Social attributes and associated performance measures in marmots: bigger male bullies and weakly affiliating females have higher annual reproductive success

Studying the structure of social interactions is fundamental in behavioral ecology as social behavior often influences fitness and thus natural selection. However, social structure is often complex, and determining the most appropriate measures of variation in social behavior among individuals can be difficult. Social network analysis generates numerous, but often correlated, measures of individual connectedness derived from a network of interactions. We used measures of individual connectedness in networks of affiliative and agonistic interactions in yellow-bellied marmots, Marmota flaviventris, to first determine how variance was structured among network measures. Principal component analysis reduced our set of network measures to four “social attributes” (unweighted connectedness, affiliation strength, victimization, and bullying), which revealed differences between patterns of affiliative and agonistic interactions. We then used these extracted social attributes to examine the relationship between an individual’s social attributes and several performance measures: annual reproductive success, parasite infection, and basal stress. In male marmots, bullying was positively associated with annual reproductive success, while in females, affiliation strength was negatively associated with annual reproductive success. No other social attributes were significantly associated with any performance measures. Our study highlights the utility of considering multiple dimensions when measuring the structure and functional consequences of social behavior.     

Individual differences in the behavior of juvenile yellow-bellied marmots

Summary Yellow-bellied marmots express considerable individuality as measured by behavior in a maze, mirror-image stimulation (MIS), and social behavior in the field. Maze behavior discriminated between residents and dispersers; residents explored the maze more widely than did dispersers. Males could not be distinguished from females nor survivors from non-survivors by their maze behavior. A group of six yearling females was established to examine the relationship between individual behavioral phenotypes (as determined by MIS) and social behavior in the field. This experiment provided a situation in which social behavior was not influenced by age, sex, or reproduction (female yearlings are non-reproductive). The number of social interactions per individual ranged from 25 to 69. The number of observed interactions per individual differend significantly from the expected for greeting, allogrooming, total amicable, play, and total social interactions. Rankings of greeting, total amicable, and total interactions were directly correlated with rankings on the avoidance axis; play was inversely correlated with the approach axis. These results suggest that marmots have individual behavioral phenotypes that are expressed in their social interactions with their conspecifics.     

Foraging patterns of yellow-bellied marmosts: role of kinship and individual variability

Summary Two colonies of yellow-bellied marmots (Marmota flaviventris) at an elevation of 2900 m in Colorado were studied to elucidate the role of various behavioral and ecological factors as determinants of spatial foraging patterns. The locations of known individuals were periodically recorded. These locality data were plotted as three-dimensional block diagrams, the peak heights representing the frequency of observation. Predation risk and vegetation distribution influenced the location of foraging areas; kinship was an important factor in the determination of the amount of foraging area shared between individual marmots. Spatial overlap tended to be greater among close kin, but this was modified by individual behavioral characteristics, reproductive state, the existence of separate burrow systems within a colony, and the age of the animal. Mothers and juveniles, and littermates as young and resident yearlings, had nearly identical foraging areas.     

Kinship,reproductive strategies and social dynamics of yellow-bellied marmots

Summary Social behavior of yellow-bellied marmots was observed for three years in colonies where kinship was known and for one year in a high elevation colony where harems were contiguous. Social dynamics of yellow-bellied marmots is dependent on kinship, group composition, and age-sex classes. This pattern is a consequence of the reproductive strategies of males and females. Females behave cohesively toward sisters or daughters, but not with sons and agonistically toward other females. Males generally behave amicably toward females and agonistically toward males, including their sons. Thus, reproductive strategies limit nepotism. This behavior is consistent with a population process in which sons typically disperse as yearlings. At least some of the variation in the expected patterns of social behaviors is attributable to individual differences. Because male and female reproductive strategies differ, a marmot population consists of two social subsystems. The female unit is the closely-related kin group which may also be a burrow group. The male unit is a harem which usually consists of two or more competing female kin groups.     

The evolution of marmot sociality: II. Costs and benefits of joint hibernation

Summary Social groups of alpine marmots (Marmota marmota) were studied for 7 years. The groups consisted of a territorial pair and up to 18 lower ranking animals of various ages, mostly the pair's offspring (Tables 1, 2). Group members lived in a common home range and always hibernated together in one hibernaculum. Groups with older, subordinate animals experienced slightly higher summer mortality but significantly reduced winter mortality (Fig. 1). Infant winter mortality was further decreased if most older subordinates were potentially their full sibs (Fig. 2). Subordinate group members lost less mass during winter with increasing size of the hibernating group, but this trend was reversed when infants were present. Furthermore, augmented mass loss due to low hibernaculum quality became evident (Fig. 3). Apart from these effects, the presence of infants caused additional mass loss in potential full sibs. The opposite was found in subordinates certainly descending from other parents than those of the infants (Table 3).Winter mortality and mass loss data revealed (i) a general benefit of joint hibernation, (ii) an unavoidable cost of infants' presence to other group members, (iii) that only potential full sibs helped in warming infants, (iv) that helping was energetically expensive and increased infant survival. The evolution of postponed dispersal in ground-dwelling squirrels has been attributed to the direct fitness gained by enhanced reproductive chances of offspring when not expelled from the natal territory (Armitage 1981, 1987, 1988). This study shows that group living in alpine marmots has benefits during winter and indicates the additional importance of kin selection in marmot social evolution.     

Do yellow-bellied marmots respond to predator vocalizations?

We conducted four experiments to determine whether yellow-bellied marmots, Marmota flaviventris, discriminate among predator vocalizations, and if so, whether the recognition mechanism is learned or experience-independent. First, we broadcast to marmots the social sounds of coyotes, Canis latrans, wolves, Canis lupus, and golden eagles, Aquila chrysaetos, as well as conspecific alarm calls. Coyotes and eagles are extant predators at our study site, while wolves have been absent since the mid-1930s. In three follow-up experiments, we reversed the eagle call and presented marmots with forward and reverse calls to control for response to general properties of call structure rather than those specifically associated with eagles, we tested for novelty by comparing responses to familiar and unfamiliar birds, and we tested for the duration of predator sounds by comparing a wolf howl (that was much longer than the coyote in the first experiment) with a long coyote howl of equal duration to the original wolf. Marmots suppressed foraging and increased looking most after presentation of the conspecific alarm call and least after that of the coyote in the first experiment, with moderate responses to wolf and eagle calls. Marmots responded more to the forward eagle call than the reverse call, a finding consistent with a recognition template. Marmots did not differentiate vocalizations from the novel and familiar birds, suggesting that novelty itself did not explain our results. Furthermore, marmots did not differentiate between a wolf howl and a coyote howl of equal duration, suggesting that the duration of the vocalizations played a role in the marmots’ response. Our results show that marmots may respond to predators based solely on acoustic stimuli. The response to currently novel wolf calls suggests that they have an experience-independent ability to identify certain predators acoustically. Marmots’ response to predator vocalizations is not unexpected because 25 of 30 species in which acoustic predator discrimination has been studied have a demonstrated ability to respond selectively to cues from their predators.     

Predation risk and foraging behavior of the hoary marmot in Alaska

Summary I observed hoary marmots for three field seasons to determine how the distribution of food and the risk of predation influenced marmots' foraging behavior. I quantified the amount of time Marmota caligata foraged in different patches of alpine meadows and assessed the distribution and abundance of vegetation eaten by marmots in these meadows. Because marmots dig burrows and run to them when attacked by predators, marmot-toburrow distance provided an index of predation risk that could be specified for different meadow patches.Patch use correlated positively with food abundance and negatively with predation risk. However, these significant relationships disappeared when partial correlations were calculated because food abundance and risk were intercorrelated. Using multiple regression, 77.0% of the variance in patch use was explained by a combination of food abundance, refuge burrow density, and a patch's distance from the talus where sleeping burrows were located. Variations in vigilance behavior (look-ups to search for predators while feeding) according to marmots' ages, the presence of other conspecifics, and animals' proximity to their sleeping burrows all indicated that predation risk influenced foraging.In a forage-manipulation experiment, the use of forage-enhanced patches increased six-fold, verifying directly the role of food availability on patch used. Concomitant with increased feeding, however, was the intense construction of refuge burrows in experimental patches that presumably reduced the risk of feeding. Thus, I suggest that food and predation risk jointly influence patch use by hoary marmots and that both factors must be considered when modeling the foraging behavior of species that can be predator and prey simultaneously.     

Effects of Tourists on Behavior and Demography of Olympic Marmots

Abstract:  If changes in animal behavior resulting from direct human disturbance negatively affect the persistence of a given species or population, then these behavioral changes must necessarily lead to reduced demographic performance. We tested for the effects of human disturbance on Olympic marmots ( Marmota olympus ), a large ground-dwelling squirrel that has disappeared from several areas where recreation levels are high. We assessed the degree to which antipredator and foraging behavior and demographic rates (survival and reproduction) differed between sites with high recreation levels (high use) and those with little or no recreation (low use). Compared with the marmots at low-use sites, marmots at high-use sites displayed significantly reduced responses to human approach, which could be construed as successful accommodation of disturbance or as a decrease in predator awareness. The marmots at high-use sites also looked up more often while foraging, which suggests an increased wariness. Marmots at both types of sites had comparable reproductive and survival rates and were in similar body condition. Until now, the supposition that marmots can adjust their behavior to avoid negative demographic consequences when confronted with heavy tourism has been based on potentially ambiguous behavioral data. Our results support this hypothesis in the case of Olympic marmots and demonstrate the importance of considering demographic data when evaluating the impacts of recreation on animal populations.     

The social network structure of a wild meerkat population: 2. Intragroup interactions

Knowledge of the structure of networks of social interactions is important for understanding the evolution of cooperation, transmission of disease, and patterns of social learning, yet little is known of how environmental, ecological, or behavioural factors relate to such structures within groups. We observed grooming, dominance, and foraging competition interactions in eight groups of wild meerkats (Suricata suricatta) and constructed interaction networks for each behaviour. We investigated relationships between networks for different social interactions and explored how group attributes (size and sex ratio), individual attributes (tenure of dominants), and ecological factors (ectoparasite load) are related to variation in network structure. Network structures varied within a group according to interaction type. Further, network structure varied predictably with group attributes, individual attributes, and ecological factors. Networks became less dense as group size increased suggesting that individuals were limited in their number of partners. Groups with more established dominant females were more egalitarian in their grooming and foraging competition interactions, but more despotic in their dominance interactions. The distribution of individuals receiving grooming became more skewed at higher parasite loads, but more equitable at low parasite loads. We conclude that the pattern of interactions between members of meerkat groups is not consistent between groups but instead depends on general attributes of the group, the influence of specific individuals within the group, and ecological factors acting on group members. We suggest that the variation observed in interaction patterns between members of meerkat groups may have fitness consequences both for individual group members and the group itself.     

Mate guarding and gallivanting by male hoary marmots (Marmota caligata)

Summary Seven years data on the vernal behavior of hoarty marmots, Marmota caligata, suggest that males engage in a two-part reproductive strategy, which consists of guarding their mates against possible copulation with additional males, and also gallivanting — wandering about in search of additional reproductive opportunities for themselves. Data are presented which support seven predictions derived from the assumption that mate guarding and gallivanting are parts of a reproductive strategy by male marmots.     

Dominance and fertility in a functionally monogynous ant

Summary Colonies of some leptothoracine ants may contain several inseminated but sterile females in addition to a single, fertile queen (functional monogyny). We here report the first observations on the behavior of these supernumerary females in the nearctic ant Leptothorax sp.A, a species belonging to the L. muscorum complex.In four colonies, each with up to eight intermorphic females, ritualized or openly aggressive interactions between individuals were observed, similar to those among workers of some other leptothoracine ants. The responses of individual females during encounters with nestmates apparently reflect the existence of linear dominance hierarchies. In each colony, the highest ranking individual was fed and groomed significantly more often than other females, and was the only one to oviposit after hibernation and to become fully physogastric during the first weeks of spring. When these -females were removed from three colonies, several other females started to lay eggs. However, in each colony only the highest ranking individual remained fertile; the others either were pushed out of the nest and finally killed by the workers, or their ovaries degenerated again.Aggressive interactions among females may also play an important role in the foundation of new colonies either by inducing intermorphs to leave the maternal nest to found new colonies solitarily or by inducing colony fission. Offprint requests to: J. Heinze at his new address     

Using home range estimates to construct social networks for species with indirect behavioral interactions

Social network analysis has become a vital tool for studying patterns of individual interactions that influence a variety of processes in behavior, ecology, and evolution. Taxa in which interactions are indirect or whose social behaviors are difficult to observe directly are being excluded from this rapidly expanding field. Here, we introduce a method that uses a probabilistic and spatially implicit technique for delineating social interactions. Kernel density estimators (KDE) are nonparametric techniques that are often used in home range analyses and allow researchers studying social networks to generate interaction matrices based on shared space use. We explored the use of KDE analysis and the effects of altering KDE input parameters on social network metrics using data from a natural population of the spatially persistent forked fungus beetle, Bolitotherus cornutus.     

Activity of root voles (Microtus oeconomus) under snow: social encounters synchronize individual activity rhythms

Microtine rodents usually display short-term activity rhythms synchronized by light. Social interactions have also been suggested to act as a zeitgeber, entraining individual activity, but evidence supporting this is scarce. In areas with a permanent snow cover during winter, small rodents spend most of the time in the subnivean space, between the snow cover and the ground, where they most likely are unaffected by otherwise dominating photoperiodic cues. The subnivean space, however, is fragmented, and this limits movement and may isolate individuals living just a few meters apart. These conditions provide excellent opportunities to test for the existence of social synchronization. During two winters, I experimentally decreased the subnivean fragmentation by placing out a network of corrugated aluminium sheets on the ground before snowfall, thus increasing the potential for movement and social interaction within the subnivean space. Other areas were left as controls. Intensive PIT-tag monitoring in the subnivean system provided individual activity data of root voles (Microtus oeconomus) without disturbing normal activity. The data revealed that microtines under snow displayed a free-running activity rhythm and that the activity was evenly distributed throughout the 24-h day, indicating a lack of photo-entrainment. Despite this lack of light, interacting individuals were synchronous, and pairwise synchrony decreased with decreasing potential for social interactions. These results suggest that social interactions indeed entrain microtine activity. Several possible adaptive advantages of the synchrony of microtine rodent activity have been proposed, and these theories are discussed in light of the result presented.     

Structure and resilience of the social network in an insect colony as a function of colony size

Social interactions are critical to the organization of worker activities in insect colonies and their consequent ecological success. The structure of this interaction network is therefore crucial to our understanding of colony organization and functioning. In this paper, I study the properties of the interaction network in the colonies of the social wasp Ropalidia marginata. I find that the network is characterized by a uniform connectivity among individuals with increasing heterogeneity as colonies become larger. Important network parameters are found to be correlated with colony size and I investigate how this is reflected in the organization of work in colonies of different sizes. Finally, I test the resilience of these interaction networks by experimental removal of individuals from the colony and discuss the structural properties of the network that are related to resilience in a social network. This contribution is part of the special issue “Social Networks: new perspectives” (Guest Editors: J. Krause, D. Lusseau, and R. James).     

Macro-habitat patch structure,environmental harshness,and Marmota flaviventris

Summary Social behavior of 15 colonies of Yellow-bellied Marmots was studied at sites differing in both elevation (plant growing season length) and patch structure (density and spacing of suitable colony sites in large blocks of habitat) from 1976 through 1978. Colonies were typically composed of family groups. In low elevation colonies, offspring dispersed at the end of the juvenile year. In all high elevation areas, offspring dispersed as yearlings, and parent-offspring and sibling interactions during the juvenile year were highly amicable. In high elevation areas in continuous habitat, dispersal by yearlings occurred with no agonistic interactions. In high elevation areas with patchy habitat, however, brief but intense periods of extremely agonistic sibling and parent-offspring interactions occurred immediately prior to dispersal of yearlings.Social behavior and dispersal are uncorrelated with elevation, plant growing season length, or available foraging time. Social interaction among relatives in marmot colonies is amicable when other suitable colony sites are located nearby; in these areas, dispersal occurs without any antagonism. Agonistic behavior occurs only in areas with a patchy distribution of suitable colony sites. At these sites, dispersal occurs only after periods of extreme antagonism. Further, those offspring who do not disperse from the colony site are the ones who dominate and initiate agonistic interactions with their siblings. The large-scale structure of the habitat influences the propensity of the individual to disperse. When the animal is reluctant to disperse because of a combination of high transit difficulty and low desirability of a new site, angonistic social interactions with relatives force dispersal.     

Individual dispersal status influences space use of conspecific residents in the common lizard, Lacerta vivipara

The effects of immigration on the behaviour of residents may have important implications for the local population characteristics. A manipulative laboratory experiment with yearlings of the common lizard (Lacerta vivipara) was performed to test whether the introduction of dispersing or philopatric individuals influences the short-term spacing behaviour of resident individuals. Staged encounters were carried out to induce interactions within dyads. The home cage of each responding individual was connected by a corridor to an unfamiliar “arrival cage” to measure the latency to leave their own home cage after each encounter. Our results showed that the time that pairs spent in close proximity was longer when a dispersing individual was introduced in the home cage. The latency to leave the home cage was longer after the introduction of a dispersing individual. These response variables were not influenced by the relative body sizes of contestants nor by the level of aggression towards each other. In contrast, the aggressive response was significantly influenced by the residency asymmetry established experimentally (“owner” of the home cage vs introduced individual). Our results suggest that the space use by resident individuals is influenced by the dispersal status of conspecifics. The potential ultimate causes driving this effect are discussed.     

The effects of exposure to zinc and cadmium separately and jointly on the free amino acid pool of Gammarus pulex (L.)

Effects of the heavy metals zinc and cadmium on the free amino acid (FAA) pool of Gammarus pulex were studied at different metal concentrations and combinations as well as different exposure times. The dominant effect of these two metals was the reduction of most free amino acids and the whole FAA pool, except in the 10‐day low zinc and cadmium concentration exposures which resulted in a rise of free amino acid pool.

Among the free amino acids, the most sensitive to zinc exposure, were alanine, glutamic acid, arginine, and taurine; valine, leucine, asparagine, and isoleucine were among the most sensitive to cadmium. No predictable changes of individual free amino acids were shown in the mixed metals exposures. Elevation of taurine concentration was constant in seven of the eight treatments, it is suggested that this elevation may be related to the hepatopancreatic damage observed and induced synthesis of metallothioneins.     

Egg composition in relation to social environment and maternal physiological condition in the collared flycatcher

Offspring survival can be influenced by resources allocated to eggs, which in turn may be affected by the environmental factors the mother experiences during egg formation. In this study, we investigated whether experimentally elevated social interactions and number of neighbouring pairs influence yolk composition of collared flycatchers (Ficedula albicollis). Social challenge was simulated by presentation of a conspecific female. Experimental females spent more time near the cage and produced eggs with higher androgen concentration, but local breeding density did not affect yolk androgen level. Moreover, we found that females exposed to more intra-specific interactions and those that bred at higher density produced eggs with smaller yolk. These females may be more constrained in foraging time due to more frequent social encounters, and there might be increased competition for food at areas of higher density. In contrast, the present study did not reveal any evidence for the effect of social environment on yolk antioxidant and immunoglobulin levels. However, we found that yolk lutein and immunoglobulin concentrations were related to the female’s H/L ratio. Also, yolk lutein and α-tocopherol levels showed a seasonal increase and were positively related to the female’s plasma carotenoid level. Mothers may incur significant costs by transferring these compounds into the eggs, thus only females in good physiological condition and those that lay eggs later, when food is probably more abundant, could allocate higher amounts to the eggs without compromising their defence mechanisms. Our results suggest that environmental circumstances during egg formation can influence conditions for embryonic development.     

Mate competition in the velvet swimming crab Necora puber: effects of perceived resource value on male agonistic behaviour

Male velvet swimming crabs [Necora puber (L.)] were observed to engage in long and vigorous agonistic interactions to gain possession of a sexually receptive female. The role of agonistic behaviour in male mate competition in this species was examined by investigating the effect of the perceived presence of sexually receptive females on interactions between males. Exposing male crabs to water conditioned by sexually receptive females resulted in prolonged interactions, with a greater incidence of potentially injurious behaviour than interactions between control crabs, exposed only to sea water. Maleconditioned water also resulted in more offensive behaviour, but these interactions were of shorter duration and not significantly different from sea water controls. Agonistic superiority was strongly correlated with contestant relative size when males were exposed to male-conditioned water or sea water, but not when exposed to female-conditioned water. Overall, the results conformed with the general predictions of game theoretic models in relation to the influence of resource value on agonistic behaviour. Crabs were more persistent and probably incurred greater fitness costs in the perceived presence of a sexually receptive female, when interactions may have been resolved on the basis of factors more closely related to actual fighting ability than the relative body sizes of contestants.