Seasonal movements and behaviour of basking sharks from archival tagging: No evidence of winter hibernation

Habitat selection processes in highly migratory animals such as sharks and whales are important to understand because they influence patterns of distribution, availability and therefore catch rates. However, spatial strategies remain poorly understood over seasonal scales in most species, including, most notably, the plankton-feeding basking shark Cetorhinus maximus. It was proposed nearly 50 yr ago that this globally distributed species migrates from coastal summer-feeding areas of the northeast Atlantic to hibernate during winter in deep water on the bottom of continental-shelf slopes. This view has perpetuated in the literature even though the 'hibernation theory' has not been tested directly. We have now tracked basking sharks for the first time over seasonal scales (1.7 to 6.5 mo) using 'pop-up' satellite archival transmitters. We show that they do not hibernate during winter but instead undertake extensive horizontal (up to 3400 km) and vertical (> 750 m depth) movements to utilise productive continental-shelf and shelf-edge habitats during summer, autumn and winter. They travel long distances (390 to 460 km) to locate temporally discrete productivity 'hotspots' at shelf-break fronts, but at no time were prolonged movements into open-ocean regions away from shelf waters observed. Basking sharks have a very broad vertical diving range and can dive beyond the known range of planktivorous whales. Our study suggests this species can exploit shelf and slope-associated zooplankton communities in mesopelagic (200 to 1000 m) as well as epipelagic habitat (0 to 200 m).

Hibernation and non-shivering thermogenesis in the Hottentot golden mole (Amblysomus hottentottus longiceps)

Although heterothermy (hibernation and torpor) is a common feature among mammals, there is debate over whether it is a derived or ancestral trait relative to endothermic homeothermy. Determination of the physiological characteristics of primitive mammals is central to understanding the evolution of endothermy. Moreover, evaluation of physiological mechanisms responsible for endothermic heat production [e.g. non-shivering thermogenesis (NST)] is key to understanding how early mammals responded to historical climate changes and colonised different geographical regions. Here we investigated the capacity for NST and heterothermy in the Hottentot golden mole, a basal eutherian mammal. NST was measured as the metabolic response to injections of noradrenalin and heterothermy by recording body temperature in free-ranging animals. We found that hibernation and torpor occurred and that the seasonal phenotypic adjustment of NST capacity was similar to that found in other placental mammals. Using phylogenetically independent contrasts, we compared measured values of NST with those obtained from the literature. This showed that all variation in NST was accounted for by differences in phylogeny and not zoogeography. These findings lend support to the observation that NST and heterothermy occur in the Afrotheria, the basal placental mammalian clade. Furthermore, this work suggests that heterothermy, rather than homeothermy is a plesiomorphic trait in mammals and supports the notion that NST mechanisms are phylogenetically ancient.

Frequent Arousal from Hibernation Linked to Severity of Infection and Mortality in Bats with White-Nose Syndrome

White-nose syndrome (WNS), an emerging infectious disease that has killed over 5.5 million hibernating bats, is named for the causative agent, a white fungus (Geomyces destructans (Gd)) that invades the skin of torpid bats. During hibernation, arousals to warm (euthermic) body temperatures are normal but deplete fat stores. Temperature-sensitive dataloggers were attached to the backs of 504 free-ranging little brown bats (Myotis lucifugus) in hibernacula located throughout the northeastern USA. Dataloggers were retrieved at the end of the hibernation season and complete profiles of skin temperature data were available from 83 bats, which were categorized as: (1) unaffected, (2) WNS-affected but alive at time of datalogger removal, or (3) WNS-affected but found dead at time of datalogger removal. Histological confirmation of WNS severity (as indexed by degree of fungal infection) as well as confirmation of presence/absence of DNA from Gd by PCR was determined for 26 animals. We demonstrated that WNS-affected bats aroused to euthermic body temperatures more frequently than unaffected bats, likely contributing to subsequent mortality. Within the subset of WNS-affected bats that were found dead at the time of datalogger removal, the number of arousal bouts since datalogger attachment significantly predicted date of death. Additionally, the severity of cutaneous Gd infection correlated with the number of arousal episodes from torpor during hibernation. Thus, increased frequency of arousal from torpor likely contributes to WNS-associated mortality, but the question of how Gd infection induces increased arousals remains unanswered.

White-Nose Syndrome-Affected Litttle Brown Myotis (Myotis Lucifugus) Increase Grooming and Other Active Behaviors During Arousals from Hibernation

White-nose syndrome (WNS) is an emerging infectious disease of hibernating bats linked to the death of an estimated 5.7 million or more bats in the northeastern United States and Canada. White-nose syndrome is caused by the cold-loving fungus Pseudogymnoascus destructans (Pd), which invades the skin of the muzzles, ears, and wings of hibernating bats. Previous work has shown that WNS-affected bats arouse to euthermic or near euthermic temperatures during hibernation significantly more frequently than normal and that these too-frequent arousals are tied to severity of infection and death date. We quantified the behavior of bats during these arousal bouts to understand better the causes and consequences of these arousals. We hypothesized that WNS-affected bats would display increased levels of activity (especially grooming) during their arousal bouts from hibernation compared to WNS-unaffected bats. Behavior of both affected and unaffected hibernating bats in captivity was monitored from December 2010 to March 2011 using temperature-sensitive dataloggers attached to the backs of bats and infrared motion-sensitive cameras. The WNS-affected bats exhibited significantly higher rates of grooming, relative to unaffected bats, at the expense of time that would otherwise be spent inactive. Increased self-grooming may be related to the presence of the fungus. Elevated activity levels in affected bats likely increase energetic stress, whereas the loss of rest (inactive periods when aroused from torpor) may jeopardize the ability of a bat to reestablish homeostasis in a number of physiologic systems.

The Effects of Hibernation on Immunological Functions in Female Big Brown Bats (Eptesicus fuscus)

The emerging disease White-Nose Syndrome in hibernating bat populations across the United States has increased the need to understand the physiological benefits and consequences of hibernation and the effects on immunological responsiveness. Hibernation has been well-documented in many mammalian species, yet few studies have examined hibernation immunology in bats, particularly with respect to normal immunological patterns. In order to characterize the levels of circulating leukocytes and plasma immunoglobulins in euthermic and hibernating female big brown bats (Eptesicus fuscus), blood smear differential leukocyte counts and total immunoglobulin assays were performed for each group using blood samples from the active and hibernation seasons. Hibernation patterns – torpor and arousals from torpor – were determined by placing temperature-sensitive dataloggers on the backs of bats assigned to the hibernating group during the hibernation season. Data indicate that the ratio of circulating neutrophils to lymphocytes is lower in bats assigned to the euthermic group during the hibernation season than in bats assigned to the hibernation group during the hibernation period, but that relative immunoglobulin levels do not differ during the hibernation season, regardless of whether bats were active or hibernating. Neither bats assigned to the hibernation group nor bats assigned to the euthermic group demonstrate a significant change in the ratio of circulating neutrophils and lymphocytes between their active and hibernating seasons. Bats assigned to the hibernation group were also observed to arouse from torpor somewhat synchronously. These results suggest that innate and adaptive cell levels are maintained, at best, in hibernating bats that are not immunologically challenged and that bats that remain euthermic during the hibernation season are able to continually regulate their levels of neutrophils and lymphocytes and therefore their innate and adaptive immune system responses.

Transgenic system for conditional induction and rescue of chronic myocardial hibernation provides insights into genomic programs of hibernation

A key energy-saving adaptation to chronic hypoxia that enables cardiomyocytes to withstand severe ischemic insults is hibernation, i.e., a reversible arrest of contractile function. Whereas hibernating cardiomyocytes represent the critical reserve of dysfunctional cells that can be potentially rescued, a lack of a suitable animal model has hampered insights on this medically important condition. We developed a transgenic mouse system for conditional induction of long-term hibernation and a system to rescue hibernating cardiomyocytes at will. Via myocardium-specific induction (and, in turn, deinduction) of a VEGF-sequestering soluble receptor, we show that VEGF is indispensable for adjusting the coronary vasculature to match increased oxygen consumption and exploit this finding to generate a hypoperfused heart. Importantly, ensuing ischemia is tunable to a level at which large cohorts of cardiomyocytes are driven to enter a hibernation mode, without cardiac cell death. Relieving the VEGF blockade even months later resulted in rapid revascularization and full recovery of contractile function. Furthermore, we show that left ventricular remodeling associated with hibernation is also fully reversible. The unique opportunity to uncouple hibernation from other ischemic heart phenotypes (e.g., infarction) was used to determine the genetic program of hibernation; uncovering hypoxia-inducible factor target genes associated with metabolic adjustments and induced expression of several cardioprotective genes. Autophagy, specifically self-digestion of mitochondria, was identified as a key prosurvival mechanism in hibernating cardiomyocytes. This system may lend itself for examining the potential utility of treatments to rescue dysfunctional cardiomyocytes and reverse maladaptive remodeling.

Effects of hibernation on bone in yellow-bellied marmots

Disuse osteoporosis is a problem for people with spinal cord injury or stroke, patients confined to bed rest, and astronauts exposed to microgravity. Unlike most mammals however, bears have been shown to prevent bone loss during hibernation, a seasonal period of disuse. Similarly, studies in ground squirrels indicate preservation of whole bone strength during hibernation, though evidence suggests there may be some increased osteocytic osteolysis. Uncovering the mechanism by which these animals prevent bone loss during hibernation could lead to an improved treatment for osteoporosis in humans. Marmots are a good animal model for these studies because they are small enough to easily house in an animal facility yet still utilize intracortical remodeling like humans and bears, and unlike smaller rodents like squirrels. Marmots preserve bone mechanical and microstructural properties during hibernation. Bone mechanical and geometrical properties are not diminished in post-hibernation samples compared to pre-hibernation samples. Mineral content, measured by ash fraction, was higher in post-hibernation samples (p = 0.0003). Haversian porosity as well as remodeling cavity density were not different (p > 0.38) between pre- and post-hibernation samples. Similarly, average lacunar area, lacunar density, and lacunar porosity were all lower (p < 0.0001) in post-hibernation samples. Trabecular thickness was larger in posthibernation samples (p = 0.0058). Bone volume fraction was not different between groups, but approached significance (p = 0.0725). Further studies in marmots and other hibernators could help uncover the mechanism that allows hibernators to prevent disuse osteoporosis during hibernation.

Exploration of the role of serum factors in maintaining bone mass during hibernation in black bears

Disuse osteoporosis is a condition in which reduced mechanical loading (e.g. bed-rest, immobilization, or paralysis) results in unbalanced bone turnover. The American black bear is a unique, naturally occurring model for the prevention of disuse osteoporosis. Bears remain mostly inactive for up to half a year of hibernation annually, yet they do not lose bone mechanical strength or structural properties throughout hibernation. The long-term goal of this study is to determine the biological mechanism through which bears maintain bone during hibernation. This mechanism could pinpoint new signaling pathway targets for the development of drugs for osteoporosis prevention. In this study, bone specific alkaline phosphatase (BSALP), a marker of osteoblast activity, and tartrate resistant acid phosphatase (TRACP), a marker of osteoclast number, were quantified in the serum of hibernating and active black bears. BSALP and TRACP decreased during hibernation, suggesting a balanced reduction in bone turnover. This decrease in BSALP and TRACP were correlated positively to serum adiponectin and inversely to serum neuropeptide Y, suggesting a possible role of these hormones in suppressing bone turnover during hibernation. Osteocalcin (OCN) and undercarboxylated OCN increased dramatically in the serum of hibernating bears. These increases were inversely correlated with adiponectin, glucose, and serotonin, suggesting that OCN may have a unique role in energy homeostasis during hibernation. Finally, MC3T3-E1 osteoblasts were cultured in the serum from active and hibernating bears, and seasonal cell responses were quantified. Cells cultured in serum from hibernating bears had a reduced caspase-3/7 response, and more living cells, after apoptotic threat. The caspase-3/7 response was positively correlated to serum adiponectin and to gene expression of OCN and Runx2, suggesting that reduced caspase-3/7 activity may be related to the reduced differentiation potential of osteoblasts in hibernation serum, and that adiponectin is a potential effector hormone. In summary, the activities of osteoblasts and osteoclasts are reduced during hibernation in bears. This reduced turnover is due, in part, to hormonal control. Further study of potential effectors adiponectin and neuropeptide Y may provide insight into the biological mechanism through which bears maintain bone throughout hibernation.

Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation

Protein synthesis (PS) has been considered essential to sustain mammalian life, yet was found to be virtually arrested for weeks in brain and other organs of the hibernating ground squirrel, Spermophilus tridecemlineatus. PS, in vivo, was below the limit of autoradiographic detection in brain sections and, in brain extracts, was determined to be 0.04% of the average rate from active squirrels. Further, it was reduced 3-fold in cell-free extracts from hibernating brain at 37°C, eliminating hypothermia as the only cause for protein synthesis inhibition (active, 0.47 ± 0.08 pmol/mg protein per min; hibernator, 0.16 ± 0.05 pmol/mg protein per min, P < 0.001). PS suppression involved blocks of initiation and elongation, and its onset coincided with the early transition phase into hibernation. An increased monosome peak with moderate ribosomal disaggregation in polysome profiles and the greatly increased phosphorylation of eIF2α are both consistent with an initiation block in hibernators. The elongation block was demonstrated by a 3-fold increase in ribosomal mean transit times in cell-free extracts from hibernators (active, 2.4 ± 0.7 min; hibernator, 7.1 ± 1.4 min, P < 0.001). No abnormalities of ribosomal function or mRNA levels were detected. These findings implicate suppression of PS as a component of the regulated shutdown of cellular function that permits hibernating ground squirrels to tolerate “trickle” blood flow and reduced substrate and oxygen availability. Further study of the factors that control these phenomena may lead to identification of the molecular mechanisms that regulate this state.

Ablation of suprachiasmatic nucleus alters timing of hibernation in ground squirrels.

Hibernation patterns were monitored continuously for 2.5 years in female squirrels that were neurologically intact or in which the hypothalamic suprachiasmatic nucleus (SCN) was completely ablated (SCNx). The number of hibernation bouts in SCNx squirrels increased by 159%, total hibernation time increased by 58%, and periodic arousals from hibernation were 47% longer in SCNx than in control squirrels; the duration of individual torpor bouts was 2 days shorter and far more variable in SCNx than in control animals. Some SCNx squirrels cycled through bouts of torpor continuously for nearly 2 years. The SCN appears to be part of the mechanism that controls the duration of the hibernation season and the temporal structure of individual torpor bouts.

An evolutionary framework for studies of hibernation and short-term torpor

Data from diverse studies endorse ideas that short term torpor and hibernation are expressions of ancient characters. In evolutionary terms, their basic mechanisms are probably plesiomorphic (= ancestral/primitive) and physiologically similar. This contrasts with the alternate view that they are apomorphic (= derived, specialized), arising independently in many taxa from homeothermic ancestry by numerous apparent convergences. This paper explores some of the implications of accepting the plesiomorphic interpretation. Hibernation is, of course, a complex phenomenon that has undergone variations and refinements in different mammalian lineages. The argument is not that hibernation in total is a plesiomorphic character, but that it is built upon fundamental processes that are. Taking this view provides a framework for research that emphasizes the value of comparative studies, particularly of reptiles and birds. Studies of reptiles, for example, might unravel the mystery about periodic arousals. A plesiomorphic framework also explains the most extreme examples of hibernation as derived specializations from ancestry in which heterothermy is more about energy management than escape from cold. It cautions against using low body temperature (Tb) alone to diagnose torpor, emphasizes the need to distinguish between constitutional eurythermy (plesiomorphic) and constitutional stenothermy (apomorphic), and leads to a parsimonious theory about the evolution of endothermy. The paper proposes that brown adipose tissue (BAT) is apomorphic within eutheria and highlights the conundrum posed by the occurrence of both nonshivering thermogenesis (NST) and rapid arousal from hibernation in noneutherian mammals that lack BAT and uncoupling protein 1 (UCP1). It endorses the likely existence of a different, ancient and widespread mechanism for regulatory NST in mammals.

Genome analysis reveals insights into physiology and longevity of the Brandt’s bat Myotis brandtii

Bats account for one-fifth of mammalian species, are the only mammals with powered flight, and are among the few animals that echolocate. The insect-eating Brandt’s bat (Myotis brandtii) is the longest-lived bat species known to date (lifespan exceeds 40 years) and, at 4–8 g adult body weight, is the most extreme mammal with regard to disparity between body mass and longevity. Here we report sequencing and analysis of the Brandt’s bat genome and transcriptome, which suggest adaptations consistent with echolocation and hibernation, as well as altered metabolism, reproduction and visual function. Unique sequence changes in growth hormone and insulin-like growth factor 1 receptors are also observed. The data suggest that an altered growth hormone/insulin-like growth factor 1 axis, which may be common to other long-lived bat species, together with adaptations such as hibernation and low reproductive rate, contribute to the exceptional lifespan of the Brandt’s bat.

Bats: Important reservoir hosts of emerging viruses

Bats (order Chiroptera, suborders Megachiroptera and Microchiroptera) are abundant, diverse, and geographically widespread. These mammals provide us with resources, but their importance is minimized and many of their populations and species are at risk, even threatened or endangered. Some of their characteristics (food choices, colonial or solitary nature, population structure, ability to fly, seasonal migration and daily movement patterns, torpor and hibernation, life span, roosting behaviors, ability to echolocate, virus susceptibility) make them exquisitely suitable hosts of viruses and other disease agents. Bats of certain species are well recognized as being capable of transmitting rabies virus, but recent observations of outbreaks and epidemics of newly recognized human and livestock diseases caused by viruses transmitted by various megachiropteran and microchiropteran bats have drawn attention anew to these remarkable mammals. This paper summarizes information regarding chiropteran characteristics and information regarding 66 viruses that have been isolated from bats. From these summaries, it is clear that we do not know enough about bat biology, that we are doing too little in terms of bat conservation, and that there remain a multitude of questions regarding the role of bats in disease emergence.

Bat habitat requirements : implications for land use planning

Knowledge of the habitat requirements of bat species is needed in decision making in land use planning. Bats' hibernation requirements were studied both in Estonia and in southern Finland. In both countries, the northern bat and the brown long-eared bat hibernated in colder and drier locations, whereas Daubenton's bat and Brandt's/whiskered bats hibernated in warmer and more humid locations. In Estonia, the pond bat hibernated in the warmest and most humid conditions, whereas Natterer's bat hibernated in the coldest and driest conditions. Hibernacula were at their coldest in mid-season and became warmer towards the end of the season. The results suggest that bats made an active choice of colder hibernation temperatures at the seasons end. They minimised the negative effects of hibernation early in the hibernation season by hibernating in warmer locations and energy expenditure late in the hibernation season by hibernating in colder locations. The use of foraging habitats was studied in northern and southern Finland. The northern bat used foraging sites opportunistically. Daubenton's bat foraged mainly in water habitats, whereas Brandt's/whiskered bats and the brown long-eared bat foraged mainly in forest habitats. In northern Finland, Daubenton's bats foraged almost exclusively on rivers and typically together with the northern bat. Daubenton's bats and Brandt's/whiskered bats were found only where there were lower ambient light levels. One of the most important things in the management of foraging areas for them is to keep them shady. Hibernacula in Finland typically housed few bats, suggesting that hibernation sites used by even a small number of bats are important. Bats typically used natural stone for hibernation suggesting that natural underground sites in rocks or cliffs or man-made underground sites built using natural stone are important for them. The results suggest that appropriate timing of surveys may vary according to the species and latitude.

Ground beetles and rove beetles be associated with temporary ponds in England

To date, research on the ecology and conservation of wetland invertebrates has concentrated overwhelmingly on fully aquatic organisms. Many of these spend part of their life-cycle in adjacent terrestrial habitats, either as pupae (water beetles) or as adults (mayflies, dragonflies, stoneflies, caddisflies and Diptera or true-flies). However, wetland specialist species also occur among several families of terrestrial insects (Williams & Feltmate 1992) that complete their whole life-cycle in the riparian zone or on emergent vegetation. There are 441 terrestrial invertebrate species which characteristically occur in riparian habitats along British rivers. Most of these species belong to two families of predatory beetles: the ground beetles (Carabidae) and the rove beetles (Staphylinidae). This paper describes the diversity of ground and rove beetles around ponds, summarises life-histories, hibernation strategies, and morphological and behavioural adaptions.