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42 delBarco-Trillo, J., Greene, L., Goncalves, I., Fenkes, M., Wisse, J.H., Drewe, J.A., Manser, M.B, Clutton-Brock, T. and Drea, C.M. (2016) Beyond aggression: Androgen-receptor blockade modulates social interaction in wild meerkats.... more
42  delBarco-Trillo, J., Greene, L., Goncalves, I., Fenkes, M., Wisse, J.H., Drewe, J.A., Manser, M.B, Clutton-Brock, T. and Drea, C.M. (2016) Beyond aggression: Androgen-receptor blockade modulates social interaction in wild meerkats. Hormones and Behavior. 78: 95-106

In male vertebrates, androgens are inextricably linked to reproduction, social dominance, and aggression, often at the cost of paternal investment or prosociality. Testosterone is invoked to explain rank-related reproductive differences, but its role within a status class, particularly among subordinates, is underappreciated. Recent evidence, especially for monogamous and cooperatively breeding species, suggests broader androgenic mediation of adult social interaction. We explored the actions of androgens in subordinate, male members of a cooperatively breeding species, the meerkat (Suricata suricatta). Although male meerkats show no rank-related testosterone differences, subordinate helpers rarely reproduce. We blocked androgen receptors, in the field, by treating subordinate males with the antiandrogen, flutamide. We monitored androgen concentrations (via baseline serum and time-sequential fecal sampling) and recorded behavior within their groups (via focal observation). Relative to controls, flutamide-treated animals initiated less and received more high-intensity aggression (biting, threatening, feeding competition), engaged in more prosocial behavior (social sniffing, grooming, huddling), and less frequently initiated play or assumed a ‘dominant’ role during play, revealing significant androgenic effects across a broad range of social behavior. By contrast, guarding or vigilance and measures of olfactory and vocal communication in subordinate males appeared unaffected by flutamide treatment. Thus, androgens in male meerkat helpers are aligned with the traditional trade-off between promoting reproductive and aggressive behavior at a cost to affiliation. Our findings, based on rare endocrine manipulation in wild mammals, show a more pervasive role for androgens in adult social behavior than is often recognized, with possible relevance for understanding tradeoffs in cooperative systems.
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Language's intentional nature has been highlighted as a crucial feature distinguishing it from other communication systems. Specifically, language is often thought to depend on highly structured intentional action and mutual mindreading... more
Language's intentional nature has been highlighted as a crucial feature distinguishing it from other communication systems. Specifically, language is often thought to depend on highly structured intentional action and mutual mindreading by a communicator and recipient. Whilst similar abilities in animals can shed light on the evolution of intentionality, they remain challenging to detect unambiguously. We revisit animal intentional communication and suggest that progress in identifying analogous capacities has been complicated by (i) the assumption that intentional (that is, voluntary) production of communicative acts requires mental-state attribution, and (ii) variation in approaches investigating communication across sensory modalities. To move forward, we argue that a framework fusing research across modalities and species is required. We structure intentional communication into a series of requirements, each of which can be operationalised, investigated empirically, and must be met for purposive, intentionally communicative acts to be demonstrated. Our unified approach helps elucidate the distribution of animal intentional communication and subsequently serves to clarify what is meant by attributions of intentional communication in animals and humans.
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In male vertebrates, androgens are inextricably linked to reproduction, social dominance, and aggression, often at the cost of paternal investment or prosociality. Testosterone is invoked to explain rank-related reproductive differences,... more
In male vertebrates, androgens are inextricably linked to reproduction, social dominance, and aggression, often at the cost of paternal investment or prosociality. Testosterone is invoked to explain rank-related reproductive differences, but its role within a status class, particularly among subordinates, is underappreciated. Recent evidence, especially for monogamous and cooperatively breeding species, suggests broader androgenic mediation of adult social interaction. We explored the actions of androgens in subordinate, male members of a cooperatively breeding species, the meerkat (Suricata suricatta). Although male meerkats show no rank-related testosterone differences, subordinate helpers rarely reproduce. We blocked androgen receptors, in the field, by treating subordinate males with the antiandrogen, flutamide. We monitored androgen concentrations (via baseline serum and time-sequential fecal sampling) and recorded behavior within their groups (via focal observation). Relative to controls, flutamide-treated animals initiated less and received more high-intensity aggression (biting, threatening, feeding competition), engaged in more prosocial behavior (social sniffing, grooming, huddling), and less frequently initiated play or assumed a 'dominant' role during play, revealing significant androgenic effects across a broad range of social behavior. By contrast, guarding or vigilance and measures of olfactory and vocal communication in subordinate males appeared unaffected by flutamide treatment. Thus, androgens in male meerkat helpers are aligned with the traditional trade-off between promoting reproductive and aggressive behavior at a cost to affiliation. Our findings, based on rare endocrine manipulation in wild mammals, show a more pervasive role for androgens in adult social behavior than is often recognized, with possible relevance for understanding tradeoffs in cooperative systems.
Offspring fitness generally improves with increasing egg size. Yet, eggs of most aquatic organisms are small. A common but largely untested assumption is that larger embryos require more oxygen than they can acquire through diffusion via... more
Offspring fitness generally improves with increasing egg size. Yet, eggs of most aquatic organisms are small. A common but largely untested assumption is that larger embryos require more oxygen than they can acquire through diffusion via the egg surface, constraining egg size evolution. However, we found no detrimental effects of large egg size on embryo growth and survival under hypoxic conditions. We tested this in the broad-nosed pipefish, Syngnathus typhle, whose males provide extensive care (nourishment, osmoregulation and oxygenation) to their young in a brood pouch on their bodies. We took advantage of this species' pronounced variation in egg size, correlating positively with female size, and tested the effect of hypoxia (40% dissolved oxygen) versus fully oxygenated (100%) water on embryo size and survival of large versus small eggs after 18 days of paternal brooding. Egg size did not affect embryo survival, regardless of O2 treatment. While hypoxia affected embryo size negatively, both large and small eggs showed similar reductions in growth. Males in hypoxia ventilated more and males with large eggs swam more, but neither treatment affected their position in the water column. Overall, our results call into question the most common explanation for constrained egg size evolution in aquatic environments.
Comparing five species of pipefish, egg size was significantly larger in species with brood pouches (Syngnathus typhle, Syngnathus acus and Syngnathus rostellatus) than in species without brood pouches (Entelurus aequoreus and Nerophis... more
Comparing five species of pipefish, egg size was significantly larger in species with brood pouches (Syngnathus typhle, Syngnathus acus and Syngnathus rostellatus) than in species without brood pouches (Entelurus aequoreus and Nerophis ophidion). Egg size correlated positively with female body size in species with brood pouches, but was similar across female sizes in the species lacking pouches. These results may reflect differences in offspring competition as a consequence of variable offspring relatedness within a brood, due to the mating systems adopted by the different species and the presence or absence of a brood pouch.
The pipefish brood pouch presents a unique mode of parental care that enables males to protect, osmoregulate, nourish and oxygenate the developing young. Using a very fine O2 probe, we assessed the extent to which males of the broad-nosed... more
The pipefish brood pouch presents a unique mode of parental care that enables males to protect, osmoregulate, nourish and oxygenate the developing young. Using a very fine O2 probe, we assessed the extent to which males of the broad-nosed pipefish (Syngnathus typhle) oxygenate the developing embryos and are able to maintain pouch fluid O2 levels when brooding in normoxia (100% O2 saturation) and hypoxia (40% O2 saturation) for 24 days. In both treatments, pouch fluid O2 saturation levels were lower compared with the surrounding water and decreased throughout the brooding period, reflecting greater offspring demand for O2 during development and/or decreasing paternal ability to provide O2 to the embryos. Male condition (hepatosomatic index) was negatively affected by hypoxia. Larger males had higher pouch fluid O2 saturation levels compared with smaller males, and levels were higher in the bottom section of the pouch compared with other sections. Embryo size was positively correlated with O2 availability, irrespective of their position in the pouch. Two important conclusions can be drawn from our findings. First, our results highlight a potential limitation to brooding within the pouch and dismiss the notion of closed brood pouches as well-oxygenated structures promoting the evolution of larger eggs in syngnathids. Second, we provide direct evidence that paternal care improves with male size in this species. This finding offers an explanation for the documented strong female preference for larger partners because, in terms of oxygenation, the brood pouch can restrict embryo growth.
Adrenal hormones likely affect anti-predator behavior in animals. With experimental field studies, we first investigated associations between mean fecal glucocorticoid metabolite (fGC) excretion and vigilance and with behavioral responses... more
Adrenal hormones likely affect anti-predator behavior in animals. With experimental field studies, we first investigated associations between mean fecal glucocorticoid metabolite (fGC) excretion and vigilance and with behavioral responses to alarm call playbacks in free-ranging meerkats (Suricata suricatta). We then tested how vigilance and behavioral responses to alarm call playbacks were affected in individuals administered exogenous cortisol. We found a positive association between mean fGC concentrations and vigilance behavior, but no relationship with the intensity of behavioral responses to alarm calls. However, in response to alarm call playbacks, individuals administered cortisol took slightly longer to resume foraging than control individuals treated with saline solution. Vigilance behavior, which occurs in the presence and absence of dangerous stimuli, serves to detect and avoid potential dangers, whereas responses to alarm calls serve to avoid immediate predation. Our data show that mean fGC excretion in meerkats was associated with vigilance, as a re-occurring anti-predator behavior over long time periods, and experimentally induced elevations of plasma cortisol affected the response to immediate threats. Together, our results indicate an association between the two types of anti-predator behavior and glucocorticoids, but that the underlying mechanisms may differ. Our study emphasizes the need to consider appropriate measures of adrenal activity specific to different contexts when assessing links between stress physiology and different anti-predator behaviors.
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