Evolution and drivers of long-distance vocal communication in mammals

Aquatic and semi-aquatic mammals, while resting at the water surface or ashore, breathe with a low frequency (f) by comparison to terrestrial mammals of the same body size, the difference increasing the larger the species. Among various interpretations, it was suggested that the low-f breathing is a consequence of the end-inspiratory breath-holding pattern adopted by aquatic mammals to favour buoyancy at the water surface, and evolved to be part of the genetic makeup. If this interpretation was correct it could be expected that, differently from f, the heart rate (HR, beats/min) of aquatic and semi-aquatic mammals at rest would not need to differ from that of terrestrial mammals and that their HR-f ratio would be higher than in terrestrial species. Literature data for HR (beats/min) in mammals at rest were gathered for 56 terrestrial and 27 aquatic species. In aquatic mammals the allometric curve (HR=191·M-0.18; M= body mass, kg) did not differ from that of terrestrial species (HR=212·M-0.22) and their HR-f ratio (on average 32±5) was much higher than in terrestrial species (5±1) (P<0.0001). The comparison of these HR allometric curves to those for f previously published indicated that the HR-f ratio was body size-independent in terrestrial species while it increased significantly with M in aquatic species. The similarity in HR and differences in f between aquatic and terrestrial mammals agree with the possibility that the low f of aquatic and semi-aquatic mammals may have evolved for a non-respiratory function, namely the regulation of buoyancy at the water surface.

We tested the prediction that home range area and dispersal distance in mammals are related when considered independently of body size. Regression of log- transformed data demonstrated that more variance in maximum dispersal distance could be explained by home range area (74%) than could be explained by body size (50%). The relationship between maximum dispersal distance and home range size was isometric (slope 5 1) when the square root of home range area (i.e., linear dimension of home range) was used. Thus, maximum dispersal distance was related to home range size by a single constant of 40. A linear relationship remained between these two variables after the effects of body size were removed (F 5 31.6, df 5 1, 32, P 5 3.2 3 10 26 , R 2 5 0.50). A similar isometric relationship with home range size was found for median dispersal distance (related by a multiple of 7). This isometric relationship between dispersal distance and home range size was tested using a second data source: maximum movements made by mammals after translocation, which also was linearly related to home range area (F 5 94.5, df 5 1, 23, P 5 1.3 3 10 29 , R 2 5 0.81). The slope and intercept of this relationship were not different from those of the relationship between maximum dispersal distance and home range area. We suggest that the vagility of mammals affected both home range size and dispersal distance (or movement after translocation) independently of body size, such that these movements could be predicted by home range area better than by body size alone. The resulting isometric relationship between dispersal distance and home range size has potential as a useful scaling rule for ecological practitioners.

While basal metabolic rate (BMR) scales proportionally with body mass (Mb ), it remains unclear whether the relationship differs between mammals from aquatic and terrestrial habitats. We hypothesized that differences in BMR allometry would be reflected in similar differences in scaling of O2 delivery pathways through the cardiorespiratory system. We performed a comparative analysis of BMR across 63 mammalian species (20 aquatic, 43 terrestrial) with a Mb range from 10 kg to 5318 kg. Our results revealed elevated BMRs in small (>10 kg and <100 kg) aquatic mammals compared to small terrestrial mammals. The results demonstrated that minute ventilation, that is, tidal volume (VT )·breathing frequency (fR ), as well as cardiac output, that is, stroke volume·heart rate, do not differ between the two habitats. We found that the "aquatic breathing strategy", characterized by higher VT and lower fR resulting in a more effective gas exchange, and by elevated blood hemoglobin concentrations resulting in a higher volume of O2 for the same volume of blood, supported elevated metabolic requirements in aquatic mammals. The results from this study provide a possible explanation of how differences in gas exchange may serve energy demands in aquatic versus terrestrial mammals.

Sleep has been studied widely in mammals and to some extent in other vertebrates. Higher vertebrates such as birds and mammals have evolved an inimitable rapid eye movement (REM) sleep state. During REM sleep, postural muscles become atonic and the temperature regulating machinery remains suspended. Although REM sleep is present in almost all the terrestrial mammals, the aquatic mammals have either radically reduced or completely eliminated REM sleep. Further, we found a significant negative correlation between REM sleep and the adaptation of the organism to live on land or in water. The amount of REM sleep is highest in terrestrial mammals, significantly reduced in semi-aquatic mammals and completely absent or negligible in aquatic mammals. The aquatic mammals are obligate swimmers and have to surface at regular intervals for air. Also, these animals live in thermally challenging environments, where the conductive heat loss is approximately ~90 times greater than air. Therefore, they have to be moving most of the time. As an adaptation, they have evolved unihemispheric sleep, during which they can rove as well as rest. A condition that immobilizes muscle activity and suspends the thermoregulatory machinery, as happens during REM sleep, is not suitable for these animals. It is possible that, in accord with Darwin's theory, aquatic mammals might have abolished REM sleep with time. In this review, we discuss the possibility of the intrinsic role of aquatic conditions in the elimination of REM sleep in the aquatic mammals.

During evolution, animals have returned from land to water, adapting with morphological modifications to life in an aquatic environment. We compared the osteochondral units of the humeral head of marine and terrestrial mammals across species spanning a wide range of body weights, focusing on microstructural organization and biomechanical performance. Aquatic mammals feature cartilage with essentially random collagen fiber configuration, lacking the depth-dependent, arcade-like organization characteristic of terrestrial mammalian species. They have a less stiff articular cartilage at equilibrium with a significantly lower peak modulus, and at the osteochondral interface do not have a calcified cartilage layer, displaying only a thin, highly porous subchondral bone plate. This totally different constitution of the osteochondral unit in aquatic mammals reflects that accommodation of loading is the primordial function of the osteochondral unit. Recognizing the crucial importance of the microarchitecture-function relationship is pivotal for understanding articular biology and, hence, for the development of durable functional regenerative approaches for treatment of joint damage, which are thus far lacking.

Movement and home range of owned free-roaming male dogs in Puerto Natales, Chile

We measured the BASAL breathing frequency following an overnight fast in adult, non‐pregnant/non‐lactating, inactive mammals ranging in body mass from 15 to 5520 kg. The data included results from 338 individual animals from 34 species that were divided into terrestrial, semi‐aquatic (Otariidae and Phocidae) and aquatic mammals. Following attempts to limit the collection of breathing frequency using a basal definition and to correct the analysis phylogenetically, our results suggest that there are differences in the allometric mass‐exponent between terrestrial and aquatic/semi‐aquatic mammals. An allometric regression model, whereby both body mass and breathing frequency were transformed using log10, suggested that the allometric mass exponent for terrestrial mammals (−0.303) was different from both aquatic mammals (−0.124) and semi‐aquatic mammals (−0.091). For semi‐aquatic mammals, the breathing frequency was lower in water, but we detected no association between the breathing frequency and the temperature of the medium (water or air). We propose that allometric studies of cardiorespiratory function should, if possible, adhere to the basal definition during data collection, similar to that used for metabolic rate. Such data will provide valuable information for comparative medicine of large species that are difficult to study, for which controlled baseline data might be difficult to obtain.

Studying the factors determining the sizes of home ranges, based on body mass, feeding style, and sociality level, is a long-standing goal at the intersection of ecology and evolution. Yet, how species-specific life history traits interact with different components of the landscape to shape differences in individual home ranges at within-population level has received much less attention. Here, we review the empirical literature on ungulates to map our knowledge of the relative effects of the key environmental drivers (resource availability, landscape heterogeneity, lethal and non-lethal risks) on the sizes of individual home ranges within a population and assess whether species' characteristics (body mass, diet, and social structure), account for observed variation in the responses of the sizes of individual home ranges to local environmental drivers. Estimating the sizes of home ranges and measuring environmental variables raise a number of methodological issues, which complicate the comparison of empirical studies. Still, from an ecological point of view, we showed that (1) a majority of papers (75%) supported the habitat productivity hypothesis, (2) the support for the influence of landscape heterogeneity was less pervasive across studies, (3) the response of cattle-type to variation in food availability was stronger than the response of moose-type, and (4) species-specific body mass or sociality level had no detectable effect on the level of support to the biological hypotheses. To our surprise, our systematic review revealed a dearth of studies focusing on the ecological drivers of the variation in the sizes of individual home ranges (only about 1% of articles that dealt with home ranges), especially in the later decade where more focus has been devoted to movement. We encourage researchers to continue providing such results with sufficient sample sizes and robust methodologies, as we still need to fully understand the link between environmental drivers and individual space use while accounting for life-history constraints.

To develop industry-specific policies for mitigating environmental pressures, previous studies primarily focus on identifying sectors that directly generate large amounts of environmental pressures (a.k.a. production-based method) or indirectly drive large amounts of environmental pressures through supply chains (e.g., consumption-based method). In addition to those sectors as important environmental pressure producers or drivers, there exist sectors that are also important to environmental pressure mitigation as transmission centers. Economy-wide environmental pressure mitigation might be achieved by improving production efficiency of these key transmission sectors, that is, using less upstream inputs to produce unitary output. We develop a betweenness-based method to measure the importance of transmission sectors, borrowing the betweenness concept from network analysis. We quantify the betweenness of sectors by examining supply chain paths extracted from structural path analysis that pass through a particular sector. We take China as an example and find that those critical transmission sectors identified by betweenness-based method are not always identifiable by existing methods. This indicates that betweenness-based method can provide additional insights that cannot be obtained with existing methods on the roles individual sectors play in generating economy-wide environmental pressures. Betweenness-based method proposed here can therefore complement existing methods for guiding sector-level environmental pressure mitigation strategies.

The home range of the Florida red-bellied turtle, Pseudemys nelsoni, in a Florida spring run is described using both maximum distance over water and Ford and Krumme's (1979) technique for producing a home range. Ford and Krumme's (1979) technique was also used to find the probabilities of capture/ relocation within the composite home range. Spatial positions in the river were based on underwater captures/relocations and basking relocations. The results from both methods suggest that individuals at this study site use a small home range, on the order of 120 m in length, with no sex differences. These results are constrasted with those for P. floridana at the same site and with telemetrygenerated data for P. nelsoni in a shallow lake in Paynes Prairie, Florida. Sympatric P.floridana appear to have larger home ranges, with a patchier distribution of nonzero capture/relocation probabilities. Estimates of the home-range areas of P. nelsoni in the lake are an order of magnitude larger than those in the run, perhaps due to more dispersed resources or the use of telemetry for relocating animals.

Tracking small-bodied animals in estuarine environments entails significant technological and analytical challenges. Diamond-backed terrapins are small (max 1.4kg) turtles that inhabit salt marshes of the eastern U.S. and the Gulf of Mexico. Terrapin movements have been studied with VHF radio telemetry, acoustic telemetry, and mark and recapture methods, which have indicated maximum straight-line movement distances < 10km and mean home ranges < 1 km2. We deployed 21 Argos satellite tags on adult female terrapins at two sites on Long Island, New York to better understand the spatial ecology of this imperiled species, and to test newly available tracking technology. We processed the location data three ways: (1) we used a location data filter to remove unlikely terrestrial and oceanic locations and applied a state-space model to account for Argos location errors, (2) we applied the state-space model to unfiltered data to determine the effects of not removing unlikely locations, and (3) we used only the highest quality location class 3 (LC 3) locations. We used the data resulting from each of these approaches to calculate four different movement metrics: summer home range size (95% minimum convex polygons (MCPs) and kernel density estimates (50% and 95% KDE, with both reference [href] and least squares cross validation [LSCV] bandwidths)), the total distance traveled from June to August, maximum distance traveled in one day, and daily movement rates. Home ranges estimated from the three processing techniques were similar in size and covered the same spatial areas. Estimates for total distance traveled, daily movement rates, and maximum distance traveled were similar between the state-space modeling techniques, but LC 3 estimated distances were twice as long. Movement metrics and home ranges were similar between the two study sites, despite differences in urbanization and bay size. These results suggest that most movement metrics and home range estimates are fairly insensitive to these different analytical techniques, even at relatively smaller spatial scales. Additionally, our study indicates substantially larger home ranges and longer straight-line movements than VHF telemetry or sonic tag studies, highlighting the utility of satellite tags to improve our understanding of terrapin ecology and conservation.

The aim of the study was to identify the habitat preferences and home range of resident and relocated brown hares during the nohunting period. The trial was carried out in a protected area and in a free-hunting territory (FHT), both located in the Florence province. During the captures, 21 hares were equipped with a necklace radio-tag: seven hares (resident group) were released in the same area of capture and 14 hares (relocated group) were relocated in six different locations within the FHT. The effect of the place of release was analysed by ANOVA and/or nonparametric methods. Results showed that the home ranges of the resident group were characterized by a greater amount of fallow land and shrub land than of the relocated group (P<0.05). Home range sizes and maximum distances from the releasing sites were greater in the relocated group. Resident hares preferred landscape characterized by a higher density of patches (152 vs. 70 n/100 ha), patch richness (43 vs. 12 n/100 ha), and patch area (4703 vs. 8142 m2) than the relocated hares (P<0.01). The landscape structure indices, the home range sizes and the maximum distance from the releasing sites suggest that the relocated hares, even if released in suitable habitats, will move from their releasing point to look for better habitats. The landscape with the most complexity is preferred by the resident hares. This result should be considered when a project is programmed to reintroduce this lagomorph into a territory, or when it is necessary to improve the dynamics of a natural population.

Territoriality and stable home ranges are a common space-use pattern among animals. These ranges provide its inhabitants with important resources and thus favourable territories are associated with an increased fitness. While the role of territory quality and changes of territory ownership have often been investigated, the changes of territorial boundaries have been less studied. Here, we investigated space-use changes in a social mammal species, applying a novel analytical approach, calculating long-term dissimilarity in space use using distancematrices based on periodic utilization distributions. This approach makes it possible to identify different space-use patterns, which cannot be distinguished by only considering changes between consecutive time periods. We analysed meerkat (Suricata suricatta) movements of a total of 24 different groups over a 16-year period, resulting in 134 group years. We then correlated the identified home-range changes to life-history events and possible environmental drivers. Groups had stable territories for several years before they abandoned their home range mostly to move quickly to new areas where they again remained for several years. Of 26 identified sudden shifts, 22 occurred in the summer months and often involved distances larger than the original home-range size. Home-range movements that were close together in time were often also spatially clustered and moved in a similar direction. These shifts were often preceded by more frequent interactions between groups, but did not seem to be a product of direct displacements by other groups. The normalized difference vegetation index as a measure of food production and social factors such as dominance changes did not correlate to changes. Against our expectation space-use changes were not accumulations of small changes, but more often involved long-distance moves into unknown ranges. This means that the groups enter areas where they cannot profit from local knowledge. The methods used identify episodes of long stability alternated by sudden changes in meerkats and in general provides insight into long-term space use. Our methods can be used to analyse long-term space use, either within or across species.

Animal dispersion in space and time results from environmental pressures, and affects the outcome of a species’ social organization. When females are solitary, males may either roam or be pair‐living. We studied possible environmental influences affecting the social organization of the round‐eared sengi (Macroscelides proboscideus) in a semi‐desert in South Africa, using trapping and radio‐tracking across 2.5 yr. Adult sex ratios did not deviate from 1:1 and we found no indication of sexual dimorphism in body mass. Females maintained exclusive areas, which had little overlap (&lt;4%) with neighbouring females (NF), and males overlapped predominately only with the home range of single females. Generally, inter‐ and intra‐sexual overlap with neighbouring individuals was low (3–6%) for both sexes, indicating territoriality and pair‐living. Pairs were perennial and territories were maintained year‐round. However, males generally maintained much larger areas than females, which were sensitive to population density. Male space use appeared to be primarily limited by the presence of neighbouring males. Female home ranges were smaller‐sized despite changes in population density, possibly for energetic efficiency. Some paired males attempted to take over widowed females, but shifted back to their original home range following the intrusion of an un‐paired male. We conclude that social monogamy is the predominant social organization in round‐eared sengis in a semi‐desert that may have resulted from females living solitarily in small exclusive territories, balanced sex ratios, and from a low variation of body mass between males.

Cetaceans and pinnipeds are lineages of mammals that have independently returned to the aquatic environment, acquiring varying degrees of dependence on it while sharing adaptations for underwater living. Here, we focused on one critical adaptation from both groups, their ability to withstand the ischemia and reperfusion experienced during apnea diving, which can lead to the production of reactive oxygen species (ROS) and subsequent oxidative damage. Previous studies have shown that cetaceans and pinnipeds possess efficient antioxidant enzymes that protect against ROS. In this study, we investigated the molecular evolution of key antioxidant enzyme genes (CAT, GPX3, GSR, PRDX1, PRDX3, and SOD1) and the ROS-producing gene XDH, in cetaceans and pinnipeds lineages. We used the ratio of non-synonymous (dN) to synonymous (dS) substitutions as a measure to identify signatures of adaptive molecular evolution in these genes within and between the two lineages. Additionally, we performed protein modeling and variant impact analyzes to assess the functional consequences of observed mutations. Our findings revealed distinct selective regimes between aquatic and terrestrial mammals in five of the examined genes, including divergences within cetacean and pinniped lineages, between ancestral and recent lineages and between crowns groups. We identified specific sites under positive selection unique to Cetacea and Pinnipedia, with one site showing evidence of convergent evolution in species known for their long and deep-diving capacities. Notably, many sites under adaptive selection exhibited radical changes in amino acid properties, with some being damaging mutations in human variations, but with no apparent detrimental impacts on aquatic mammals. In conclusion, our study provides insights into the adaptive changes that have occurred in the antioxidant systems of aquatic mammals throughout their evolutionary history. We observed both distinctive features within each group of Cetacea and Pinnipedia and instances of convergence. These findings highlight the dynamic nature of the antioxidant system in response to challenges of the aquatic environment and provide a foundation for further investigations into the molecular mechanisms underlying these adaptations.