thompson et al., 2009; Higham et al., 2011a; Lodge, 2012; Surbeck et al., 2015). Furthermore, age and sex (Thompson et al., 2020) as well as female reproductive state have been shown to affect uCP (e.g. Emery Thompson et al., 2012; McCabe et al., 2013; Nurmi et al., 2018; but see Lodge, 2012; Grueter et al., 2014).
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2020, Journal of Human EvolutionCitation Excerpt :Specifically, one could compare if rates of feeding, feeding-related displacement and aggressions, and general activity rates differ between Pan populations at different ages and then examine how variation in these behavioral variables relates to elevations in cortisol levels. Using urinary C-peptide concentrations, it would also be possible to examine how these behavioral data relate to energy balance (Deschner et al., 2008; Emery Thompson et al., 2009; Girard-Buttoz et al., 2011; Surbeck et al., 2015). In Pan, population density (the number of individuals per km2) influences intergroup competition and encounter frequency, making it a major predictor for rates of violence and killings, especially intergroup infanticide in different populations (Wilson et al., 2014).
The costs of living at the edge: Seasonal stress in wild savanna-dwelling chimpanzees
2018, Journal of Human EvolutionCitation Excerpt :Females were assigned ranks below males, and individuals (two pairs) tied in score were assigned identical ranks. As chimpanzees are known to vary their party sizes as a means of mitigating potential food resource competition (Chapman et al., 1995; Anderson et al., 2002) and this measure is known to correlate with c-peptide levels in bonobos (Surbeck et al., 2015), we controlled for average party size observed for the focal individual on the day prior to each sample in the c-peptide model. Party size measurements differed among observers at Fongoli; parties were measured as all individual chimpanzees observed over the course of a day, or summarized to daily means based on all visible individuals every 15 min collected during focal follows.