All clear? Meerkats attend to contextual information in close calls to coordinate vigilance

Socio-demographic factors, such as group size and their effect on predation vulnerability, have, in addition to intrinsic factors, dominated as explanations when attempting to understand animal vigilance behaviour. It is generally assumed that animals evaluate these external factors visually; however, many socially foraging species adopt a foraging technique that directly compromises the visual system. In these instances, such species may instead rely more on the acoustical medium to assess their relative risk and guide their subsequent anti-predator behaviour. We addressed this question in the socially foraging meerkat (Suricata suricatta). Meerkats forage with their head down, but at the same time frequently produce close calls (‘Foraging' close calls). Close calls are also produced just after an individual has briefly scanned the surrounding environment for predators (‘Guarding' close calls). Here, we firstly show that these Guarding and Foraging close call variants are in fact acoustically distinct and secondly subjects are less vigilant (in terms of frequency and time) when exposed to Guarding close call playbacks than when they hear Foraging close calls. We argue that this is the first evidence for socially foraging animals using the information encoded within calls, the main adaptive function of which is unrelated to immediate predator encounters, to coordinate their vigilance behaviour. In addition, these results provide new insights into the potential cognitive mechanisms underlying anti-predator behaviour and suggest meerkats may be capable of signalling to group members the ‘absence' of predatory threat. If we are to fully understand the complexities underlying the coordination of animal anti-predator behaviour, we encourage future studies to take these additional auditory and cognitive dimensions into accoun

Coercion promotes alloparental care in cooperative breeders.

Members of social groups may negotiate among each other about the exchange of goods and services. If this involves asymmetries between interacting partners, for instance in condition, power, or expected payoffs, coercion may be involved in the bargain. Cooperative breeders are excellent models to study such interactions, because asymmetries are inherent in the relationship between dominant breeders and subordinate helpers. Currently it is unclear whether punishment is used to enforce costly cooperation in such systems. Here we investigated experimentally in the cooperatively breeding cichlid Neolamprologus pulcher whether alloparental brood care provided by subordinates is contingent on enforcement by dominant breeders. We manipulated first the brood care behavior of a subordinate group member and then the possibility of the dominant breeders to punish idle helpers. When subordinates were prevented from providing brood care, breeders increased their attacks on them, which triggered increased alloparental brood care by helpers as soon as this was again possible. In contrast, when the possibility to punish helpers was prevented, energetically costly alloparental brood care did not increase. Our results confirm predictions of the pay-to-stay mechanism causing alloparental care in this species and they suggest more generally that coercion can play an important role in the control of cooperation

Benefits of secondary predator cue inspection and recruitment in a cooperative mammal (Suricata Suricatta)

Raubdruck und die Gefahr gefressen zu werden ist ein entscheidender Faktor im Leben beinahe jeden Tieres. Aus diesem Grund ist es nicht weiter verwunderlich, dass potentielle Beutetiere zahlreiche Anpassungen zur Vermeidung dieser Gefahr zeigen. Indirekte Hinweise auf die Anwesenheit von Raubfeinden als Indikator für die unmittelbare Bedrohung an einem bestimmten Ort und zu einer bestimmten Zeit zu beachten ist eine Möglichkeit zur Verringerung des Risikos. Bei vielen Säugetierarten konnte gezeigt werden, dass Individuen auf den Geruch von Prädatoren reagieren. Indirekte Hinweise können aber auch visuell oder akustisch wahrgenommen werden. Häufig erhöhen Tiere ihre Wachsamkeit, suchen vermehrt Schutz auf oder beenden die Futtersuche in betroffenen Gebieten. Folglich nehmen sie weniger Nahrung auf. Man kann aber davon ausgehen, dass Tiere durch diese Anpassungen die Gefahr verringern, selbst zur Beute zu werden. Bei kooperativ organisierten Tierarten kann ein Individuum, welches Hinweise auf Beutegreifer erkennt, nicht nur selbst schneller reagieren, sondern auch zusätzlich profitieren, wenn es seine Gruppenmitglieder über die Gefahr informiert. Wenn jedes Individuum der gewarnten Gruppe Verhaltensweisen zur Feindvermeidung verstärkt, nützen diese Maßnahmen allen Mitgliedern. Verglichen mit einer Situation ohne Informationstransfer, ermöglicht die geteilte Wachsamkeit unter Umständen dem Individuum, welches den indirekten Hinweis findet, mehr Zeit für andere Aktivitäten, wie beispielsweise Nahrungssuche, verwenden zu können. Erdmännchen (Suricata suricatta) sind eine hochsoziale Mangustenart, die im südlichen Afrika vorkommt. In der spärlichen Vegetation der Halbwüste finden sie wenig Deckung und sind einem hohen Raubdruck ausgesetzt. Sie haben ein sehr effizientes Wachsystem entwickelt und reagieren stark auf jeden Stimulus, der auf Raubfeinde hinweist. Ein Erdmännchen, das einen solchen Hinweis wahrnimmt, ruft mittels spezieller Rekrutierlaute seine gesamte Gruppe zusammen. Alle Mitglieder unterbrechen die Nahrungssuche und inspizieren den Stimulus. Wenn kein Räuber entdeckt wird dauert die Inspektion einige Minuten. Anschließend beginnen die Erdmännchen wieder mit der Nahrungssuche. Durch diese Informationsmöglichkeit kann sich jedes Gruppenmitglied auf die mögliche Gefahr einstellen und seine Wachsamkeit erhöhen, was wiederum der gesamten Gruppe zugute kommt.   In dieser Arbeit wurde ein experimenteller Ansatz gewählt um bei frei lebenden, an Menschen habituierten Erdmännchen, drei Hypothesen zu testen: 1) Erdmännchen entdecken einen Raubfeind früher, nachdem sie mit einem indirekten Hinweis auf den Räuber, wie z.B. dem Geruch konfrontiert worden sind. 2) Wenn kein Räuber entdeckt wird, aber alle Tiere in der Gruppe zu dem indirekten Hinweis rekrutiert werden, verbringt jedes Individuum während der folgenden Nahrungssuche mehr Zeit mit Verhaltensweisen zur Feindvermeidung. 3) Wird durch experimentelle Manipulation die Kommunikationsmöglichkeit unterbunden, so bleibt jenes Individuum, das den indirekten Hinweis findet, das Einzige in der Gruppe, das über die erhöhte Gefahr Bescheid weiß. Folglich muss dieses Individuum seine Futtersuche im Vergleich zur Normalsituation, in der es seine Gruppenmitglieder rekrutiert verringern. Um diese drei Hypothesen zu testen wurden zwei unterschiedliche Experimente durchgeführt. In beiden Experimenten kamen indirekte Hinweise auf Raubfeinde wie Katzenurin, Katzenhaar (Felis Catus) Löffelohrenhundfell (Otocyon megalotis), oder Wüstenluchsfell (Caracal caracal) zur Anwendung. Im ersten Versuch wurde die Zeit gestoppt, welche die Erdmännchen benötigten, mit und ohne indirekten Hinweis einen Raubfeind zu entdecken. Im Zweiten hingegen wurde ein Hinweis ohne Anwesenheit eines Raubfeindes präsentiert und zu Vergleichszwecken das Rekrutieren möglich oder unmöglich gemacht. Die Ergebnisse zeigten, dass Erdmännchen tatsächlich früher auf eine Räuberattrappe in Form eines ausgestopften und präparierten Karakals reagierten, wenn sie vorher einen indirekten Hinweis in Form von Geruchsspuren fanden. Damit konnte erstmals experimentell nachgewiesen werden, dass Tiere die Möglichkeit haben Räuber früher zu entdecken, wenn sie auf indirekte Hinweise wie Geruchsspuren treffen. Dies legt nahe, dass die Reaktion auf potentielle Gefahr in Form eines Hinweises auf die Präsenz eines Räubers die Überlebenswahrscheinlichkeit für Beutetiere erhöht. Wenn allerdings, wie im zweiten Experiment, kein Räuber zu sehen war begannen die Erdmännchen wieder mit der Nahrungssuche. So reduzierten alle Tiere die für Nahrungssuche aufgewendete Zeit zugunsten von Verhaltensweisen zur Räubervermeidung. Dieser Effekt ist ähnlich stark ausgeprägt in Tieren, die rekrutiert wurden und in Tieren die rekrutierten. Wurde hingegen der Rekrutierruf des mit dem Räuberstimulus konfrontierten Individuums durch gleichzeitiges Abspielen eines Playbacks mit weißem Rauschen im gleichen Frequenzbereich gestört, zeigte die Gruppe keine Reaktion auf den Rufer. Die Gruppe konnte dann den Räubergeruch auch nicht wahrnehmen. Wurde nun die Zeit, die das rekrutierende Tier nach einer erfolgreichen und nach einer durch Manipulation erfolglosen Rekrutierung in Feindvermeidung investierte verglichen, zeigte sich kein signifikanter Unterschied. Allerdings hielt sich das Tier bei der verhinderten Rekrutierung häufiger an geschützten Plätzen auf, als wenn es die Gruppe informieren konnte. Diese Ergebnisse deuten darauf hin, dass Erdmännchen als Reaktion auf die experimentell unterbundene Kommunikation möglicherweise Einbußen in der Effizienz der Futtersuche erleiden, da sie sich vermehrt in Deckung aufhalten. Daraus lässt sich schließen, dass der Hauptvorteil für das Erdmännchen, welches den Hinweis findet, darin besteht, dass ein Räuber entweder während der Inspektion des Hinweises durch die gesamte Gruppe oder während der anschließenden Futtersuche früher entdeckt wird. Diese frühe Entdeckung erhöht die Überlebenswahrscheinlichkeit für alle Gruppenmitglieder, was wiederum Vorteile mit sich bringt, wenn es darum geht das Revier zu verteidigen oder andere Raubfeinde zu entdecken („viele Augen sehen mehr als wenige“). Daher ist die Reaktion auf indirekte Raubfeindhinweise wie Geruchsspuren vorteilhaft, auch wenn sich kurzfristig die Zeit für Nahrungssuche für alle Erdmännchen einer Gruppe verringert. Schlussendlich legen die Ergebnisse nahe, dass das rekrutierende Individuum von der frühen Entdeckung des Räubers so stark profitiert, dass sich das Rekrutieren auszahlt, obwohl sich dadurch die Dauer der Nahrungssuche für diese Tier nicht erhöht

Repeatability and Heritability of Behavioural Types in a Social Cichlid

Aim. The quantitative genetics underlying correlated behavioural traits (‘‘animal personality”) have hitherto been studied mainly in domesticated animals. Here we report the repeatability (R) and heritability (h2) of behavioural types in the highly social cichlid fish Neolamprologus pulcher. Methods. We tested 1779 individuals repeatedly and calculated the h2 of behavioural types by variance components estimation (GLMM REML), using 1327 offspring from 162 broods from 74 pairs. Results. Repeatability of behavioural types was significant and considerable (0.546), but declined from 0.83 between tests conducted on the same day, to 0.19 on tests conducted up to 1201 days apart. All h2 estimates were significant but low (e.g., pair identity h2 = 0.15 ± 0.03 SE). Additionally, we found significant variation between broods nested within the parent(s), but these were not related to several environmental factors tested. Conclusions. We conclude that despite a considerable R, h2 in this cichlid species is low, and variability in behavioural type appears to be strongly affected by other (non)genetic effects

Invasive parasites habitat change and heavy rainfall reduce breeding success in Darwin's finches

Invasive alien parasites and pathogens are a growing threat to biodiversity worldwide, which can contribute to the extinction of endemic species. On the Galápagos Islands, the invasive parasitic fly Philornis downsi poses a major threat to the endemic avifauna. Here, we investigated the influence of this parasite on the breeding success of two Darwin's finch species, the warbler finch (Certhidea olivacea) and the sympatric small tree finch (Camarhynchus parvulus), on Santa Cruz Island in 2010 and 2012. While the population of the small tree finch appeared to be stable, the warbler finch has experienced a dramatic decline in population size on Santa Cruz Island since 1997. We aimed to identify whether warbler finches are particularly vulnerable during different stages of the breeding cycle. Contrary to our prediction, breeding success was lower in the small tree finch than in the warbler finch. In both species P. downsi had a strong negative impact on breeding success and our data suggest that heavy rain events also lowered the fledging success. On the one hand parents might be less efficient in compensating their chicks' energy loss due to parasitism as they might be less efficient in foraging on days of heavy rain. On the other hand, intense rainfalls might lead to increased humidity and more rapid cooling of the nests. In the case of the warbler finch we found that the control of invasive plant species with herbicides had a significant additive negative impact on the breeding success. It is very likely that the availability of insects (i.e. food abundance) is lower in such controlled areas, as herbicide usage led to the removal of the entire understory. Predation seems to be a minor factor in brood loss

Differences in cooperative behavior among Damaraland mole rats are consequences of an age-related polyethism.

In many cooperative breeders, the contributions of helpers to cooperative activities change with age, resulting in age-related polyethisms. In contrast, some studies of social mole rats (including naked mole rats, Heterocephalus glaber, and Damaraland mole rats, Fukomys damarensis) suggest that individual differences in cooperative behavior are the result of divergent developmental pathways, leading to discrete and permanent functional categories of helpers that resemble the caste systems found in eusocial insects. Here we show that, in Damaraland mole rats, individual contributions to cooperative behavior increase with age and are higher in fast-growing individuals. Individual contributions to different cooperative tasks are intercorrelated and repeatability of cooperative behavior is similar to that found in other cooperatively breeding vertebrates. Our data provide no evidence that nonreproductive individuals show divergent developmental pathways or specialize in particular tasks. Instead of representing a caste system, variation in the behavior of nonreproductive individuals in Damaraland mole rats closely resembles that found in other cooperatively breeding mammals and appears to be a consequence of age-related polyethism.This study was funded by an European Research Council grant to THCB (294494).This is the author accepted manuscript. The final version is available from the National Academy of Sciences via http://dx.doi.org/10.1073/pnas.160788511

Allo-parental care in Damaraland mole-rats is female biased and age dependent, though independent of testosterone levels

Abstract In Damaraland mole-rats (Fukomys damarensis), non-breeding subordinates contribute to the care of offspring born to the breeding pair in their group by carrying and retrieving young to the nest. In social mole-rats and some cooperative breeders, dominant females show unusually high testosterone levels and it has been suggested that high testosterone levels may increase reproductive and aggressive behavior and reduce investment in allo-parental and parental care, generating age and state-dependent variation in behavior. Here we show that, in Damaraland mole-rats, allo-parental care in males and females is unaffected by experimental increases in testosterone levels. Pup carrying decreases with age of the non-breeding helper while the change in social status from non-breeder to breeder has contrasting effects in the two sexes. Female breeders were more likely than female non-breeders to carry pups but male breeders were less likely to carry pups than male non-breeders, increasing the sex bias in parental care compared to allo-parental care. Our results indicate that testosterone is unlikely to be an important regulator of allo-parental care in mole-rats.Peer reviewe

Group-size-dependent punishment of idle subordinates in a cooperative breeder where helpers pay to stay

In cooperative breeding systems, dominant breeders sometimes tolerate unrelated individuals even if they inflict costs on the dominants. According to the 'pay-to-stay' hypothesis, (i) subordinates can outweigh these costs by providing help and (ii) dominants should be able to enforce help by punishing subordinates that provide insufficient help. This requires that dominants can monitor helping and can recognize group members individually. In a field experiment, we tested whether cooperatively breeding cichlid Neolamprologus pulcher subordinates increase their help after a forced 'idle' period, how other group members respond to a previously idle helper, and how helper behaviour and group responses depend on group size. Previously, idle helpers increased their submissiveness and received more aggression than control helpers, suggesting that punishment occurred to enforce help. Subordinates in small groups increased their help more than those in large groups, despite receiving less aggression. When subordinates were temporarily removed, dominants in small groups were more likely to evict returning subordinates. Our results suggest that only in small groups do helpers face a latent threat of punishment by breeders as predicted by the pay-to-stay hypothesis. In large groups, cognitive constraints may prevent breeders from tracking the behaviour of a large number of helpers

Reproduction triggers adaptive increases in body size in female mole-rats

In social mole-rats, breeding females are larger and more elongated than non-breeding female helpers. This status-related morphological divergence is thought to arise from modifications of skeletal growth following the death or removal of the previous breeder and the transition of their successors from a non-breeding to a breeding role. However, it is not clear what changes in growth are involved, whether they are stimulated by the relaxation of reproductive suppression or by changes in breeding status, or whether they are associated with fecundity increases. Here, we show that, in captive Damaraland mole-rats (Fukomys damarensis), where breeding was experimentally controlled in age-matched siblings, individuals changed in size and shape through a lengthening of the lumbar vertebrae when they began breeding. This skeletal remodelling results from changes in breeding status because (i) females removed from a group setting and placed solitarily showed no increases in growth and (ii) females dispersing from natural groups that have not yet bred do not differ in size and shape from helpers in established groups. Growth patterns consequently resemble other social vertebrates where contrasts in size and shape follow the acquisition of the breeding role. Our results also suggest that the increases in female body size provide fecundity benefits. Similar forms of socially responsive growth might be more prevalent in vertebrates than is currently recognized, but the extent to which this is the case, and the implications for the structuring of mammalian dominance hierarchies, are as yet poorly understood.The Kalahari Mole-rat Project is supported by a European Research Council Grant awarded to T.C.-B. (no. 294494); J.T. was funded by a Natural Environment Research Council Doctoral Training Program; parts of the fieldwork were funded by a British Ecological Society Grant awarded to Markus Zöttl (no. 5301/6343).http://rspb.royalsocietypublishing.org2019-06-13hj2018Mammal Research InstituteZoology and Entomolog

Thiamin dynamics during the adult life cycle of Atlantic salmon (Salmo salar)

Thiamin is an essential water-soluble B vitamin known for its wide range of metabolic functions and antioxidant properties. Over the past decades, reproductive failures induced by thiamin deficiency have been observed in several salmonid species worldwide, but it is unclear why this micronutrient deficiency arises. Few studies have compared thiamin concentrations in systems of salmonid populations with or without documented thiamin deficiency. Moreover, it is not well known whether and how thiamin concentration changes during the marine feeding phase and the spawning migration. Therefore, samples of Atlantic salmon (Salmo salar) were collected when actively feeding in the open Baltic Sea, after the sea migration to natal rivers, after river migration, and during the spawning period. To compare populations of Baltic salmon with systems without documented thiamin deficiency, a population of landlocked salmon located in Lake Vänern (Sweden) was sampled as well as salmon from Norwegian rivers draining into the North Atlantic Ocean. Results showed the highest mean thiamin concentrations in Lake Vänern salmon, followed by North Atlantic, and the lowest in Baltic populations. Therefore, salmon in the Baltic Sea seem to be consistently more constrained by thiamin than those in other systems. Condition factor and body length had little to no effect on thiamin concentrations in all systems, suggesting that there is no relation between the body condition of salmon and thiamin deficiency. In our large spatiotemporal comparison of salmon populations, thiamin concentrations declined toward spawning in all studied systems, suggesting that the reduction in thiamin concentration arises as a natural consequence of starvation rather than to be related to thiamin deficiency in the system. These results suggest that factors affecting accumulation during the marine feeding phase are key for understanding the thiamin deficiency in salmonids. Atlantic salmon, Baltic Sea, M74 syndrome, Salmon life cycle, Thiamin, Thiamin deficiencypublishedVersio