Open Access

Mammals harbor trillions of microorganisms and understanding the ecological and evolutionary processes structuring these ecosystems may provide insights relevant to public health and medicine. Comparative studies with our closest living relatives, non-human primates, have provided first insights into their rich bacteriophage communities. Here, I discuss how this phage diversity can be useful for combatting antibiotic-resistant infections and understanding disease emergence risk. For example, some primate-associated phages show a pattern suggesting a long-term co-divergence with their primate superhosts—co-diverging phages may be more likely to exhibit a narrow host range and thus less useful for phage therapy. Captive primates lose their natural phageome, which is replaced by human-associated phages making phages an exciting tool for studying rates of microorganism transmission at human–wildlife interfaces. This commentary tackles avenues for selecting phages for therapeutic interventions based on their ecological and evolutionary history, while discussing frameworks to allow primate-associated phages to be incorporated into the arsenal of clinicians.

Targeted metabolomics has been widely used in pheromone research but may miss pheromone components in study organisms that produce pheromones in trace amount and/or lack bio-detectors (e.g., antennae) to readily locate them in complex samples. Here, we used non-targeted metabolomics—together with high-performance liquid chromatography–mass spectrometry (HPLC–MS), gas chromatography-MS, and behavioral bioassays—to unravel the sex pheromone of the triangulate cobweb spider, Steatoda triangulosa. A ternary blend of three contact pheromone components [N-4-methylvaleroyl-O-isobutyroyl-l-serine (5), N-3-methylbutyryl-O-isobutyroyl-l-serine (11), and N-3-methylbutyryl-O-butyroyl-l-serine (12)] elicited courtship by S. triangulosa males as effectively as female web extract. Hydrolysis of 5, 11 and 12 at the ester bond gave rise to two mate-attractant pheromone components [butyric acid (7) and isobutyric acid (8)] which attracted S. triangulosa males as effectively as female webs. Pheromone components 11 and 12 are reported in spiders for the first time, and were discovered only through the use of non-targeted metabolomics and GC–MS. All compounds resemble pheromone components previously identified in widow spiders. Our study provides impetus to apply non-targeted metabolomics for pheromone research in a wide range of animal taxa.

Adaptations, either structural, physiological, or behavioural are essential for the survival of species or individuals in changing environments. For animals that live in two distinct environments, adaptations only persist if they provide advantages in one or both media, and if the adaptations do not negatively interfere with other substantial life functions in any of the media. The ability to flexibly respond to rapid environmental changes within such adapted forms potentially provides safeguards, limiting adverse effects of any impact. This also applies to the sensory modalities of amphibious living vertebrates (e.g., seals (Pinnipedia), crocodilians (Crocodilia), penguins (Sphenisciformes)). They are evolutionarily very well adapted to the aquatic element for foraging but have also kept adaptations that enable them to live on land, where they perform major life history tasks like breeding. It is therefore likely that the hearing and vocal systems are also strongly impacted by living in water and air, as they have different acoustic properties. However, to date, the auditory perception and vocal flexibility of penguins have remained largely unexplored in both media. To address some gaps in our knowledge, this thesis focusses on three questions concerning the ability of penguins to hear in air and their vocal flexibility during the breeding season: 1) can penguins in the wild adjust vocal properties depending on the acoustic environment of their colony?; 2) can captive penguins be trained to perform hearing trials? and; 3) how well can penguins hear in air? Gentoo penguins (Pygoscelis papua) live in large social breeding groups that can include different species. Because of differences in the acoustic environment of such colonies, the vocal characteristics of Gentoo penguins may differ between colonies that include multiple species and those where only Gentoo penguins breed. To examine differences in vocalisations, the vocal parameters of ecstatic display calls (e.g., frequency, structure, duration) were compared between individual Gentoo penguins breeding in colonies with Adélie (Pygoscelis adeliae) or Chinstrap penguins (Pygoscelis antarcticus) and those breeding in monospecific colonies. Gentoo penguin calls showed a lower frequency and narrower energy distribution when they bred in proximity to Adélie penguins but their calls did not vary when they bred in proximity to Chinstrap penguins, whose vocalisations are more distinct. Even though the underlying mechanisms remain unknown, these results suggest that Gentoo penguins can adjust the parameters of their vocalisations according to the social (and presumably acoustic) environment of their colonies. To validate that these vocal adjustments result from the acoustic environment encountered by penguins in their colony, it is essential to know precisely what they can hear in air. The most sensitive method to examine the hearing capacity of animals is to train them for psychoacoustic measurements. Such training methods have, however, not yet been applied to penguins and there was considerable uncertainty whether the existing training methods (typically used for marine mammals and terrestrial birds) could be applied to penguins. Moreover, it was unknown how individual differences and environmental conditions could affect their trainability. In this thesis, I describe the successful training of four captive Humboldt penguins (Spheniscus humboldti) for psychoacoustic measurements over a 48-month period. Monitoring training progress revealed that their trainability depended on individuality, time of day, moult, pairing and daylength. Penguins have an ear morphology evolved for an aquatic lifestyle. How this morphological adaptation might influence their auditory capabilities in air was previously unknown. Using psychophysical hearing tests in the afore-mentioned Humboldt penguins, I found that their hearing range at 50 % hit rate was below 76 dB rms re 20 μPa between 0.250 kHz and 10 kHz, with the most sensitive hearing at 2 kHz (mean threshold of 15.3 dB rms re 20 μPa, SD = 10.6 dB, n = 4). After a surprisingly rapid decline of sensitivity in all animals at 0.500 kHz (mean ± SD = 64.1 dB rms re 20 μPa ± 9 dB, n = 4), three of the animals consistently detected the 0.250 kHz frequency stimulus again at comparably low sound levels (mean ± SD = 36.8 dB rms re 20μPa ± 2.4 dB, n = 3). Specific aquatic adaptations of penguins therefore do not appear to have strongly limited their hearing capacity in air compared to other aquatic birds. By combining my studies on two species, one in the wild and one in captivity, this thesis suggests that penguins may be able to adjust their vocal characteristics to the acoustic environment of their colony by adapting towards lower frequency vocalisations. This finding was supported by the unexpected sensitivity in the lower frequency range found here in the trained penguins. The range of acoustic flexibility required by each species for their ecological niche, could depend on morphological adaptations to a semi-aquatic lifestyle, and their phenotypic plasticity. This thesis provides hypotheses on the specific traits that could be involved, and that can now be further elucidated by targeted investigations.

Accurate population estimates are crucial to developing successful conservation policy, but the underlying data remain difficult to collect for many taxa. This is especially true for elusive species, such as temperate-zone bats, where visual counts in hibernacula underestimate their population to an unknown extent. Infrared light barriers that count all entering and exiting bats at the entrance of a hibernaculum could offer a more accurate alternative for bat population monitoring. We used infrared video recordings to quantify light barrier accuracy (i.e., concordance between light barrier and video registration of entries and exits) at five hibernacula over 30 weeks during autumn and spring. Subsequently, we developed a standardized methodology to estimate light barrier-based population sizes based on the number of emerging bats in spring, and compared these estimates to visual counts at 12 sites. Finally, we calculated confidence intervals around the estimated population sizes, and used these to evaluate population trends using 6-year-long light barrier datasets from four sites. Light barrier accuracy varied based on the model and precise location of the installation, with the best combination achieving near-perfect accuracy across the entire emergence phase. When compared to the resulting light barrier-based population estimates, winter hibernation counts markedly underestimated population totals, recovering less than 10% of the bats at the most complex sites. Moreover, light barrier-based population trends showed regional patterns of growth and decline, which were not evident in the visual counts. This study demonstrates that light barriers can estimate the population size and trends of bat assemblages with unprecedented accuracy, even at large, complex, or inaccessible hibernacula that cannot be precisely assessed with visual hibernation counts. Installing light barriers at a representative network of sites, where their installation does not require large-scale entrance modifications, has the potential to revolutionize bat monitoring and contribute to data-driven conservation.

Hibernation is a widespread adaptation in animals to seasonally changing environmental conditions. In the face of global anthropogenic change, information about plastic adjustments to environmental conditions and associated mortality costs are urgently needed to assess population persistence of hibernating species. Here, we used a five-year data set of 1047 RFID-tagged individuals from two bat species, Myotis nattereri and Myotis daubentonii that were automatically recorded each time they entered or left a hibernaculum. Because the two species differ in foraging strategy and activity pattern during winter, we expected species–specific responses in the timing of hibernation relative to environmental conditions, as well as different mortality costs of early departure from the hibernaculum in spring. Applying mixed-effects modelling, we disentangled population-level and individual-level plasticity in the timing of departure. To estimate mortality costs of early departure, we used both a capture mark recapture analysis and a novel approach that takes into account individual exposure times to mortality outside the hibernaculum. We found that the timing of departure varied between species as well as among and within individuals, and was plastically adjusted to large-scale weather conditions as measured by the NAO (North Atlantic Oscillation) index. Individuals of M. nattereri, which can exploit milder temperatures for foraging during winter, tuned departure more closely to the NAO index than individuals of M. daubentonii, which do not hunt during winter. Both analytical approaches used to estimate mortality costs showed that early departing individuals were less likely to survive until the subsequent hibernation period than individuals that departed later. Overall, our study demonstrates that individuals of long-lived hibernating bat species have the potential to plastically adjust to changing climatic conditions, although the potential for adjustment differs between species.