Amphibious Mammals Research Articles

In-air hearing in Hawaiian monk seals: implications for understanding the auditory biology of Monachinae seals

The auditory biology of Monachinae seals is poorly understood. Limited audiometric data and certain anatomical features suggest that these seals may have reduced sensitivity to airborne sounds compared to related species. Here, we describe the in-air hearing abilities of a Hawaiian monk seal (Neomonachus schauinslandi) trained to participate in a psychophysical paradigm. We report absolute (unmasked) thresholds for narrowband signals measured in quiet conditions across the range of hearing and masked thresholds measured in the presence of octave-band noise at two frequencies. The behavioral audiogram indicates a functional hearing range from 0.1 to 33 kHz and poor sensitivity, with detection thresholds above 40 dB re 20 µPa. Critical ratio measurements are elevated compared to those of other seals. The apparently reduced terrestrial hearing ability of this individual—considered with available auditory data for a northern elephant seal (Mirounga angustirostris)—suggests that hearing in Monachinae seals differs from that of the highly sensitive Phocinae seals. Exploration of phylogenetic relationships and anatomical traits support this claim. This work advances understanding of the evolution of hearing in amphibious marine mammals and provides updated information that can be used for management and conservation of endangered Hawaiian monk seals.

Adaptations for amphibious vision in sea otters (Enhydra lutris): structural and functional observations.

Sea otters (Enhydra lutris) are amphibious mammals that maintain equal in-air and underwater visual acuity. However, their lens-based underwater accommodative mechanism presumably requires a small pupil that may limit sensitivity across light levels. In this study, we consider adaptations for amphibious living by assessing the tapetum lucidum, retina, and pupil dynamics in sea otters. The sea otter tapetum lucidum resembles that of terrestrial carnivores in thickness and fundic coverage. A heavily rod-dominated retina appears qualitatively similar to the ferret and domestic cat, and a thick outer nuclear layer relative to a thinner inner nuclear layer is consistent with nocturnal vertebrates and other amphibious carnivores. Pupil size range in two living sea otters is smaller relative to other amphibious marine carnivores (pinnipeds) when accounting for test conditions. The pupillary light response seems slower than other aquatic and terrestrial species tested in comparable brightness, although direct comparisons require further assessment. Our results suggest that sea otters have retained features for low-light vision but rapid adjustments and acute underwater vision may be constrained across varying light levels by a combination of pupil shape, absolute eye size, and the presumed coupling between anterior lens curvature and pupil size during accommodation.

Convergent evolution of olfactory and thermoregulatory capacities in small amphibious mammals

Olfaction and thermoregulation are key functions for mammals. The former is critical to feeding, mating, and predator avoidance behaviors, while the latter is essential for homeothermy. Aquatic and amphibious mammals face olfactory and thermoregulatory challenges not generally encountered by terrestrial species. In mammals, the nasal cavity houses a bony system supporting soft tissues and sensory organs implicated in either olfactory or thermoregulatory functions. It is hypothesized that to cope with aquatic environments, amphibious mammals have expanded their thermoregulatory capacity at the expense of their olfactory system. We investigated the evolutionary history of this potential trade-off using a comparative dataset of three-dimensional (3D) CT scans of 189 skulls, capturing 17 independent transitions from a strictly terrestrial to an amphibious lifestyle across small mammals (Afrosoricida, Eulipotyphla, and Rodentia). We identified rapid and repeated loss of olfactory capacities synchronously associated with gains in thermoregulatory capacity in amphibious taxa sampled from across mammalian phylogenetic diversity. Evolutionary models further reveal that these convergences result from faster rates of turbinal bone evolution and release of selective constraints on the thermoregulatory-olfaction trade-off in amphibious species. Lastly, we demonstrated that traits related to vital functions evolved faster to the optimum compared to traits that are not related to vital functions.

Back to the Beach: Adaptations that Enabled Terrestrial Mammals to Return to the Water

Modern aquatic mammals are extremely diverse. This includes classic marine mammals such as cetaceans (whales, including dolphins and porpoises) and sirenians (manatees, dugongs), but also many amphibious mammals that spend some time on land (e.g., seals, otters, hippos, polar bears). Aquatic mammals retain terrestrial‐based systems that have been vastly modified for existence in water, but this alone does not make them extreme. However, within this group are some notable extremists: the cetaceans. They have the strangest anatomical aquatic adaptations – the ones with the “‐est” adjectives – enabling the deepest dive, slowest pulse, longest apnea, shortest exhalation, largest nose, narrowest mandible, strongest suction, biggest hyoid, widest mouth, stretchiest gular region, hairiest moustache, loudest sound, lowest song, longest tooth, highest vocalization, fattiest ear, tiniest external auditory meatus, densest tympanic bulla, curliest tongue, smoothest skin, stiffest cervical vertebrae, bumpiest forelimb, heaviest testes, and fastest copulation. For example, the sperm whale can dive to the bottom of the ocean and hold its breath for nearly an hour. Its head that is nearly one‐third of its body length, and is comprised of an enormous nose modified for sound production. Its mandible may plow the sea floor, and the hyoid and tongue create suction to engulf prey. The blue whale is the biggest mammal that ever existed, and has the widest mouth for engulfing prey. It has the largest larynx capable of making the loudest and lowest vocalizations. The narwhal has an elongated tooth that is likely the basis for the legend of the unicorn's horn. The dolphin uses modified nostrils to generate ultra high frequency sounds for echolocation, and uses acoustic fats as pinnae to receive sounds. A whale calf can curl the tongue into a straw for channeling milk when nursing underwater. Whale skin is very smooth enabling hydrodynamic water flow, and compressed/fused cervical vertebrae eliminate friction from lateral head deviations. The elongated flippers of humpback whales have bumps on the leading edge that increase efficiency. The porpoise is the smallest whale but has the largest testes and longest penis that can be rapidly extruded for the quickest mating. These amazing anatomical aquatic adaptations make cetaceans one of the most extreme groups of animals on Earth.

Kinematics of terrestrial locomotion in harbor seals and gray seals: Importance of spinal flexion by amphibious phocids

AbstractPinnipeds are amphibious mammals with flippers, which function for both aquatic and terrestrial locomotion. Evolution of the flippers has placed constraints on the terrestrial locomotion of phocid seals. The detailed kinematics of terrestrial locomotion of gray (Halichoerus grypus) and harbor (Phoca vitulina) seals was studied in captivity and in the wild using video analysis. The seals exhibited dorsoventral undulations with the chest and pelvis serving as the main contact points. An anteriorly directed wave produced by spinal flexion aided in lifting the chest off the ground as the fore flippers were retracted to pull the body forward. The highest length‐specific speeds recorded were 1.02 BL/s for a gray seal in captivity and 1.38 BL/s for a harbor seal in the wild. The frequency and amplitude of spinal movement increased directly with speed, but the duty factor remained constant. Substrate did not influence the kinematics except for differences due to moving up or down slopes. The highly aquatic nature of phocids seals has restricted them to locomote on land primarily using spinal flexion, which can limit performance in speed and duration.

Hearing in the sea otter (Enhydra lutris): auditory profiles for an amphibious marine carnivore.

In this study we examine the auditory capabilities of the sea otter (Enhydra lutris), an amphibious marine mammal that remains virtually unstudied with respect to its sensory biology. We trained an adult male sea otter to perform a psychophysical task in an acoustic chamber and at an underwater apparatus. Aerial and underwater audiograms were constructed from detection thresholds for narrowband signals measured in quiet conditions at frequencies from 0.125-40 kHz. Aerial hearing thresholds were also measured in the presence of octave-band masking noise centered at eight signal frequencies (0.25-22.6 kHz) so that critical ratios could be determined. The aerial audiogram of the sea otter resembled that of sea lions and showed a reduction in low-frequency sensitivity relative to terrestrial mustelids. Best sensitivity was -1 dB re 20 µPa at 8 kHz. Under water, hearing sensitivity was significantly reduced when compared to sea lions and other pinniped species, demonstrating that sea otter hearing is primarily adapted to receive airborne sounds. Critical ratios were more than 10 dB higher than those measured for pinnipeds, suggesting that sea otters are less efficient than other marine carnivores at extracting acoustic signals from background noise, especially at frequencies below 2 kHz.

Toros-Menalla (Chad, 7 Ma), the earliest hominin-bearing area: How many mammal paleocommunities?

The fossiliferous area of Toros-Menalla (TM) (Djurab Desert, northern Chad) has yielded one of the richest African mammal faunas of the late Miocene. It is also the place where the earliest known hominin, Sahelanthropus tchadensis, was found. Although more than 300 localities are recorded in that area, previous paleoecological studies focused only on the largest and richest one. The integration of the material from other TM localities, and thus of a significant number of mammal taxa, is crucial to improve the corresponding paleoenvironmental reconstructions. Before such inferences can be drawn, it is necessary to test for the ecological integrity of these mammal assemblages: how many paleocommunities do they represent?The faunal structures of several assemblages selected for their apparent resilience to sampling biases are compared here. The criteria used in the inter-assemblage comparison are ecological diversity, taxonomic structure (taxonomic rank of abundance) and taxonomic composition. Based on multivariate analyses, two groups of TM assemblages can be distinguished. One of them contains the hominin-bearing assemblages. It is taxonomically richer and shows a wider ecological spectrum than its counterpart. The degree of taphonomic alteration undergone by the TM assemblages, as well as the distribution of amphibious mammals among them, suggest different depositional settings for these two groups of assemblages, the richest of which was probably associated with lower hydraulic energy. Overall, it seems that the TM assemblages recorded the same mammal paleocommunity preserved in two contrasted depositional settings. Moreover, the spatial overlap of these assemblages provides further evidence for the mosaic character of the landscape associated with S. tchadensis.

Proximity loggers on amphibious mammals: a new method to study social relations in their terrestrial habitat

Amphibious mammal species alternate between foraging at sea and attendance on land. Due to thermoregulatory requirements, they often haul out during the night, making social interactions difficult to observe. We tested the suitability of UHF-proximity loggers for assessing social relationships among Galapagos sea lions Zalophus wollebaeki. To survive periods at sea, proximity loggers were embedded in epoxy. Automatic downloads to receiving stations rendered logger recovery unnecessary. Encounters were logged within a range of 10 m. Logs provided information about interacting individuals as well as time and duration of encounters. 'Received signal strength indicator' values correlated with distance, but were influenced by antenna angle and environmental factors. Laboratory tests and validation in the field demonstrated that the spa- tial resolution corresponded to 2 m. Data needed to be corrected, as single encounters were recorded as multiple logs and reciprocity of loggings between animals was not always achieved. Digital data correlated with observational data, but associations were 4 times more likely to be detected using proximity loggers. Data revealed that non-territorial males frequently associated for extended periods of time, especially during the night and even outside the study colony. The modified proximity logger system proves an excellent tool to determine social structure in situations where direct observation is limited.

Basic mechanisms in pinniped vision

Pinnipeds are amphibious mammals. The amphibious lifestyle is challenging for all sensory systems including vision, and specific adaptations of the eyes have evolved in response to the changed requirements concerning vision in two optically very different media, water and air. The present review summarizes the information available on pinniped eyes with an emphasis on harbour seal vision for which most information is available to date. Recent studies in this species have improved the understanding of amphibious vision by reanalysing refraction, by studying corneal topography, and by measuring visual acuity as a function of ambient luminance. The harbour seal eye can be characterized as an eye that balances high resolution, supported by data on ganglion cell density and topography, and sensitivity. Furthermore, it was shown that seals have multifocal lenses, broad visual Welds, and distinct eye movement abilities. The mechanisms described here form the basis for future research on visually guided behaviour.

Novel sound production through contingency learning in the Pacific walrus (Odobenus rosmarus divergens)

Walruses (Odobenus rosmarus) are highly vocal amphibious mammals with a range of anatomical specializations that can provide plasticity to their sound emissions. The objective of this descriptive study was to determine whether contingency learning could be used to increase variability and induce novelty in the acoustic behavior of walruses. The subjects were two twelve-year-old captive walruses, a male and a female that had previously been conditioned using food reinforcement to produce several specific sounds in response to different discriminative cues. In the current task, these individuals were encouraged to produce novel sounds and novel sound combinations in air by withholding reinforcement for sounds previously emitted in a given session and providing reinforcement only for qualitative differences in emitted sounds. Following training in air, the walruses were tested under water with the same reinforcement contingency. The subjects responded as they had done in air, by varying their underwater sound emissions until reinforcement was provided. Many of the sounds and sound combinations produced by the subjects during underwater testing were quite different from those produced during training in air and those produced under water during baseline observations. Both the male and female spontaneously emitted knocks and soft bells which are components of the songs known to be emitted by mature male walruses during the breeding season. The finding that reinforced variability can induce creativity in sound production is consistent with recent experiments on budgerigar birds showing that vocal topographies, like motor responses, may be influenced by contingency learning.

Electrophysiological Assessment of Temporal Resolution in Pinnipeds

Studies of auditory temporal processing in marine mammals have traditionally focused on the highly refined temporal resolution capabilities of dolphins and other odontocete cetaceans. However, a recent electrophysiological investigation of manatee (Trichechus manatus) hearing has shown their temporal resolution to be better than expected, leading to speculation that enhanced temporal processing capabilities are adaptive for underwater sound localization. This study measured evoked responses from several California sea lions (Zalophus californianus), a harbor seal (Phoca vitulina), and a northern elephant seal (Mirounga angustirostris) to determine how well the auditory systems of these amphibious mammals resolve rhythmic stimuli. Trains of broadband clicks were presented in air at repetition rates from 125 to 1,500 s -1 , and the averaged evoked responses elicited by these stimuli were recorded from the skin. Rate-following responses were detected in the sea lions at rates up to 1,000 s -1 , with an estimated upper limit of temporal resolution between 875 to 1,000 s -1 . This upper limit is better than previously anticipated and was further substantiated by limited testing with the harbor seal and northern elephant seal. While these findings might support an underwater sound localization hypothesis, measurements comparable to those of the pinnipeds were also obtained in a phylogenetically similar terrestrial mammal: a domestic dog (Canis familiaris). It is therefore possible that increased temporal resolution in pinnipeds and other nonecholocating marine mammals is not a result of the evolutionary pressure of an aquatic environment.

Comparative anatomy of the ciliary body of the West Indian manatee (Trichechus manatus) and selected species

To examine the anatomy of the ciliary body in the West Indian manatee (Trichechus manatus), paying close attention to its vascularization and to compare to those of its distant relative, the African elephant (Loxodonta africana), the amphibious hippopotamus (Hippopotamus amphibius) and the aquatic short-finned pilot whale (Globicephala macrorhynchus). Specimens from each species were preserved in 10% buffered formalin, and observed stereomicroscopically before being embedded in paraffin, sectioned and stained by Masson trichrome, hematoxylin and eosin, and periodic acid-Schiff for light microscopic evaluation. The network of blood vessels in the ciliary processes of the West Indian manatee appear to have an intricate pattern, especially with regard to venous outflow. Those of the elephant are slightly less complex, while those of the hippopotamus and whale have different vascular patterns within the ciliary body. Musculature within the ciliary body is absent within the manatee and pilot whale. In general, there appears to be a direct relationship between the increased development of vasculature and the loss of musculature within the ciliary bodies of the aquatic and amphibious mammals presently studied. Specifically, the ciliary body of the West Indian manatee has a comparatively unique construction, especially with regard to its vasculature.

Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad.

All six known specimens of the early hominid Sahelanthropus tchadensis come from Toros-Menalla site 266 (TM 266), a single locality in the Djurab Desert, northern Chad, central Africa. Here we present a preliminary analysis of the palaeontological and palaeoecological context of these finds. The rich fauna from TM 266 includes a significant aquatic component such as fish, crocodiles and amphibious mammals, alongside animals associated with gallery forest and savannah, such as primates, rodents, elephants, equids and bovids. The fauna suggests a biochronological age between 6 and 7 million years. Taken together with the sedimentological evidence, the fauna suggests that S. tchadensis lived close to a lake, but not far from a sandy desert, perhaps the oldest record of desert conditions in the Neogene of northern central Africa.

Aquatic adaptations in desmostylians

Osteological characteristics of extant, quadrupedal, aquatic or amphibious mammals are compared and used to determine the presence and state of development, or absence, of aquatic adaptations in the order Desmostylia. The specimens compared include seventeen bones from in each species four higher taxa: Rodentia, Carnivora, Mustelidae and Artiodactyla. The aquatic form is compared with its terrestrial counterpart within each group. Quantitative evidence of convergence is used to sort out characters that are adaptive in relation to aquatic habits. Aquatic conformations or tendencies are identified as those characters, displayed by aquatic forms in different taxonomic groups, that have more in common with each other than with corresponding characters of land animals in the same taxa. About 80% of the 49 aquatic adaptive characters identified are also found in desmostylians. This analysis documents the gradual evolutionary transition of desmostylians to an aquatic mode of life. Furthermore, the results show that the desmostylian swam better using its hind‐limbs at least than the hippopotamus.

Behaviour and ecology of riparian mammals

List of contributors Preface 1. Adaptations to the semi-aquatic habit and habitat N. Dunstone 2. Physiological challenges in semi-aquatic mammals: swimming against the energetic tide T. M. Williams 3. Diving capacity and foraging behaviour of the water shrew (Neomys fodiens) P. Vogel, C. Bodmer, M. Spreng and J. Aeschimann 4. Habitat use by water shrews, the smallest of amphibious mammals S. Churchfield 5. The importance of the riparian environment as a habitat for British bats P. A. Racey 6. A preliminary study of the behaviour of the European mink Mustela lutreola in Spain, by means of radiotracking S. Palazon and J. Ruiz-Olmo 7. The demography of European otters Lutra lutra M. L. Gorman, H. Kruuk, C. Jones, G. McLaren and J. W. H. Conroy 8. Habitat use and conservation of otters (Lutra lutra) in Britain: a review H. Kruuk, D. N. Carss, J. W. H. Conroy and M. J. Gaywood 9. The relationship between riverbank habitat and prey availability and the distribution of otter (Lutra lutra) signs: an analysis using a geographical information system T. J. Thom, C. J. Thomas, N. Dunstone and P. R. Evans 10. Influence of altitude on the distribution, abundance and ecology of the otter (Lutra lutra) J. Ruiz-Olmo 11. Diets of semi-aquatic carnivores in northern Belarus, with implications for population changes V. Sidorovich, H. Kruuk, D. W. Macdonald and T. Maran 12. Otter (Lutra lutra) prey selection in relation to fish abundance and community structure in two different freshwater habitats D. N. Carss, K. C. Nelson, P. J. Bacon and H. Kruuk 13. Diet, foraging behaviour and coexistence of African otters and the water mongoose D. T. Rowe-Rowe and M. J. Somers 14. Feeding ecology of the smooth-coated otter Lutra perspicillata in the National Chambal Sanctuary, India S. A. Hussain and B. C. Choudhury 15. Population trends of hippopotami in the rivers of the Kruger National Park, South Africa P. C. Viljoen and H. C. Biggs 16. Reproductive strategies of female capybaras: dry-season gestation E. A. Herrera 17. The continuing decline of the European mink Mustela lutreola: evidence for the intraguild aggression hypothesis T. Maran, D. W. Macdonald, H. Kruuk, V. Sidorovich and V. V. Rozhnov 18. Otters and pollution in Spain J. Ruiz-Olmo, J. M. Lopez-Martin and M. Delibes 19. The rapid impact of resident American mink on water voles: case studies in lowland England C. Strachan, D. J. Jeffries, G. R. Barreto, D. W. Macdonald and R. Strachan 20. Status, habitat use and conservation of giant otter in Peru C. Schenck and E. Staib Index.

Locomotor evolution in the earliest cetaceans: functional model, modern analogues, and paleontological evidence

We discuss a model for the origin of cetacean swimming that is based on hydrodynamic and kinematic data of modern mammalian swimmers. The model suggests that modern otters (Mustelidae: Lutrinae) display several of the locomotor modes that early cetaceans used at different stages in the transition from land to water. We use mustelids and other amphibious mammals to analyze the morphology of the Eocene cetaceanAmbulocetus natans, and we conclude thatAmbulocetusmay have locomoted by a combination of pelvic paddling and dorsoventral undulations of the tail, and that its locomotor mode in water resembled that of the modern otterLutramost closely. We also suggest that cetacean locomotion may have resembled that of the freshwater otterPteronuraat a stage beyondAmbulocetus.

Seed dispersal of Nymphoides peltata (S.G. Gmelin) O. Kuntze (Menyanthaceae)

Nymphoides peltata (S.G. Gmelin) O. Kuntze is a common and relatively widespread aquatic plant; for efficient dispersal seeds must be transported over land from one body of water to another. The seeds are thin-walled and digested by fish and waterfowl and thus unsuitable for endozoochory. The seeds are disc-like with rigid marginal trichomes, they are heavier than water and are kept floating by a relatively weakly hydrophobic coating. They occupy the air-water interface and aggregate into chainlike rafts thus offering vectors moving through the water large targets. The seeds are picked up by some parts of waterfowl, such as the flanks, the region between bill and eyes and the webs of the feet of the mallard, and the bill and shield of the coot; perhaps some amphibious mammals also play a role. The marginal trichomes ensure that the seeds stick to the vector in a dry atmosphere. When the marginal trichomes are removed the seeds sink with the slightest disturbance, but if they do stick to a vector they fall off as they become dry. The weakly hydrophobic coating guarantees that the seeds will be discarded in water where they need to be for germination. Seeds made highly hydrophobic by being coated with silicon or teflon would not stick to vectors, neither would they sink; if made hydrophilic they would not float nor would they stick to vectors in water but if deliberately placed on a vector in air they were not discarded when the vector was put into water.

Refractive state, ocular anatomy, and accommodative range of the sea otter ( Enhydra lutris)

Sea otters are carnivorous, amphibious mammals that are active both above and under water. Accordingly, it might be expected that their eyes are adapted for both aerial and aqueous vision. We examined the anatomy and physiological optics of the sea otter eye with a view towards describing and explaining its amphibious visual characteristics. We employed photokeratoscopy to measure the refractive power of the sea otter cornea, which we found to be 59 D. Using video dynamic photorefraction, we found that sea otters can focus targets clearly both in air and water, relying on accommodation to compensate for the refractive loss of their corneas upon immersion in water. Our anatomical investigations revealed that the anterior epithelium of the cornea is extensively developed, as is the iris musculature, meridional ciliary muscle, and the corneoscleral venous plexus. The first feature is most likely an adaptation to the salinity of the marine environment. We believe the latter features are part of a novel, well-developed lenticular accommodative mechanism.

Intraocular muscles of the Canadian river otter and Canadian beaver and their optical function

The gross morphology and microscopic anatomy of the ciliary and iris musculature of the Canadian river otter (Lutra canadensis) and Canadian beaver (Castor canadensis) were studied to help evaluate whether either species has an exaggerated accommodative mechanism for use underwater. The intraocular muscles of the otter are of a size and organization indicative of an extreme lens-deforming accommodative ability involving both the ciliary body and iris. By contrast, the intraocular muscles of the beaver eye indicate that accommodation is not significant in this animal. Thus, the intraocular musculature of the class Mammalia is not homogeneous, even within the amphibious mammals. Refractive and corneal measurements on two living river otters confirm that this animal is capable of an accommodative range that can neutralize the loss of corneal refractive power when the eye is in water.

On the origins of Hippopotamidae togetherwith descriptions of two new species, a new genus and a new subfamily from the Miocene of Kenya

The discovery of Kenyapotamus coryndoni and K. ternani, two new taxa of Hippopotamidae, permits a reassessment of the origins of the family. Hitherto considered to have been derived from an anthracothere stock, it now seems more likely that Hippopotamidae evolved from Old World Tayassuidae early in the middle Miocene or in the lower Miocene. The new genus is known by two species, a small one at Fort Ternan and Maboko, a slightly larger one at Ngeringerowa and Nakali. The palaeoenvironments of large amphibious mammals of Eastern Africa are examined. It is noted that Anthracotheres which were common in lower Miocene deposits of Kenya became extinct locally by the time that the earliest hippopotamids came on the scene. A straightforward niche exchange may be visualised whereby hippopotamids either replaced anthracotheres in the East African large mammal amphibious niche, or evolved in response to the vacation of this niche by anthracotheres. The earliest true Hippopotamus appears in the Kenya fossil record rather abruptly at about 7 m.y. ago. So far the new genus and Hippopotamus have not been found together in the same deposits.