Many animal species respond less aggressively to calls emitted by neighbors in comparison with strangers, an asymmetry known as the “dear enemy” effect. The adaptive significance of having “dear enemies” would be to minimize defensive costs towards less-threatening individuals (like neighbors). The opposite situation, in which known neighbors become untrustworthy, representing an even greater menace than strangers, is call “nasty neighbor effect”. In addition to these neighbor-stranger discrimination abilities, some species are also capable of recognizing neighbors individually, allowing them to avoid risky encounters based on identity and past experiences, minimizing the probability of losing an encounter. In this study we tested if black-and-gold howler monkey (Alouatta caraya) males can recognize neighbors individually and investigated the nature of long-term relationships under the dear enemy/nasty neighbors hypotheses. We conducted 36 playback experiments on four dominant males in “El Cachapé” reserve, in Argentina. We exposed each male to three different treatments, consisting of roars from: 1- Neighbors from the area of home range overlap, 2- Misplaced neighbors from the opposite side to the area of home range overlap, and 3- Strangers, quantifying eight response variables during each experiment. Our results showed that dominant males recognize neighbors individually (by roaring longer in response to misplaced neighbors), clearly reacting more aggressively to neighbors who violate mutual agreements (like home range boundaries). Also, dominant males displayed a longer roar duration and closer approach to the sound source when hearing roars from strangers, supporting the hypothesis that neighbors are dear enemies in this species. Our results show that neighbor vocal recognition is key to understanding the configuration of areas of collective use and navigation decision in primates and that strangers exert the major threat to group stability in howler monkeys.
Phenotypic variation may influence social structure if animals associate nonrandomly based on phenotypic traits. For animals that rely on cognition for survival, variation in cognitive ability may also affect social structure. Individuals with worse cognitive abilities could benefit from preferentially associating with conspecifics with better cognition, from being more gregarious, or both, allowing them access to resources. Climatic conditions influence resource availability, which may also affect the relative benefits of assortment or gregariousness, resulting in spatiotemporal variation of social patterns. Using 5 years of data, we investigated assortment by spatial cognitive ability and associations between sociality and spatial cognition in food-caching mountain chickadees, Poecile gambeli, inhabiting harsher environments at higher elevations and milder environments at lower elevations. Elevation environments differ in overwinter severity and in the harshest winter, high elevation chickadees with better spatial learning and memory abilities were less gregarious and showed lower social differentiation (or choosiness) than those with worse spatial learning and memory abilities but did not assort based on these traits. In two other seasons, including the second harshest winter, high elevation chickadees that were less cognitively flexible showed more social differentiation than those that were more cognitively flexible. In these two seasons alone, chickadees negatively assorted by spatial learning and memory performance. Chickadees from low elevations only demonstrated negative assortment in the second harshest winter. All other results were nonsignificant, suggesting that overall, individual spatial cognitive abilities or those of their associates have little influence on social preferences.
We showed that under certain environmental conditions, social behavior may be related to spatial cognitive abilities in mountain chickadees that rely heavily on spatial cognition for overwinter survival, but that overall, cognition does not appear to influence social behavior. In the few years that patterns were present, they fit three trends: 1) chickadees with worse spatial cognitive abilities were more gregarious; 2) chickadees with worse spatial cognitive abilities were choosier; and/or 3) chickadees had stronger associations with social partners that had spatial cognitive abilities that differed from their own and weaker associations with those of similar cognitive abilities. While it is unclear under which specific circumstances these patterns emerge, they coincided with extreme snowfall, suggesting that individuals with worse spatial cognition alter their social behavior to buffer against their relatively greater risk of starvation under extenuating circumstances.
The neighbor-stranger response difference, which serves as a fundamental social network relationship, plays a crucial role in establishing and expanding complex social networks. However, the underlying causes of this phenomenon have received limited attention in controlled indoor settings. This study focused on Portunus trituberculatus, a representative crustacean species in the Western Pacific Ocean. We analyzed the behavioral responses of crabs towards intruders of varying familiarity and threat levels. Additionally, we quantified various parameters such as territory size, behavior quantification, time allocation, and territorial behavior score. The results showed that with increased familiarity, there was a decrease in the frequency of occupiers’ aggressive dash and aggressive wave. As the threat from the intruder decreased, occupiers displayed fewer territorial behaviors and engaged in fewer bouts, while the success rate in fights improved and the territorial behavior score declined. The results indicate a clear dear-enemy effect in the territorial defense of P. trituberculatus, and demonstrates that crabs adjusted the defense strategy according to the relative threat level of intruders. We verified the formation hypothesis of dear-enemy effect in crabs. In the future, we will expand the research from individuals to populations, analyze crustacean social networks from the perspective of group decision making, and provide more support for population dynamic analysis and decision evolution research of crustaceans.
Anuran communication is largely based on acoustic signals, but different sensory modes are also widespread, including visual communication using body color traits as a way of signaling. The Brazilian treefrog, Boana albomarginata, has a complex behavioral repertoire presenting several call types and performing gestures as visual signals. This species has a greenish body color with orange patches on the flanks and thighs. These patches become visible when males are in a calling posture or performing visual signals such as leg kicking and limb lifting, suggesting that they might use the patches as visual cues. We sampled seven populations, using call recordings and photographs to access males call and color traits. We demonstrate that there is variation in color and call properties across populations. Additionally, we observe variation in the relationship between color traits and call properties in different populations, revealing that only two populations exhibit a significant correlation between color and call traits. Further, while call properties and color traits were not related with individual body size, they were associated with body condition. The results indicate a universal pattern across populations for call properties, wherein males in better condition consistently displayed lower-pitched calls, longer calls, and shorter intervals between calls. Regarding color traits, males in better condition in four out of the seven evaluated populations exhibited larger orange patch sizes, lower orange hue values, and higher hue contrasts. Although we observed some level of relation among color, call, and body traits, there is not a universal pattern across all populations.
Animal social interactions are mediated by signals transmitted through different sensory modes (i.e., acoustic, chemical, tactile, and visual), and more than one of these modalities can compose the behavioral repertoire of one species. Using photographs and acoustic recordings of Boana albomarginata males in natural environments, we documented geographic variation in both signals, call and color, and investigated their potential to convey individual body size and condition. Our findings reveal that both signals were correlated with individual body condition. In addition, color traits were associated with call properties in some populations.
Across the animal kingdom, males advertise their quality to potential mates. Males of low reproductive quality, such as those that are sick, may be excluded from mating. In eusocial species, there is some evidence that reproductive females gauge the quality of their mates. However, males often spend much more time with non-reproductive females when being raised or when returning from unsuccessful mating flights. Do non-reproductive workers evaluate the quality of male reproductives? Here we address this question using male honey bees (Apis mellifera), called drones, as a model. We generated immune-challenged drones by injecting them with lipopolysaccharide and tested: 1) do workers evict immune-challenged drones from their colony, 2) do cuticular hydrocarbon (CHC) profiles, body size, or mass change when drones are immune-challenged, and 3) are these changes used by workers to exclude low quality males from the colony? We found that an immune challenge causes changes in CHC profiles of drones and reduces their body mass. Workers selectively evict small and immune-challenged drones who, themselves, do not self-evict. This work demonstrates that some eusocial males undergo an additional layer of scrutiny prior to mating mediated by the non-reproductive worker caste.
Males of some species must advertise their quality to mates but, in the case of eusocial species, must they also advertise their quality to nestmates? By manipulating honey bee male quality, we found that small and immune-challenged drones are evicted from colonies overnight. Workers may not use a drone’s cuticular hydrocarbon profile to make this assessment. This is a new example of social immunity expressed against adult males and an example of worker involvement in reproductive decisions.
The shy-bold behavioral continuum is an element of animal behavior which is often studied for its ecological relevance, particularly in the context of predation risk. How individuals respond to various predation cues is well studied at the individual level, but relatively little is known about how these responses can differ among closely related species. We exposed individual wild-caught juvenile bluegill (Lepomis macrochirus) and pumpkinseed (L. gibbosus) to kairomones of a common predator (Northern pike, Esox lucius), conspecific alarm cues, or a lake water control in a Z-maze trial commonly used to assess relative levels of bold and exploratory behaviors. Neither species exhibited any significant behavioral responses to either predation cue, but bluegill consistently displayed more bold-type behaviors than pumpkinseed. Although the lack of a behavioral response to predation cues in this study is equivocal, we identify clear differences in boldness between these two congeners and discuss the possibility of ecological niche differentiation driving these behavioral differences.
Fission–fusion dynamics describe the tendency for members of some animal societies to associate in subgroups that change size and structure fluidly over time. These dynamics shape social complexity and social structure, but are difficult to study because they unfold simultaneously over large spatial scales. Here we use simultaneous, fine-scale GPS data from spotted hyenas to examine fission–fusion dynamics through a dyadic analysis of merge-split events between pairs of individuals. We introduce a species-agnostic framework for identifying merge-split events and discretizing them into three phases (merging, together, and splitting), enabling analysis of each phase as well as the connections among phases. Applying this framework to the hyena data, we examine the temporal and spatial properties of merges and splits between dyads and test the extent to which social encounters are driven by key locations. Specifically, we focus on communal dens—shelters for juvenile hyenas where classical observational studies often report large aggregations of adults. We find that overall, 62% of merges occurred at communal dens, supporting the idea that dens facilitate meet-ups and subsequent social behavior. Social encounters most commonly involved close approaches within a few meters between hyenas, while co-travel together occurred in only 11% of events. Comparison to permutation-based reference models suggests that independent movement decisions structure broad-scale patterns of social encounters but do not explain the fine-scale dynamics of interactions that unfold during these encounters. We reflect on how physical features such as dens can become social hotspots, causing social and spatial processes to become fundamentally intertwined.
Geographical variation in animals’ acoustic signals has received much attention. However, few studies have compared the patterns and underlying selective forces driving geographical divergence of vocalizations with similar and different functions within the same species. Also, the social consequences of geographical divergence in acoustic signals are still rather poorly understood. Here we recorded three types of social calls of male great Himalayan leaf-nosed bats (Hipposideros armiger) across eight colonies in China. Two calls share similar functions and the third has a function distinct from the other two. We examined the patterns and causes of geographical variation of each of these calls. We found that all three calls had significant geographic variation with similar patterns of spatial variation. Only one of the two social calls with similar functions was found to be affected by genetic drift, while the other two calls were not affected by selection, drift, or morphological constraints. Furthermore, we found that bats could discriminate between vocalizations of their own colony and those of an allopatric colony. Overall, these results suggest that acoustic signals with similar functions may be shaped by different driving forces and acoustic signals with different functions may exhibit similar geographical patterns. This study expands our limited knowledge of the patterns of geographical variation of vocalizations emitted at different emotional states and highlights the importance of comparing simultaneously patterns and causes of geographical divergence of vocalizations with similar and different functions.
We used video playback of courting male Schizocosa ocreata wolf spiders to examine responses of intended receivers (conspecific females) and eavesdroppers (competitor males, predatory spiders, toads) to manipulations of spider color (natural color, monochromatic gray, monochromatic RBG average) displayed against complex leaf litter backgrounds (color, grayscale). Models of chromatic and achromatic contrast between spider stimuli and backgrounds were used to predict receiver responses. The results support the hypothesis that interactions between spider and background coloration affect detection and recognition, although responses varied with receiver type. Detection responses of intended receivers (female S. ocreata) did not fit predictions of the chromatic contrast model in some cases, but showed a fair fit to the achromatic model. Detection responses of social eavesdroppers (male S. ocreata) fit the chromatic and achromatic contrast models slightly better than did female responses (poor fit and very good fit, respectively). Eavesdropping wolf spider predators (Rabidosa) exhibited detection responses that significantly matched predictions of the chromatic (very good fit) and achromatic (excellent fit) models. Whereas jumping spiders (Phidippus) showed a good fit to the chromatic and achromatic contrast models, toad predators had a good fit only to the chromatic model. Recognition responses revealed a different pattern of fit to the chromatic and achromatic models across receiver types, although Rabidosa again indicated a significant fit to both models. Taken together, the results of this study identify both chromatic and achromatic features of spider appearance as likely explanations for differences in behavioral responses of intended and unintended receivers. This outcome suggests the possibility that both sexual and natural selection likely target different features of male appearance during courtship.
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