Evidence for a reproductive sharing continuum in cooperatively breeding mammals and birds: consequences for comparative research.

Extreme reproductive skew occurs when a dominant female/male almost monopolizes reproduction within a group of multiple sexually mature females/males, respectively. It is sometimes considered an additional, restrictive criterion to define cooperative breeding. However, datasets that use this restrictive definition to classify species as cooperative breeders systematically overestimate reproductive skew by including groups in which reproduction cannot be shared by definition (e.g. groups with a single female/male). Here, we review the extent of reproductive sharing in 41 mammal and 37 bird species previously classified as exhibiting alloparental care and extreme reproductive skew, while only considering multi-female or multi-male groups. We demonstrate that in groups where unequal reproduction sharing is possible, extreme reproductive skew occurs in a few species only (11/41 mammal species and 12/37 bird species). These results call for significant changes in datasets that classify species' caring and mating system. To facilitate these changes, we provide an updated dataset on reproductive sharing in 63 cooperatively breeding species. At the conceptual level, our findings suggest that reproductive skew should not be a defining criterion of cooperative breeding and support the definition of cooperative breeding as a care system in which alloparents provide systematic care to other group members' offspring.

Immediate effects of nectar robbing by Palestine sunbirds (Nectarinia osea) on nectar alkaloid concentrations in tree tobacco (Nicotiana glauca).

Plant secondary metabolites (PSMs), such as alkaloids, are often found in many parts of a plant, including flowers, providing protection to the plant from various types of herbivores or microbes. PSMs are also present in the floral nectar of many species, but typically at lower concentrations than in other parts of the plant. Nectar robbers often damage floral tissue to access the nectar. By doing so, these nectar robbers may initiate an increase of PSMs in the floral nectar. It is often assumed that it takes at least a few hours before the plant demonstrates an increase in PSMs. Here, we addressed the question of whether PSMs in the floral tissue are immediately being released into the floral nectar following nectar robbing. To address this research question, we investigated whether there was an immediate effect of nectar robbing by the Palestine Sunbird (Nectarinia osea) on the concentration of nectar alkaloids, nicotine and anabasine, in Tree Tobacco (Nicotiana glauca). We found that the concentration of anabasine, but not nicotine, significantly increased in floral nectar immediately following simulated nectar robbing. These findings suggest that nectar robbers could be ingesting greater amounts of PSMs than they would if they visit flowers legitimately. As a consequence, increased consumption of neurotoxic nectar alkaloids or other PSMs could have negative effects on the nectar robber.

What is cooperative breeding in mammals and birds? Removing definitional barriers for comparative research.

Cooperative breeding (i.e. when alloparents care for the offspring of other group members) has been studied for nearly a century. Yet, inconsistent definitions of this breeding system still hamper comparative research. Here, we identify two major inconsistencies, discuss their consequences and propose a way forward. First, some researchers restrict the term 'cooperative breeding' to species with non-breeding alloparents. We show that such restrictive definitions lack distinct quantitative criteria to define non-breeding alloparents. This ambiguity, we argue, reflects the reproductive-sharing continuum among cooperatively breeding species. We therefore suggest that cooperative breeding should not be restricted to the few species with extreme reproductive skew and should be defined independent of the reproductive status of alloparents. Second, definitions rarely specify the type, extent and prevalence of alloparental care required to classify species as cooperative breeders. We thus analysed published data to propose qualitative and quantitative criteria for alloparental care. We conclude by proposing the following operational definition: cooperative breeding is a reproductive system where >5% of broods/litters in at least one population receive species-typical parental care and conspecifics provide proactive alloparental care that fulfils >5% of at least one type of the offspring's needs. This operational definition is designed to increase comparability across species and disciplines while allowing to study the intriguing phenomenon of cooperative breeding as a behaviour with multiple dimensions.

Predator-released hydrocarbons repel oviposition by a mosquito.

Prey species commonly use predator-released kairomones (PRKs) to detect risk of predation, yet the chemical identity of PRKs remains elusive. Chemical identification of PRKs will facilitate the study of predator-prey interactions and the risk of predation, and when the prey are pests, will potentially provide environmentally friendly means of pest control. In temporary pools of the Mediterranean and Middle East, larvae of the mosquito Culiseta longiareolata Macquart are highly vulnerable to the common predatory backswimmer, Notonecta maculata Fabricius. We demonstrate that N. maculata releases two hydrocarbons, n-heneicosane and n-tricosane, which repel ovipositing females of C. longiareolata. In behavioural tests with environmentally relevant chemical concentrations in outdoor mesocosm experiments, the repellent effects of the two compounds were additive at the tested concentrations.

Weighing density and kinship: Aggressive behavior and time allocation in fire salamander (Salamandra infraimmaculata).

Kin-biased behavior (that is responding differentially to kin and non-kin) is thought to be adaptive in many social interactions. One example of this kin bias is behaving less aggressively toward a relative than a non-relative, a behavior which yields inclusive fitness benefits. However, data are lacking about the ability of animals to weigh their preference for kinship and the density of conspecifics simultaneously and to respond accordingly. Fire salamanders (Salamandra infraimmaculata) larviposit in high densities in ponds. Thus, larvae of different females confront competition and predation by other larvae. We studied whether larvae prefer their kin over particular density or vice versa. We experimentally used a transparent glass aquarium with inner chambers to test the responses of a focal larva toward its siblings and non-siblings. Specifically, we quantified the time a focal larva spent near its siblings or non-siblings, presented in varying densities, and the aggression level it demonstrated. We found that focal larvae spent more time near non-siblings if non-sibling and sibling groups were of equal density. The focal larvae were also more aggressive toward non-siblings. The results may be explained by the cannibalistic nature of these larvae: high density may provide more opportunities for food, especially when non-siblings are present. Further explanations for these findings may include other advantages of staying in a larger group and/or the stronger olfactory and visual stimulation offered by groups compared to a single individual. These findings suggest that larvae make differential responses toward conspecifics depending simultaneously on the level of relatedness and the density of the group. Such responses have important implications for social-aggregation decisions and may especially affect the fitness of cannibalistic species.

Autumn temperatures at African wintering grounds affect body condition of two passerine species during spring migration.

Most papers on the physical condition of birds during spring migration focused on food availability preceding migratory take-off. Only a few studies examined the effect of climate conditions at the wintering grounds upon autumn arrival on bird physical condition later on. Here, we hypothesized that environmental conditions upon arrival at the wintering grounds, and not necessarily upon departure, have a crucial carry-over effect on bird spring migration. Using 29,000 observations of the lesser whitethroat, Sylvia curruca, and the eastern Bonelli's warbler, Phylloscopus orientalis, we found temperatures upon arrival at the African wintering grounds to be the only climatic variable correlated with birds' body state upon spring stopover in Israel, six months later. Two different mechanisms could explain these results. One possibility is that high temperatures create favorable conditions for insect activity, which allows rapid recovery from autumn migration and hence successful winter survival and maintenance. Another possible scenario is that harsh conditions, due to the heat and dry environment, cause high mortality, permitting survival of larger individuals which, then, enjoy reduced inter- and intra-specific competition. Whatever the mechanism is, our findings suggest that conditions upon autumn arrival, and not necessarily at the end of winter as traditionally thought, may have a major impact on migrating birds.

Endocrine disrupting chemicals accumulate in earthworms exposed to sewage effluent.

Endocrine disrupting chemicals (EDCs) can alter endocrine function in exposed animals. Such critical effects, combined with the ubiquity of EDCs in sewage effluent and potentially in tapwater, have led to concerns that they could be major physiological disruptors for wildlife and more controversially for humans. Although sewage effluent is known to be a rich source of EDCs, there is as yet no evidence for EDC uptake by invertebrates that live within the sewage treatment system. Here, we describe the use of an extraction method and GC-MS for the first time to determine levels of EDCs (e.g., dibutylphthalate, dioctylphthalate, bisphenol-A and 17beta-estradiol) in tissue samples from earthworms (Eisenia fetida) living in sewage percolating filter beds and garden soil. To the best of our knowledge, this is the first such use of these techniques to determine EDCs in tissue samples in any organism. We found significantly higher concentrations of these chemicals in the animals from sewage percolating filter beds. Our data suggest that earthworms can be used as bioindicators for EDCs in these substrates and that the animals accumulate these compounds to levels well above those reported for waste water. The potential transfer into the terrestrial food chain and effects on wildlife are discussed.

February precipitation in the wintering grounds of the lesser whitethroat, Sylvia curruca: is it a cue for migration onset?

Numerous studies report shifts in bird migration phenology, presumably owing to global warming. However, most studies focus on migration patterns in the Northern Hemisphere. In this study, we investigated associations between weather conditions in African wintering grounds of the lesser whitethroat, Sylvia curruca, and spring arrival time in Eilat, Israel. Using multivariate regression models, we analysed a 30-year dataset in order to examine correlations between median springtime arrival and 46 climate variables of the wintering quarters. The model obtained exhibited a highly statistical fit, involving mean precipitation in February and March with negative effects and number of wet days during November-February. February precipitation levels were also the major factor associated with the interquartile range of arrival time. Interestingly and contrary to published results, annual or seasonal precipitation showed no correlation with spring arrival time, nor did temperature. Moreover, winter in this region falls into dry season with negligible rainfall quantities. Hence, it is unlikely that precipitation effect on habitat productivity is a driving force of migration, as suggested by other studies. Instead, we propose that precipitation in February acts as a cue for the birds, indicating the approach of spring and migration time.

Facultative adjustment of pre-fledging mass loss by nestling swifts preparing for flight.

Nestling birds often maintain nutritional reserves to ensure continual growth during interruptions in parental provisioning. However, mass-dependent flight costs require the loss of excess mass before fledging. Here we test whether individual variable mass loss prior to fledging is controlled through facultative adjustments by nestlings, or whether it reflects physiologically inflexible developmental schedules. We show that in the face of natural and experimental variation in nestling body mass and wing length, swifts always achieve very similar wing loadings (body mass per wing area) prior to fledging, presumably because this represents the optimum for flight. Experimental weights (approx. 5% body mass) temporarily attached to nestlings caused additional reductions in mass, such that final wing loadings still matched those of control siblings. Experimental reductions in nestling wing length (approx. 5% trimmed from feather tips) resulted in similar additional mass reductions, allowing wing loadings at fledging to approach control levels. We suggest that nestlings may assess their body mass relative to wing area via wing flapping and special 'push-ups' (on the tips of extended wings) performed in the nest. Thus, by facultatively adjusting body mass, but not wing growth, nestling swifts are always able to fledge with aerodynamically appropriate wing loadings.

Parental self-feeding effects on parental care levels and time allocation in Palestine sunbirds.

The trade-off between parents feeding themselves and their young is an important life history problem that can be considered in terms of optimal behavioral strategies. Recent studies on birds have tested how parents allocate the food between themselves and their young. Until now the effect of food consumption by parent birds on their food delivery to their young as well as other parental activities has rarely been studied. I have previously shown that parent Palestine sunbirds (Nectarinia osea) will consume nectar and liquidized arthropods from artificial feeders. However, they will only feed their young with whole arthropods. This provided a unique opportunity to experimentally manipulate the food eaten by parents independent of that fed to their offspring. Here, I hypothesized that parents invest in their current young according to the quality of food that they themselves consume. Breeding pairs with two or three nestlings were provided with feeders containing water (control), sucrose solution (0.75 mol) or liquidized mealworms mixed with sucrose solution (0.75 mol). As food quality in feeders increased (from water up to liquidized mealworms mixed with sucrose solution): 1) Parents (especially females) increased their food delivery of whole arthropod prey to their young. 2) Only males increased their nest guarding effort. Nestling food intake and growth rate increased with increasing food quality of parents and decreasing brood size. These results imply that increasing the nutrient content of foods consumed by parent sunbirds allow them to increase the rate at which other foods are delivered to their young and to increase the time spent on other parental care activities.

Stable isotope analysis provides new information on winter habitat use of declining avian migrants that is relevant to their conservation.

Winter habitat use and the magnitude of migratory connectivity are important parameters when assessing drivers of the marked declines in avian migrants. Such information is unavailable for most species. We use a stable isotope approach to assess these factors for three declining African-Eurasian migrants whose winter ecology is poorly known: wood warbler Phylloscopus sibilatrix, house martin Delichon urbicum and common swift Apus apus. Spatially segregated breeding wood warbler populations (sampled across a 800 km transect), house martins and common swifts (sampled across a 3,500 km transect) exhibited statistically identical intra-specific carbon and nitrogen isotope ratios in winter grown feathers. Such patterns are compatible with a high degree of migratory connectivity, but could arise if species use isotopically similar resources at different locations. Wood warbler carbon isotope ratios are more depleted than typical for African-Eurasian migrants and are compatible with use of moist lowland forest. The very limited variance in these ratios indicates specialisation on isotopically restricted resources, which may drive the similarity in wood warbler populations' stable isotope ratios and increase susceptibility to environmental change within its wintering grounds. House martins were previously considered to primarily use moist montane forest during the winter, but this seems unlikely given the enriched nature of their carbon isotope ratios. House martins use a narrower isotopic range of resources than the common swift, indicative of increased specialisation or a relatively limited wintering range; both factors could increase house martins' vulnerability to environmental change. The marked variance in isotope ratios within each common swift population contributes to the lack of population specific signatures and indicates that the species is less vulnerable to environmental change in sub-Saharan Africa than our other focal species. Our findings demonstrate how stable isotope research can contribute to understanding avian migrants' winter ecology and conservation status.

Oviposition habitat selection by Anopheles gambiae in response to chemical cues by Notonecta maculata.

A number of mosquito species avoid predator-inhabited oviposition sites by detecting predator-released kairomones. In the laboratory, we found that when offered de-ionized water and de-ionized water conditioned with Notonecta maculata, gravid Anopheles gambiae females preferentially oviposited into the former. We then conducted further experiments using two chemical components found in Notonecta-conditioned water, chemically pure n-tricosane and/or n-heneicosane, that was previously shown to repel oviposition by Culiseta longiareolata. These hydrocarbons failed to deter oviposition by An. gambiae females. Thus, different mosquito species may rely on distinct chemical cues to avoid predators. Identification and chemical characterization of such kairomones could facilitate innovative, environmentally sound mosquito control.

Detection of endocrine disrupting chemicals in aerial invertebrates at sewage treatment works.

Endocrine disrupting chemicals (EDCs) constitute a diverse group of chemical compounds which can alter endocrine function in exposed animals. Whilst most studies have focussed on exposure of wildlife to EDCs via aquatic routes, there is the potential for transfer into the terrestrial food chain through consumption of contaminated prey items developing in sewage sludge and waste water at sewage treatment works. In this study, we determine levels of EDCs in aerial insects whose larval stages develop on percolating filter beds at sewage treatment works. We compare absolute concentrations of known EDCs with those collected from aquatic environments not exposed to sewage effluent outflow. Our findings document for the first time that aerial invertebrates developing on sewage filter beds take up a range of chemicals thought to be incorporated from the sewage effluent, which act as endocrine disruptors. For two synthetic chemicals (17alpha-ethinylestradiol and butylated hydroxy aniline), concentrations were significantly higher in insects captured around percolating filter beds than sites over 2 km from the nearest sewage works. A number of species of insectivorous bats and birds, some of which are declining or threatened, use sewage works as principle foraging sites. We calculate approximate exposure levels for a species of bat known to forage within sewage works and suggest that further research is warranted to assess the ecological implications of consuming contaminated invertebrate prey.

Pollutants increase song complexity and the volume of the brain area HVC in a songbird.

Environmental pollutants which alter endocrine function are now known to decrease vertebrate reproductive success. There is considerable evidence for endocrine disruption from aquatic ecosystems, but knowledge is lacking with regard to the interface between terrestrial and aquatic ecosystems. Here, we show for the first time that birds foraging on invertebrates contaminated with environmental pollutants, show marked changes in both brain and behaviour. We found that male European starlings (Sturnus vulgaris) exposed to environmentally relevant levels of synthetic and natural estrogen mimics developed longer and more complex songs compared to control males, a sexually selected trait important in attracting females for reproduction. Moreover, females preferred the song of males which had higher pollutant exposure, despite the fact that experimentally dosed males showed reduced immune function. We also show that the key brain area controlling male song complexity (HVC) is significantly enlarged in the contaminated birds. This is the first evidence that environmental pollutants not only affect, but paradoxically enhance a signal of male quality such as song. Our data suggest that female starlings would bias their choice towards exposed males, with possible consequences at the population level. As the starling is a migratory species, our results suggest that transglobal effects of pollutants on terrestrial vertebrate physiology and reproduction could occur in birds.

Sex differences in food intake and digestive constraints in a nectarivorous bird.

Sex-specific foraging behaviour might be influenced by digestive constraints. However, evidence for sex differences in digestive performance is limited. Various physiological traits are known to be body size dependent. Therefore, we hypothesized that body size differences between male and female birds may lead to differences in their digestive characteristics. We predicted that if food intake and digestive functions are only governed by body mass, then males that are heavier than females would have higher food intake, food assimilation efficiency and gut transit time, but not after controlling for the effect of body mass. We fed a diet of equicaloric solutions of sucrose and a 1:1 mixture of glucose and fructose (hexose mixture) solutions to Palestine sunbirds (Nectarinia osea). When fed sucrose solutions, males had longer transit times but similar absorption efficiencies as females. Transit times, corrected for differences in body mass and food intake, were still longer in males than in females when fed on sucrose solutions. The sex-specific differences in transit time disappeared when the birds were fed the hexose mixture. Our results suggest that males take longer to digest than females when fed on sucrose-rich nectars as opposed to hexose-rich nectars, and therefore can allow themselves a relatively lower digestive capacity. This may suggest sex-specific co-evolution of sunbirds within mixed plant communities, which have both sucrose- and hexose-rich nectar-producing plants. Furthermore, future studies on digestion in birds may pay attention to sex-specific differences.