Insectivorous bats form mobile sensory networks to optimize prey localization: The case of the common noctule bat.

Animals that depend on ephemeral, patchily distributed prey often use public information to locate resource patches. The use of public information can lead to the aggregation of foragers at prey patches, a mechanism known as local enhancement. However, when ephemeral resources are distributed over large areas, foragers may also need to increase search efficiency, and thus apply social strategies when sampling the landscape. While sensory networks of visually oriented animals have already been confirmed, we lack an understanding of how acoustic eavesdropping adds to the formation of sensory networks. Here we radio-tracked a total of 81 aerial-hawking bats at very high spatiotemporal resolution during five sessions over 3 y, recording up to 19 individuals simultaneously. Analyses of interactive flight behavior provide conclusive evidence that bats form temporary mobile sensory networks by adjusting their movements to neighboring conspecifics while probing the airspace for prey. Complementary agent-based simulations confirmed that the observed movement patterns can lead to the formation of mobile sensory networks, and that bats located prey faster when networking than when relying only on local enhancement or searching solitarily. However, the benefit of networking diminished with decreasing group size. The combination of empirical analyses and simulations elucidates how animal groups use acoustic information to efficiently locate unpredictable and ephemeral food patches. Our results highlight that declining local populations of social foragers may thus suffer from Allee effects that increase the risk of collapses under global change scenarios, like insect decline and habitat degradation.

BREEDING AND NEONATAL REARING PRACTICES AND CHALLENGES IN LESSER HEDGEHOG TENRECS (ECHINOPS TELFAIRI) IN NORTH AMERICAN ZOOS.

The unique reproductive and energetic features of lesser hedgehog tenrecs (Echinops telfairi) have been intensively studied in the field and within laboratory settings, but information on their propagation in zoological settings is limited. Based on a survey sent to zoological institutions currently housing reproductively active lesser hedgehog tenrecs in North America, this study reports on husbandry, veterinary practices, and demographics of reproducing lesser hedgehog tenrecs and their offspring. All 14 zoological institutions in the Lesser Hedgehog Tenrec Species Survival Plan who bred tenrecs within the last 12 years responded to the online survey. Provision of a nest box, nesting material, and a diet consisting of a commercial insectivore diet, insects, and produce was found in the majority of institutions, in addition to the practice of separating the breeding male and female before parturition. From the 24 dams representing 39 pregnancies and 158 young included in this study, the median calculated litter size was four young per litter. The median age of primiparity was 2.25 yr, and the oldest female to reproduce successfully was 10 yr old. The young had an overall rate of survival to weaning of 83%. A maternal complication rate of 26% and maternal mortality rate of 5% highlights the importance of veterinary care in periparturient dams, especially for detection and treatment of dystocia. These data provide guidance to zoological institutions breeding lesser hedgehog tenrecs.

Insectivorous bats are less active near freeways.

Traffic disturbances (i.e. pollution, light, noise, and vibrations) often extend into the area surrounding a road creating a 'road-effect zone'. Habitat within the road-effect zone is degraded or, in severe cases, completely unsuitable for wildlife, resulting in indirect habitat loss. This can have a disproportionate impact on wildlife in highly modified landscapes, where remaining habitat is scarce or occurs predominantly along roadside reserves. In this study, we investigated the road-effect zone for insectivorous bats in highly cleared agricultural landscapes by quantifying the change in call activity with proximity to three major freeways. The activity of seven out of 10 species of bat significantly decreased with proximity to the freeway. We defined the road-effect zone to be the proximity at which call activity declined by at least 20% relative to the maximum detected activity. The overall road-effect zone for bats in this region was 307 m, varying between 123 and 890 m for individual species. Given that this road-effect zone exceeds the typical width of the roadside verges (<50 m), it is possible that much of the vegetation adjacent to freeways in this and similar landscapes provides low-quality habitat for bats. Without accounting for the road-effect zone, the amount of habitat lost or degraded due to roads is underestimated, potentially resulting in the loss of wildlife, ecosystem services and key ecosystem processes (e.g. predator-prey or plant-pollinator interactions) from the landscape. We suggest all future environmental impact assessments include quantifying the road-effect zone for sensitive wildlife, in order to best plan and mitigate the impact of roads on the environment. Mitigating the effects of new and existing roads on wildlife is essential to ensure enough high-quality habitat persists to maintain wildlife populations.

A global class reunion with multiple groups feasting on the declining insect smorgasbord.

We report a detection of a surprising similarity in the diet of predators across distant phyla. Though just a first glimpse into the subject, our discovery contradicts traditional aspects of biology, as the earliest notions in ecology have linked the most severe competition of resources with evolutionary relatedness. We argue that our finding deserves more research, and propose a plan to reveal more information on the current biodiversity loss around the world. While doing so, we expand the recently proposed conservation roadmaps into a parallel study of global interaction networks.

Nonnative plants reduce population growth of an insectivorous bird.

Human-dominated landscapes represent one of the most rapidly expanding and least-understood ecosystems on earth. Yet, we know little about which features in these landscapes promote sustainable wildlife populations. Historically, in urban areas, landowners have converted native plant communities into habitats dominated by nonnative species that are not susceptible to pest damage and require little maintenance. However, nonnative plants are also poor at supporting insects that are critical food resources for higher order consumers. Despite the logical connection, no study has examined the impact of nonnative plants on subsequent population responses of vertebrate consumers. Here, we demonstrate that residential yards dominated by nonnative plants have lower arthropod abundance, forcing resident Carolina chickadees (Poecile carolinensis) to switch diets to less preferred prey and produce fewer young, or forgo reproduction in nonnative sites altogether. This leads to lower reproductive success and unsustainable population growth in these yards compared with those with >70% native plant biomass. Our results reveal that properties landscaped with nonnative plants function as population sinks for insectivorous birds. To promote sustainable food webs, urban planners and private landowners should prioritize native plant species.

Extreme physiological plasticity in a hibernating basoendothermic mammal, Tenrec ecaudatus.

Physiological plasticity allows organisms to respond to diverse conditions. However, can being too plastic actually be detrimental? Malagasy common tenrecs, Tenrec ecaudatus, have many plesiomorphic traits and may represent a basal placental mammal. We established a laboratory population of T. ecaudatus and found extreme plasticity in thermoregulation and metabolism, a novel hibernation form, variable annual timing, and remarkable growth and reproductive biology. For instance, tenrec body temperature (Tb) may approximate ambient temperature to as low as 12°C even when tenrecs are fully active. Conversely, tenrecs can hibernate with Tb of 28°C. During the active season, oxygen consumption may vary 25-fold with little or no change in Tb During the austral winter, tenrecs are consistently torpid but the depth of torpor may vary. A righting assay revealed that Tb contributes to but does not dictate activity status. Homeostatic processes are not always linked, e.g. a hibernating tenrec experienced a ∼34% decrease in heart rate while maintaining constant body temperature and oxygen consumption rates. Tenrec growth rates vary but young may grow ∼40-fold in the 5 weeks until weaning and may possess indeterminate growth as adults. Despite all of this profound plasticity, tenrecs are surprisingly intolerant of extremes in ambient temperature (<8 or >34°C). We contend that while plasticity may confer numerous energetic advantages in consistently moderate environments, environmental extremes may have limited the success and distribution of plastic basal mammals.

EVALUATION OF HUSBANDRY AND MORTALITY IN LESSER HEDGEHOG TENRECS (ECHINOPS TELFAIRI).

Causes of morbidity and mortality for various species of tenrecs have not been widely published, aside from several reports of neoplasia, and these data are crucial for advancing objectives for preventive medicine, diagnosis, and treatment. A survey on husbandry, morbidity, and mortality of lesser hedgehog tenrecs ( Echinops telfairi ) in Association of Zoos and Aquariums (AZA) institutions was conducted. Out of 32 institutions, 20 responded with data for 98 living and 93 dead animals. The most common causes of mortality among the dead animals were neoplasia (24%), hepatic lipidosis (11%), septicemia (8.6%), pneumonia (8.6%), cardiomyopathy (7.5%), renal disease (6.5%), osteomyelitis (3.2%), and trauma (3.2%). There was no statistically significant correlation between sex and neoplasia. Data about educational usage were specifically provided by survey respondents for 50 of the tenrecs, with only 42% being excluded from educational programming. Tenrecs are common to many AZA institutions as both educational and exhibit animals, and this study provides a helpful reference for expected health problems and highlights the need for future investments into medical diagnosis and treatment for these animals.

OBSTETRICAL AND POSTPARTUM COMPLICATIONS IN LESSER MADAGASCAR HEDGEHOG TENRECS (ECHINOPS TELFAIRI): FOUR CASES.

Currently, little is known about diseases and health concerns in tenrecs, family Tenrecidae. During the past 10 yr of breeding lesser Madagascar hedgehog tenrecs ( Echinops telfairi ) at a single zoological institution, a diverse range of obstetric and postpartum complications have been observed: pyometra, metritis, retained fetal membranes, retained fetus, perinatal mortality, and maternal neglect with subsequent successful hand-rearing of neonates. Treatment of these problems is complicated in tenrecs because of their small size and secretive behavior. Some of the cases reported in this article had successful resolution by ovariohysterectomy or cesarean section. The four cases described in this report overall help to disseminate options and outcomes for the diagnosis, treatment, and management of obstetric and postpartum complications in this small, secretive, nondomestic species.

Influence of feeding habits in the endocrine pancreas of insectivore bat Pteronotus personatus and nectarivore bat Anoura geoffroyi: A comparative stereological and immunohistochemical study.

Pteronotus personatus as an insectivore bat and has a diet that consists of a high protein diet, whereas the diet of Anoura geoffroyi, a predominantly nectarivore bat, is rich in simple sugars like sucrose, glucose and fructose. Considering that diet influences the activation of different pathways, which may influence morphological adaptations in the gastrointestinal system, the aim of this study was to compare the morphology of the endocrine pancreas in P. personatus and A. geoffroyi. For this, histological, stereological and immunohistochemical methods were used. In P. personatus, the average diameter of the pancreatic islet was 40.47µm±13.94, while in A. geoffroyi was 88.16µm±36.40. The total number of pancreatic islets in P. personatus was 26150±2346 and in A. geoffroyi was 15970±1666. In P. personatus, the volume density of the pancreatic islets was 3.4%± 2.6, whereas in A. geoffroyi the volume density was 6.1%±3.7. In addition, the immunodensity of the α, ß and δ cells, in P. personatus was 25.8%±11.9, 35.5%±13.5, 3.9%±0.7, respectively, and in A. geoffroyi was 33.10%±12.7, 55.08%±7.4, 6.2%±4.6, respectively. In conclusion, the results of this study indicate differences in the pancreatic weight/body, weight ratio, diameter and volume density of pancreatic islets and in immunodensity of the ß and α cells between both species, which have different dietary habits.

[Spatio-ethological aspects of interactions between small mammals and wood ants].

Mechanisms of interactions between species present one of the central problems of contemporary behavioral and evolutionary ecology. Field observations of possible resource redistribution and mutual behavioral adaptations between representatives of different guilds with substantially overlapping niche parameters are, so far, few. Using the methods of small mammals censuring, with account for their mobility and burrowing activity, at the sites with high and low dynamical density of wood ants Formica aquilonia, as well as in anthills proper, spatial interactions between these animals are revealed for the first time which are based on seasonal transformations of topic competition and synoecism. Species composition and domination structure of small mammals communities appear to be similar in those territories controlled by F. aquilonia and almost free of them. However, judging by animals' spatial distribution and activity it can be suggested that wood ants, being a disturbing factor, markedly reduce the numbers and burrowing activity of small mammals in their territory and, apparently, hinder mammals dispersion. During seasonal resting of ants, when they move down into the soil, anthills attract a lot of small animals: from October to May up to 84% ant nests are burrowed by murine rodents and insectivore mammals. It seems to be possible that there are trophic relationships between small mammals and wood ants, with mammals consuming nest substrate as well as insects themselves.

Disproportionate Declines in Ground-Foraging Insectivorous Birds after Mistletoe Removal.

Insectivorous birds have been recognized as disproportionately sensitive to land-use intensification and habitat loss, with those species feeding primarily on the ground exhibiting some of the most dramatic declines. Altered litter inputs and availability of epigeic arthropods have been suggested to underlie reduced abundances and shrinking distributions but direct evidence is lacking. I used a patch-scale removal experiment in southern Australia to evaluate whether ground-feeding insectivores are especially vulnerable to altered litter-fall. Building on work demonstrating the importance of mistletoe litter to nutrient dynamics, litter was reduced by removing mistletoe (Loranthaceae) from one set of eucalypt woodlands, responses of birds three years after mistletoe removal compared with otherwise similar control woodlands containing mistletoe. Despite not feeding on mistletoes directly, insectivores exhibited the greatest response to mistletoe removal. Among woodland residents, ground-foraging insectivores showed the most dramatic response; treatment woodlands losing an average of 37.4% of their pre-treatment species richness. Once these 19 species of ground-foraging insectivores were excluded, remaining woodland species showed no significant effect of mistletoe removal. This response reflects greater initial losses in treatment woodlands during the study (which coincided with a severe drought) and double the number of species returning to control woodlands (where mistletoe numbers and litter were not manipulated) post-drought. These findings support the productivity-based explanation of declining insectivores, suggesting diminished litter-fall reduced habitat quality for these birds via decreased availability of their preferred prey. In addition to altered prey availability, interactions between litter-fall and epigeic arthropods exemplify the importance of below-ground / above-ground linkages driving ecosystem function.

Social organization in Eulipotyphla: evidence for a social shrew.

Shrews and their close relatives (order Eulipotyphla) are typically considered to be solitary. This impacts our understanding of mammalian social evolution: (i) the ancestor of mammals is believed to have been shrew-like, and even though Eulipotyphla are not more basal than other mammalian orders, this might have been one reason why the first mammals have been assumed to be solitary-living; (ii) Eulipotyphla are the third largest mammalian order, with hundreds of species entering comparative analyses. We review primary field studies reporting the social organization of Eulipotyphla, doing a literature research on 445 species. Primary literature was only available for 16 of the 445 species. We found 56% of the studied species to be social (38% were living in pairs), which is in sharp contrast to the 0.5 and 8% reported in other databases. We conclude that the available information indicates that shrews are more sociable than generally believed. An interesting alternative hypothesis is that the mammalian ancestor might have been pair-living. To understand the social evolution of mammals, comparative studies must be based on reliable and specific information, and more species of all orders must be studied in the field.

Molecular evolution of the hyaluronan synthase 2 gene in mammals: implications for adaptations to the subterranean niche and cancer resistance.

The naked mole-rat (NMR) Heterocephalus glaber is a unique and fascinating mammal exhibiting many unusual adaptations to a subterranean lifestyle. The recent discovery of their resistance to cancer and exceptional longevity has opened up new and important avenues of research. Part of this resistance to cancer has been attributed to the fact that NMRs produce a modified form of hyaluronan--a key constituent of the extracellular matrix--that is thought to confer increased elasticity of the skin as an adaptation for living in narrow tunnels. This so-called high molecular mass hyaluronan (HMM-HA) stems from two apparently unique substitutions in the hyaluronan synthase 2 enzyme (HAS2). To test whether other subterranean mammals with similar selection pressures also show molecular adaptation in their HAS2 gene, we sequenced the HAS2 gene for 11 subterranean mammals and closely related species, and combined these with data from 57 other mammals. Comparative screening revealed that one of the two putatively important HAS2 substitutions in the NMR predicted to have a significant effect on hyaluronan synthase function was uniquely shared by all African mole-rats. Interestingly, we also identified multiple other amino acid substitutions in key domains of the HAS2 molecule, although the biological consequences of these for hyaluronan synthesis remain to be determined. Despite these results, we found evidence of strong purifying selection acting on the HAS2 gene across all mammals, and the NMR remains unique in its particular HAS2 sequence. Our results indicate that more work is needed to determine whether the apparent cancer resistance seen in NMR is shared by other members of the African mole-rat clade.

Mammal survival at the Cretaceous-Palaeogene boundary: metabolic homeostasis in prolonged tropical hibernation in tenrecs.

Free-ranging common tenrecs, Tenrec ecaudatus, from sub-tropical Madagascar, displayed long-term (nine months) hibernation which lacked any evidence of periodic interbout arousals (IBAs). IBAs are the dominant feature of the mammalian hibernation phenotype and are thought to periodically restore long-term ischaemia damage and/or metabolic imbalances (depletions and accumulations). However, the lack of IBAs in tenrecs suggests no such pathology at hibernation Tbs > 22°C. The long period of tropical hibernation that we report might explain how the ancestral placental mammal survived the global devastation that drove the dinosaurs and many other vertebrates to extinction at the Cretaceous-Palaeogene boundary following a meteorite impact. The genetics and biochemistry of IBAs are of immense interest to biomedical researchers and space exploration scientists, in the latter case, those envisioning a hibernating state in astronauts for deep space travel. Unravelling the physiological thresholds and temperature dependence of IBAs will provide new impetus to these research quests.

Are tropical small mammals physiologically vulnerable to Arrhenius effects and climate change?

There is some urgency in the necessity to incorporate physiological data into mechanistic, trait-based, demographic climate change models. Physiological responses at the individual level provide the mechanistic link between environmental changes and individual performances and hence population dynamics. Here we consider the causal relationship between ambient temperature (Ta) and metabolic rate (MR), namely, the Arrhenius effect, which is directly affected by global warming through increases in average global air temperatures and the increase in the frequency and intensity of extreme climate events. We measured and collated data for several small, free-ranging tropical arboreal mammals and evaluated their vulnerability to Arrhenius effects and putative heat stress associated with climate change. Skin temperatures (Tskin) were obtained from free-ranging tarsiers (Tarsius syrichta) on Bohol Island, Philippines. Core body temperature (Tb) was obtained from the greater hedgehog tenrec (Setifer setosus) and the gray brown mouse lemur (Microcebus ravelobensis) from Ankarafantsika, Madagascar. Tskin for another mouse lemur, Microcebus griseorufus, was obtained from the literature. All four species showed evidence of hyperthermia during the daytime rest phase in the form of either Tskin or Tb that was higher than the normothermic Tb during the nighttime active phase. Potentially, tropical arboreal mammals with the lowest MRs and Tb, such as tarsiers, are the most vulnerable to sustained heat stress because their Tb is already close to Ta. Climate change may involve increases in MRs due to Arrhenius effects, especially during the rest phase or during torpor and hibernation. The most likely outcome of increased Arrhenius effects with climate change will be an increase in energy expenditure at the expense of other critical functions such as reproduction or growth and will thus affect fitness. However, we propose that these hypothetical Arrhenius costs can be, and in some species probably are, offset by the use of hyperthermic daily torpor, that is, hypometabolism at high Ta.

Brown fat in a protoendothermic mammal fuels eutherian evolution.

Endothermy has facilitated mammalian species radiation, but the sequence of events leading to sustained thermogenesis is debated in multiple evolutionary models. Here we study the Lesser hedgehog tenrec (Echinops telfairi), a phylogenetically ancient, 'protoendothermic' eutherian mammal, in which constantly high body temperatures are reported only during reproduction. Evidence for nonshivering thermogenesis is found in vivo during periodic ectothermic-endothermic transitions. Anatomical studies reveal large brown fat-like structures in the proximity of the reproductive organs, suggesting physiological significance for parental care. Biochemical analysis demonstrates high mitochondrial proton leak catalysed by an uncoupling protein 1 ortholog. Strikingly, bioenergetic profiling of tenrec uncoupling protein 1 reveals similar thermogenic potency as modern mouse uncoupling protein 1, despite the large phylogenetic distance. The discovery of functional brown adipose tissue in this 'protoendothermic' mammal links nonshivering thermogenesis directly to the roots of eutherian evolution, suggesting physiological importance prior to sustained body temperatures and migration to the cold.

Brain volume of the newly-discovered species Rhynchocyon udzungwensis (Mammalia: Afrotheria: Macroscelidea): implications for encephalization in sengis.

The Gray-faced Sengi (Rhynchocyon udzungwensis) is a newly-discovered species of sengi (elephant-shrew) and is the largest known extant representative of the order Macroscelidea. The discovery of R. udzungwensis provides an opportunity to investigate the scaling relationship between brain size and body size within Macroscelidea, and to compare this allometry among insectivorous species of Afrotheria and other eutherian insectivores. We performed a spin-echo magnetic resonance imaging (MRI) scan on a preserved adult specimen of R. udzungwensis using a 7-Tesla high-field MR imaging system. The brain was manually segmented and its volume was compiled into a dataset containing previously-published allometric data on 56 other species of insectivore-grade mammals including representatives of Afrotheria, Soricomorpha and Erinaceomorpha. Results of log-linear regression indicate that R. udzungwensis exhibits a brain size that is consistent with the allometric trend described by other members of its order. Inter-specific comparisons indicate that macroscelideans as a group have relatively large brains when compared with similarly-sized terrestrial mammals that also share a similar diet. This high degree of encephalization within sengis remains robust whether sengis are compared with closely-related insectivorous afrotheres, or with more-distantly-related insectivorous laurasiatheres.