Hatching plasticity in a Southeast Asian tree frog mitigates submergence-induced mortality

Environmentally cued hatching has been well-documented in amphibians in response to a wide range of abiotic and biotic factors. The hatching of terrestrial amphibian eggs in response to flooding may be basal within the group, but amphibian lineages in tropical Asia and sub-Saharan Africa have not received as much attention as their Neotropical counterparts. We investigated submergence-induced hatching in Feihyla hansenae, a Rhacophorid tree frog with terrestrial eggs. We quantified natural rates of clutch submergence at our study site in Thailand. Using submergence experiments, we found that embryos are capable of hatching early to escape flooding, and that failure to hatch results in mortality. Among the embryos that were able to hatch early, only the earliest, youngest hatchlings experienced a trade-off in body size that persisted for 6 days, while later, older hatchlings were not significantly smaller than spontaneous hatchlings under control conditions. By incorporating our natural and experimental data into Monte Carlo methods to simulate and compare survival probabilities with and without hatching plasticity, we found an overall 3.1% increase in submergence survival due to hatching plasticity. Our findings support the idea that flooding-induced hatching is widespread across amphibians with terrestrial eggs and highlight the importance of researching understudied tropical regions. As climate change is projected to affect rainfall patterns, the ability of embryos to escape abiotic egg-stage threats may be an indicator of species' ability to flexibly navigate a changing environment.     

Antifreeze protein from Anatolia polita (ApAFP914) improved outcome of vitrified in vitro sheep embryos

Embryo cryopreservation is an important tool to preserve endangered species. As a cryoprotectant for mouse oocytes, antifreeze protein from Anatolica polita (ApAFP914) has demonstrated utility. In the present study, the effects of controlled slow freezing and vitrification methods on the survival rate of sheep oocytes fertilized in vitro after freezing-thawing were compared. Different ApAFP914 concentrations were added to the vitrification liquid for exploring the effect of antifreeze protein on the warmed embryos. The results showed that the survival and hatching rates of in vitro derived embryos were significantly higher than that of the slow freezing method. Furthermore, among the cryopreserved embryos at different developmental stages, the survival and hatching rates of the expanded blastocyst were significantly higher than those of the blastocysts, early blastocysts and morula. The survival and the hatching rates of the fast-growing embryos were both significantly higher than that of the slow-growing embryos. Additionally, treatment of ApAFP914 (5–30 μg/mL) did not increase the freezing efficiency of the 6–6.5 d embryos. However, addition of 10 μg/mL of ApAFP914 significantly increased the hatching rate of slow-growing embryos. In conclusion, our study suggests that the vitrification is better than the slow freezing method for the conservation of in vitro sheep embryos, and supplementation of ApAFP914 (10 μg/mL) significantly increased the hatching rate of slow-growing embryos after cryopreservation.     

Control of invasive predators improves breeding success of an endangered alpine passerine

Birds living in alpine environments are becoming increasingly impacted by human‐induced threats. We investigated the impacts of introduced mammalian predators on an endangered alpine species, the New Zealand Rockwren Xenicus gilviventris, and assessed whether predator control improved its breeding success. Nest monitoring revealed that the primary cause of nest failure was predation by invasive mammals, primarily Stoats Mustela erminea and House Mice Mus musculus. Daily survival rates (DSR) decreased with nest age, and nests were at their most vulnerable to predators just prior to fledging. DSR, egg‐hatching and fledgling rates were all improved by predator trapping, demonstrating the significant impacts that even low numbers of invasive predators can have on sensitive alpine and upland species.     

Sex,growth rate,rank order after brood reduction,and hatching date affect first‐year survival of long‐lived Herring Gulls

Among most species of birds, survival from hatching throughout the first year of life is generally lower than subsequent survival rates. Survival of young birds during their first year may depend on a combination of selection, learning, unpredictable resources, and environmental events (i.e., post‐fledging factors). However, knowledge about post‐fledging development in long‐lived species is usually limited due to a lengthy immature stage when individuals are generally unobservable. Therefore, pre‐fledging characteristics are often used to predict the survival of young birds. We assessed effects of nestling growth rates, hatching date, hatching asynchrony, brood size and rank order after brood reduction, and sex on first‐year survival of 137 fledglings using a mark‐resighting analysis. We found that the survival probability (Φ_1yr = 0.39) of first‐year Herring Gulls (Larus argentatus) in our study colony located at the outer port of Zeebrugge (Belgium) was lower than that of older individuals (Φ_>1yr = 0.75). All 10 models best supported by our data included nestling growth rate, suggesting that variability in first‐year survival may be linked primarily to individual variation in growth. First‐year survival was negatively correlated with hatching date and rank order after brood reduction. Hence, carry‐over effects of breeding season events such as timing of breeding, early development, and social status had an influence on survival of Herring Gulls after fledging. Furthermore, we found sex‐biased mortality in first‐year Herring Gulls, with females (Φ_1yr = 0.45) surviving better than males (Φ_1yr = 0.38). Although adult survival is generally regarded as the key parameter driving population trajectories in long‐lived species, juvenile survival has recently been acknowledged as an important source of variability in population growth rates. Thus, increasing our knowledge of factors affecting age‐specific survival rates is necessary to improve our understanding of population dynamics and ultimately life‐history variation.     

Kin Recognition in the largely Solitary Bee,Manuelia postica (Apidae: Xylocopinae)

The recognition of conspecifics is a central issue to social behaviour. In eusocial hymenopterans, kin recognition has been clearly demonstrated. Manuelia postica is a largely solitary bee species in which larvae develop inside individual cells within a nest and remain isolated from conspecifics until the destruction of partitions by adults. Nestmate recognition in M. postica has been previously demonstrated under experimental conditions. Isolation between individuals during development and nestmate recognition ability in adult females make M. postica an ideal species for testing the occurrence of kin recognition capacity in females. Kin recognition was demonstrated through cross‐fostering field experiments involving the single transfer of recently enclosed larvae, and subsequent laboratory recognition bioassays with emerging females. Results suggest kin recognition occurs through self‐referent phenotype matching. Given the basal position of Manuelia in the phylogeny of the Apidae, kin recognition may represent an ancestral recognition mechanism in Apidae species phylogenetically more derived than M. postica.     

Temperature‐mediated survival,development and hatching variation of Pacific cod Gadus macrocephalus eggs

Laboratory‐validated data on the survival, development and hatching responses of fertilized Pacific cod Gadus macrocephalus eggs from the northern Japan stock were determined through an incubation experiment. The optimum temperature for survival until hatching ranged from 4 to 8° C. No significant difference in development rates was found between the populations from Mutsu Bay, Japan, and western Canadian coastal waters even though the samples may belong to different G. macrocephalus stocks. Gadus macrocephalus larvae hatched asynchronously from egg batches despite incubation under the same environment during their development. Both incubation temperature and temperature‐mediated hatch rank affect size and yolk reserve. These data suggest that variations in water temperatures within an ecological range markedly influence the development rates, survival and hatching of the eggs, as well as the stage at hatch larvae of G. macrocephalus. Asynchronous hatching and the production of offspring with variable sizes and yolk reserves are considered evolutionary bet‐hedging strategies that enable the species to maximize their likelihood of survival in an environment with variable temperatures.     

When predator odour makes groups stronger: effects on behavioural and chemical adaptations in two termite species

1. Being able to detect a predator before any physical contact is crucial for individual survival. Predator presence can be detected thanks to several types of signal, such as chemical cues. Chemical signals are produced by predators for their protection against desiccation, for their communication, or possibly as a side‐effect of their activity. In insects, chemical communication plays a key role in diverse biological processes, including prey‐predator or plant‐insect interactions, courtship behaviour, and kin or species recognition. 2. Cuticular hydrocarbons (CHCs) are specifically involved in recognition processes and social organisation (division of labour, caste ratios) in social insects. Here, the questions raised are whether termites can detect a predator with their cuticular compounds and whether the predator‐produced compounds can influence their prey. 3. The responses of termites Reticulitermes grassei (Clément, 1978) and Reticulitermes flavipes (Kollar, 1837) to the presence of the cuticular compounds produced by a predator, the ant species Lasius niger (Linnaeus, 1758), were investigated. More specifically, the study quantified termite traits such as caste ratios, mortality rates, CHC profile homogeneity and aggressiveness of workers after 2 months' exposure to predator‐produced compounds. 4. The results show that the predator odour did affect the aggressiveness of the native species R. grassei but not of the invasive R. flavipes. The caste ratios and the mortality rates were not affected for both species. 5. Differences between species are discussed around the native or invasive status of each species, along with the role played by chemical cues on behavioural and chemical adaptations.     

Local adaptation and embryonic plasticity affect antipredator traits in hatchling pond snails

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Early development and allometric shifts during the ontogeny of a marine catfish (Cathorops spixii‐Ariidae)

This study assessed whether the developmental series of the ariid Cathorops spixii (Agassiz, 1829) is related to growth patterns during its early ontogeny. The main morphological events of C. spixii were studied from the newly neurula embryo (6.99±0.69 mm TL) to juveniles (53.38±14.43 mm TL) in order to characterize and corroborate patterns of ontogenetic allometries. Prior to hatching, embryos were well‐developed, with an ossified axial and appendicular skeleton. Embryos grew slowly, but positive allometric growth was observed in head width (β₁ = 1.65) and eye diameter (β₁ = 1.59). This seems to be related to the fast development of sensory organs such as otoliths, Weberian apparatus, lenses, nostrils and barbels during the embryonic period when eggs are under the care of adult males. After hatching, mouth‐brooding free‐embryos grew horizontally isometric, except for the snout length that presented quick growth related to the end of endogenous feeding (β₁ = 1.73). Slow growth was observed in head width (β₁ = 0.44) and eye diameter (β₁ = 0.26), taking into account that sensory organs are formed in free‐embryos. The end of the yolk‐sac period was characterized by a direct change from free‐embryo to juvenile, without a true larval period. Juveniles are characterized by growth patterns nearly isometric in all body regions, suggesting that they already bear most of characteristics of adult fish. The quick growth of morphometric variables that are related to sensorial organs before hatching and the increase in horizontal growth after the first 6 weeks (hatched free‐embryos) reflect developmental priorities during the earliest stages where important sensorial organs are being developed for juvenile survival strategies.     

Do Parents and Helpers Discriminate between Related and Unrelated Nestlings in the Cooperative Breeding Silver‐Throated Tit?

When benefits exceed costs, natural selection may favor adults that develop the ability to recognize and preferentially direct care toward their own offspring to maximize their fitness. Investigations into the ability of adults to recognize offspring in offspring's early development period may help to understand when the ability of kin recognition starts to develop. In birds, studies of offspring recognition have mainly been conducted on bi‐parental breeding species, but relatively seldom on cooperative breeding species, despite that kin recognition may be of particular importance for cooperative breeders. The silver‐throated tit Aegithalos glaucogularis is a small passerine in which some nests have helpers during breeding. We tested whether silver‐throated tit parents and helpers were able to distinguish between their own and alien nestlings 2–5 d before fledging when recognition mechanisms were likely to have been developed. Through two forced choice experiments, of which one was conducted right beside the experimental nests (<0.8 m) and the other far away from the experimental nests (~6 m), we found that neither parents nor helpers discriminatively fed their own and alien nestlings, which suggested that at least during the experimental nestling age, and within the 6‐m‐radius area around the nests, they might not have the ability to recognize offspring. The possibility that silver‐throated tits use a larger area (>6 m radius) around their nests as a location‐based cue for offspring recognition, or would develop an offspring recognition ability at an older nestling age and/or even after fledging, warrants future studies.     

Timing matters: species‐specific interactions between spawning time,substrate quality,and recruitment success in three salmonid species

Substratum quality and oxygen supply to the interstitial zone are crucial for the reproductive success of salmonid fishes. At present, degradation of spawning grounds due to fine sediment deposition and colmation are recognized as main factors for reproductive failure. In addition, changes in water temperatures due to climate change, damming, and cooling water inlets are predicted to reduce hatching success. We tested the hypothesis that the biological effects of habitat degradation depend strongly on the species‐specific spawning seasons and life‐history strategies (e.g., fall‐ vs. spring‐spawners, migratory vs. resident species) and assessed temperature as an important species‐specific factor for hatching success within river substratum. We studied the species‐specific differences in their responses to such disturbances using egg‐to‐fry survival of Danube Salmon (Hucho hucho), resident brown trout (Salmo trutta fario), and migratory brown trout (Salmo trutta lacustris) as biological endpoint. The egg incubation and hatching success of the salmonids and their dependence on temperature and stream substratum quality were compared. Hatching rates of Danube salmon were lower than of brown trout, probably due to higher oxygen demands and increased interstitial respiration in spring. Increases in maximum water temperature reduced hatching rates of resident and migratory brown trout (both fall‐spawners) but were positively correlated with hatching rates of Danube salmon (a spring‐spawner). Significantly longer incubation periods of resident and migratory brown trout coincided with relatively low stream substratum quality at the end of the egg incubation. Danube salmon seem to avoid low oxygen concentrations in the hyporheic zone by faster egg development favored by higher water temperatures. Consequently, the prediction of effects of temperature changes and altered stream substratum properties on gravel‐spawning fishes and biological communities should consider the observed species‐specific variances in life‐history strategies to increase conservation success.     

Kin discrimination in sticklebacks is mediated by social learning rather than innate recognition

Theory predicts several advantages for animals to recognize kin. These include inbreeding avoidance and an increase in inclusive fitness. In shoaling species, kin recognition may lead to an increased amount of altruism among shoal members. Adult, non‐reproductive three‐spined sticklebacks, Gasterosteus aculeatus, prefer to shoal with kin. This preference was shown for familiar as well as for unfamiliar individuals. However, whether it is based on learned cues of familiar individuals or on innate mechanisms like self‐referent phenotype matching or ‘true’ kin recognition through recognition alleles remains unknown. In our experiments, juvenile fish were given the choice between shoals that differed in relatedness and familiarity. The number of testfish who joined each group indicated that sticklebacks prefer to shoal with familiar kin when the alternative shoal was composed of unfamiliar non‐kin. When one shoal consisted of familiar kin while the second consisted of familiar non‐kin testfish did not show any preference. Kin recognition in sticklebacks is thus most likely mediated by social learning.     

Early breeding protects anuran eggs from Saprolegnia infection

Here, we studied the ecological significance of Saprolegnia infections (‘saprolegniasis’) on the survival and development of two populations of the endemic Patagonian anuran Pleurodema thaul (Anura, Leiuperidae). We found that four different Saprolegnia species infected eggs and embryos of P. thaul, indicating that the infection by these ‘zoosporic fungi’ was different in each anuran population and among different cohorts. Late anuran cohorts generally showed a higher incidence of infection than early cohorts, but we observed no clear overall pattern between populations. In addition, in laboratory experiments, we determined that some of the Saprolegnia species induce early hatching, and that hatching timing was variable between populations. In summary, we found that early breeding (by underlying priority effects) could improve the survival of the earliest cohorts of P. thaul by allowing them to survive the stress imposed by epidemic events of Saprolegnia.     

Heterospecific sperm reduction in interspecific crosses between two closely related phytophagous ladybird beetles,Henosepilachna vigintioctomaculata and H. pustulosa (Coleoptera: Coccinellidae)

In interspecific crosses, a mismatch in internal physiological conditions between two species can reduce sperm viability in the interval from insemination to fertilization, leading to gametic isolation. Two closely related Japanese phytophagous ladybird beetles, Henosepilachna vigintioctomaculata and H. pustulosa, show several isolating barriers, including reduction in the number of heterospecific sperm in the female reproductive tract and low egg‐hatching rates in interspecific matings. However, the mechanisms of these two potential isolating barriers and the association between them are unknown. Here we investigated temporal changes in the number of sperm stored in the female reproductive tract and egg‐hatching rates in inter‐ and intraspecific crosses between these species. Although the number of sperm decreased after both inter‐ and intraspecific crosses, the reduction was more drastic in inter‐ than in intraspecific crosses for females of both species. Most of the sperm reduction occurred early on, during sperm transfer from the bursa copulatrix to the paired ampullae of the common oviduct (the sperm storage organs). These two species also demonstrated stably low egg‐hatching rates in interspecific crosses. Since the degree and timing of the sperm reduction did not correlate with egg‐hatching rates, the reduction in heterospecific sperm in interspecific crosses may not directly cause the low hatching rates. These two isolating barriers could be different expressions of the physiological mismatch and/or genetic incompatibility between gametes of these species.     

Cannibalistic siblicide in praying mantis nymphs (Miomantis caffra)

Inclusive fitness theory predicts that cannibalism should be more likely to arise if close relatives can be avoided, suggesting that cannibalistic species will possess mechanisms for minimizing predation on kin. Juvenile Miomantis caffra are good candidates for the possession of such traits because; (1) groups of siblings hatch together into the same locale, (2) they are aggressive hunters, and (3) they are strongly cannibalistic. In this study, the possibility of kin recognition or avoidance in M. caffra is investigated by laboratory comparison of cannibalism rates between groups of differing relatedness. In order to examine the likelihood of encounters between early instar siblings, the extent of dispersal away from the ootheca in the days following hatching is also observed. Nymphs did not rapidly disperse after hatching, so the chances of full siblings encountering one another in the wild appear to be high. Despite this, cannibalism was equally high in groups of full siblings and groups of mixed parenthood. We suggest that for M. caffra, a generalist ambush predator, the benefits of indiscriminate aggression may outweigh any inclusive fitness benefits that would be gained from kin discrimination.     

KIN‐BASED RECOGNITION AND SOCIAL AGGREGATION IN A CILIATE

Aggregative groups entail costs that must be overcome for the evolution of complex social interactions. Understanding the mechanisms that allow aggregations to form and restrict costs of cheating can provide a resolution to the instability of social evolution. Aggregation in Tetrahymena thermophila is associated with costs of reduced growth and benefits of improved survival through “growth factor” exchange. We investigated what mechanisms contribute to stable cooperative aggregation in the face of potential exploitation by less‐cooperative lines using experimental microcosms. We found that kin recognition modulates aggregative behavior to exclude cheaters from social interactions. Long‐distance kin recognition across patches modulates social structure by allowing recruitment of kin in aggregative lines and repulsion in asocial lines. Although previous studies have shown a clear benefit to social aggregation at low population densities, we found that social aggregation has very different effects at higher densities. Lower growth rates are a cost of aggregation, but also present potential benefits when restricted to kin aggregations: slow growth and crowd tolerance allow aggregations to form and permit longer persistence on ephemeral resources. Thus in highly dynamic metapopulations, kin recognition plays an important role in the formation and stability of social groups that increase persistence through cooperative consumptive restraint.     

Climate changes influence free‐living stages of soil‐transmitted parasites of European rabbits

Climate warming has been suggested to augment the risk of infectious disease outbreaks by extending the seasonal window for parasite growth and by increasing the rate of transmission. Understanding how this occurs in parasite‐host systems is important for appreciating long‐term and seasonal changes in host exposure to infection and to reduce species extinction caused by diseases. We investigated how free‐living stages of two soil‐transmitted helminths of the European rabbit (Oryctolagus cuniculus) responded to experimental changes in temperature by performing laboratory experiments with environmental chambers and field manipulations using open‐top‐chambers. This study was motivated by our previous observations that air temperature has increased over the last 30 years in our field site and that during this period intensity of infection of Graphidium strigosum but not Trichostrongylus retortaeformis was positively associated with this temperature increase. Laboratory and field experiments showed that both parasites accelerated egg development and increased hatching rate and larval survival in response to accumulating thermal energy. Both parasites behaved similarly when exposed to diverse temperature regimes, decadal trends, and monthly fluctuations, however, T. retortaeformis was more successful than G. strigosum by showing higher rates of egg hatching and larval survival. Across the months, the first day of hatching occurred earlier in warmer conditions suggesting that climate warming can lengthen the period of parasite growth and host exposure to infective stages. Also, T. retortaeformis hatched earlier than G. strigosum. These findings showed that seasonal changes in intensity, frequency, and duration of daily temperature are important causes of variability in egg hatching and larva survival. Overall, this study emphasizes the important role of climate warming and seasonality on the dynamics of free‐living stages in soil‐transmitted helminths and their contribution to enhance host exposure to parasitic infections. Yet, the ability to infect might ultimately depend on how hosts interact with parasites.     

Fine‐scale kin recognition in the absence of social familiarity in the Siberian jay,a monogamous bird species

Kin recognition is a critical element to kin cooperation, and in vertebrates, it is primarily based on associative learning. Recognition of socially unfamiliar kin occurs rarely, and it is reported only in vertebrate species where promiscuity prevents recognition of first‐order relatives. However, it is unknown whether the recognition of socially unfamiliar kin can evolve in monogamous species. Here, we investigate whether genetic relatedness modulates aggression among group members in Siberian jays (Perisoreus infaustus). This bird species is genetically and socially monogamous and lives in groups that are formed through the retention of offspring beyond independence, and the immigration of socially unfamiliar nonbreeders. Observations on feeders showed that genetic relatedness modulated aggression of breeders towards immigrants in a graded manner, in that they chased most intensely the immigrant group members that were genetically the least related. However, cross‐fostering experiments showed that breeders were equally tolerant towards their own and cross‐fostered young swapped as nestlings. Thus, breeders seem to use different mechanisms to recognize socially unfamiliar individuals and own offspring. As Siberian jays show a high degree of nepotism during foraging and predator encounters, inclusive fitness benefits may play a role for the evolution of fine‐scale kin recognition. More generally, our results suggest that fine‐graded kin recognition can evolve independently of social familiarity, highlighting the evolutionary importance of kin recognition for social species.     

Thermal adaptation and phenotypic plasticity in a warming world: Insights from common garden experiments on Alaskan sockeye salmon

An important unresolved question is how populations of coldwater‐dependent fishes will respond to rapidly warming water temperatures. For example, the culturally and economically important group, Pacific salmon (Oncorhynchus spp.), experience site‐specific thermal regimes during early development that could be disrupted by warming. To test for thermal local adaptation and heritable phenotypic plasticity in Pacific salmon embryos, we measured the developmental rate, survival, and body size at hatching in two populations of sockeye salmon (Oncorhynchus nerka) that overlap in timing of spawning but incubate in contrasting natural thermal regimes. Using a split half‐sibling design, we exposed embryos of 10 families from each of two populations to variable and constant thermal regimes. These represented both experienced temperatures by each population, and predicted temperatures under plausible future conditions based on a warming scenario from the downscaled global climate model (MIROC A1B scenario). We did not find evidence of thermal local adaptation during the embryonic stage for developmental rate or survival. Within treatments, populations hatched within 1 day of each other, on average, and among treatments, did not differ in survival in response to temperature. We did detect plasticity to temperature; embryos developed 2.5 times longer (189 days) in the coolest regime compared to the warmest regime (74 days). We also detected variation in developmental rates among families within and among temperature regimes, indicating heritable plasticity. Families exhibited a strong positive relationship between thermal variability and phenotypic variability in developmental rate but body length and mass at hatching were largely insensitive to temperature. Overall, our results indicated a lack of thermal local adaptation, but a presence of plasticity in populations experiencing contrasting conditions, as well as family‐specific heritable plasticity that could facilitate adaptive change.     

Investigating the Effect of Familiarity on Kin Recognition of Three‐Spined Stickleback (Gasterosteus aculeatus)

The ability to discriminate between related and unrelated individuals has been demonstrated in many species. The mechanisms behind this ability might be manifold and depend on the ecological context in which the species lives. In brood‐caring species, both familiarity and phenotype matching are known to be used in kin recognition. However, results of studies disentangling these two phenomena have proved contradictory. We aimed to broaden our knowledge about the mechanisms of kin recognition using shoaling preferences of three‐spined stickleback (Gasterosteus aculeatus) as a model behavior. In our first experiment, focal fish had the choice to shoal either with kin or unfamiliar non‐kin. In half of the trials, kin groups were composed of familiar individuals, while they were unfamiliar in the other half. Focal fish significantly preferred kin as shoaling partner, a result which was not reinforced by familiarity. In our second experiment, focal fish were given the choice between a shoal of familiar kin and a shoal of unfamiliar kin. Here, focal fish did not show any significant preference. These results indicate that familiarity does not impact stickleback's ability to recognize kin. Furthermore, they show that familiarity does not overrule recognition based on phenotype matching or innate recognition, underlining the importance of these mechanisms. Finally, our results lead to the assumption that individual recognition might play a minor role also in non‐kin‐based preferences for familiars.