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Seasonal variation in resting metabolic rate and body temperature of streaked tenrecs, Hemicentetes nigriceps and H. Semispinosus (Insectivora: Tenrecidae)
Abstract
Annual variations in resting metabolic rate (RMR) and body temperature (Tb) were measured in the streaked tenrecs Hemicentetes nigiceps and H. semispinosus. RMR in non-reproducing, non-torpid adults was lower than predicted by the Kleiber (1961) curve, supporting Genoud's (1990) hypothesis on BMR in hibernating mammals. Both species demonstrated a reduction in RMR and Tb during the austral winter and these changes were independent of body mass. H. semispinosus frequently roused from torpor to forage whereas H. nigriceps remained dormant throughout the winter, This contrast in activity patterns may result from altitudinal differences in species distributions. H. nigriceps may be an obligate hibernator whereas H. semispinosus, living at lower, warmer altitudes, may be a facultative hibernator. It is proposed that the ability of H. semispinosus to remain active during favourable climatic conditions allows winter breeding and increases annual reproductive output.
... Relative to the mammalian norm, mammals with spines, armor, and noxious chemicals exhibit locomotion associated with stability rather than speed (Lovegrove, 2001). Furthermore, they often have low metabolic rates (McNab, 1984(McNab, , 2008Haim et al., 1990;Stephenson and Racey, 1994;Lovegrove, 2000). While attributing causation can be tricky, armor, spines, and noxiousness may both be associated with and permit slower speeds and lower metabolic rates. ...
In nature, many multicellular and unicellular organisms use constitutive defenses such as armor, spines, and noxious chemicals to keep predators at bay. These defenses render the prey difficult and/or dangerous to subdue and handle, which confers a strong deterrent for predators. The distinct benefit of this mode of defense is that prey can defend in place and continue activities such as foraging even under imminent threat of predation. The same qualitative types of armor-like, spine-like, and noxious defenses have evolved independently and repeatedly in nature, and we present evidence that cancer is no exception. Cancer cells exist in environments inundated with predator-like immune cells, so the ability of cancer cells to defend in place while foraging and proliferating would clearly be advantageous. We argue that these defenses repeatedly evolve in cancers and may be among the most advanced and important adaptations of cancers. By drawing parallels between several taxa exhibiting armor-like, spine-like, and noxious defenses, we present an overview of different ways these defenses can appear and emphasize how phenotypes that appear vastly different can nevertheless have the same essential functions. This cross-taxa comparison reveals how cancer phenotypes can be interpreted as anti-predator defenses, which can facilitate therapy approaches which aim to give the predators (the immune system) the upper hand. This cross-taxa comparison is also informative for evolutionary ecology. Cancer provides an opportunity to observe how prey evolve in the context of a unique predatory threat (the immune system) and varied environments.
... Par ailleurs, la saison agit comme un facteur limitant et entraîne la diminution de l'activité des Lipotyphles et conduit même à la torpeur pendant l'hiver. La baisse du taux métabolique basal (Stephenson P. & Racey P., 1994) ainsi que la diminution de la température ambiante peuvent avoir une relation à la régulation de la température du corps. De ce fait, on peut penser que l'effet de la diminution du métabolisme au repos ne peut pas recouvrir les besoins énergétiques nécessaires à la croissance d'où la baisse du poids de Lipotyphles observée à la fin de la saison sèche par rapport au début de cette saison. ...
Avec un substrat de structure arénacée sous un climat relativement chaud et sec, la forêt dense sèche semi-caducifoliée d'Ankarafantsika est loin d'être à l'abri des pressions dégradantes à majorité d'origine anthropique: l'exploitation de la forêt par l'homme est déterminante dans la structure et la dynamique de cet écosystème forestier, avec la population animale qu'il héberge. Les informations recueillies ont permis de constater la vulnérabilité des espèces autochtones et des mesures de conservation s'imposent. La présente étude se porte sur la composition spécifique, la structure de la communauté animale, la biologie des animaux cibles, la compréhension du réseau écologique ainsi que les dimensions socio-économiques y afférentes. Onze espèces de Micromammifères composées de 6 Rongeurs et de 5 Lipotyphles ont été rencontrées. La diversité biologique de la zone réside sur la présence de nombreuses espèces dominantes et/ou résidentes qui sont les plus souvent caractéristiques ou eucènes et/ou préférentes de telle sorte que la distribution d'abondance des animaux étudiés montre une hiérarchisation souvent dominée par les espèces de grande taille. Au niveau de cette communauté micromammalienne, la balance du sex-ratio est penchée légèrement en faveur des femelles, la polygamie et le phénomène de post-partum ont été observées pour la première fois chez Eliurus myoxinus, le faible effectif des jeunes par portée chez les Rongeurs endémiques a été prouvée, la prolificité de Tenrec ecaudatus a été également constatée, la population de Setifer setosus semble équilibrée par l'existence de nombreux parasites. Les recommandations suivantes se portent sur la sensibilisation et l'éducation de la population humaine sur l'importance de ces micromammifères, la réduction des diverses pressions, la gestion des ressources de la biodiversité animale et végétale. Toutes ces recommandations cherchent à préserver la forêt, sèche semi-caducifoliée, caractéristique de la zone écofloristique de basse altitude de l'ouest malagasy.
... In both cases torpid metabolic rates were much lower than would be expected from mere Q 10 effects when comparing torpidVO 2 with maximumVO 2 at maximum T skin (0.95-0.89 ml O 2 * g −1 * h −1 ; decrease in T b from about 30 • C to about 20 • C and drop inVO 2 to less than 5% of resting rates, instead of about 50% predicted by a Q10 of 2-3; Table 1). Thus, during the resting phases of fluctuating summer conditions, the decrease inVO 2 was not "only" due to the suppression of thermogenesis leading to the highly labile thermoregulation tenrecs are famous for (Nicoll, 1986;Stephenson and Racey, 1994;Lovegrove and Génin, 2008;, but also an indication of active metabolic inhibition. Only one female, in S const24 , remained normothermic for longer than 24 h on two occasions. ...
Hibernation and daily torpor (heterothermy) allow endotherms to cope with demanding environmental conditions. The depth and duration of torpor bouts vary considerably between tropical and temperate climates, and tropical hibernators manage to cope with a wider spectrum of ambient temperature (Ta) regimes during heterothermy. As cycles in Ta can have profound effects on activity and torpor patterns as well as energy expenditure, we examined how these characteristics are affected by daily fluctuating versus constant Ta in a tropical hibernator, the lesser hedgehog tenrec (Echinops telfairi). Throughout the study, regardless of season, the tenrecs became torpid every day. In summer, E. telfairi used daily fluctuations in Ta to passively rewarm from daily torpor, which led to synchrony in the activity phases and torpor bouts between individuals and generally decreased energy expenditure. In contrast, animals housed at constant Ta showed considerable variation in timing and they had to invest more energy through endogenous heat production. During the hibernation season (winter) E. telfairi hibernated for several months in constant, as well as in fluctuating Ta and, as in summer, under fluctuating Ta arousals were much more uniform and showed less variation in timing compared to constant temperature regimes. The timing of torpor is not only important for its effective use, but synchronization of activity patterns could also be essential for social interactions, and successful foraging bouts. Our results highlight that Ta cycles can be an effective zeitgeber for activity and thermoregulatory rhythms throughout the year and that consideration should be given to the choice of temperature regime when studying heterothermy under laboratory conditions.
... (Somrimalala and Goodman 2004) 98. (Stephenson 1994) 99. (Stephenson and Racey 1994) 100. (Sterling 1994) 101. ...
Invasive and introduced species can pose major ecological challenges to vulnerable
native wildlife. Biodiversity hotspots, in particular, require protection from this
significant cause of species loss. One hotspot, Madagascar, is experiencing the
accidental introduction of a potentially ecologically damaging species – the toxin
carrying bufonid toad, Duttaphyrnus melanostictus. The presence of these toxic
invaders drives fears that if such a species gains a foothold widespread poisoning of
Malagasy predators could occur, mirroring the invasion of Australia by Rhinella
marina. This includes numerous endemic and endangered species. The mechanism
by which the toxin acts upon organisms has been previously identified via the study
of toxin resistant versus toxin non-resistant taxa. Specific amino acid substitutions
are required on the organism’s Na+/K+–ATPase for them to be resistant to bufonid
toxin. This solution to combat the toxin is widely consistent across taxa providing a
method to discover and predict toxin resistance or vulnerability. Here I investigate
the Na+/K+–ATPase gene to detect vulnerability of a selection of Malagasy fauna to
the toxics of Duttaphrynus melanostictus. It is discovered that no tested species on
Madagascar have the capacity to survive ingestion of the novel toxin. The
vulnerability is found in all examined species, including snakes, frogs, lizards, lemurs
and tenrecs. The results suggest that the invasive Duttaphrynus melanostictus is
liable to have significant impact on Malagasy fauna.
... Hibernation is also found in basal mammals including the echidna, some marsupials, and afrotherians like the elephant shrew, golden moles and tenrecs (Ruf and Geiser, 2015;Scantlebury et al., 2008). All five spiny tenrec species, including the focus of this work, T. ecaudatus, are known to hibernate (Stephenson and Racey, 1994). The limited data on hibernating T. ecaudatus demonstrate that T b follows soil temperature for the duration of the hibernation season with no evidence of brief periods of euthermy between bouts of torpor . ...
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 Tbs of 28°C. During the active season, oxygen consumption may vary 25-fold with little or no changes in Tb During the Austral winter, tenrecs are consistently torpid but the depth of torpor may be variable. 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 to 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.
A variety of responses to climate seasonality have evolved by small mammals, including adjustments of the basal rate of metabolism (BMR) and the use of daily or seasonal torpor (here referred to as short-bout and long-bout torpor). The seasonal variation of their BMR is known to depend mainly on the concurrent variation of body mass, but it should also be affected by structural and functional changes occurring within the body that could depend on the expression of torpor. Thus it was hypothesized that BMR seasonality is related to the expression of torpor at an interspecific level. Seasonal BMR and body mass data were gathered from the literature and phylogenetic comparative analyses were done to test this hypothesis among mammals of less than 1 kg. BMR seasonality (dBMR) was quantified as the log-transformed ratio of the mean whole-animal BMR reported for the period P2 (autumn-winter) over that for the period P1 (spring-summer). Predictors were the seasonal body mass adjustment (dm), mean body mass (m) and torpor expression (TO, a three-level factor: no torpor, short-bout torpor, long-bout torpor). The seasonal variation of BMR was significantly related to dm but also to. Accounting for dm, species expressing long-bout torpor, but not those entering short-bout torpor, collectively exhibited a lower dBMR than species not entering torpor. Fat storage and use by species entering long-bout torpor, alone, could not explain their lower dBMR, as the TO:dm interaction was not significant. The low dBMR of species entering long-bout torpor may result from their collective tendency to down-regulate more strongly costly visceral organs during P2. The dBMR of the different TO categories overlapped appreciably, which highlights our still limited knowledge of the BMR seasonality among small mammals.
The emergence of the genus Homo is widely linked to the colonization of 'new' highly seasonal savannah habitats. However, until recently, our understanding of the possible impact of seasonality on this shift has been limited because we have little general knowledge of how seasonality affects the lives of primates. This 2005 book documents the extent of seasonality in food abundance in tropical woody vegetation, and then presents systematic analyses of the impact of seasonality in food supply on the behavioural ecology of non-human primates. Syntheses in this volume then produce broad generalizations concerning the impact of seasonality on behavioural ecology and reproduction in both human and non-human primates, and apply these insights to primate and human evolution. Written for graduate students and researchers in biological anthropology and behavioural ecology, this is an absorbing account of how seasonality may have affected an important episode in our own evolution.
Mammalian heterotherms, species that employ short or long periods of torpor, are found in many different climatic regions. Although the underlying physiological mechanisms of heterothermy in species from lower latitudes (i.e., the tropics and southern hemisphere) appear analogous to those of temperate and arctic heterotherms, the ultimate triggers and resulting patterns of energy expenditure and body temperature are often noticeably different. Phenotypic flexibility in the patterns of thermoregulation in non-Holarctic species can be extensive (depending on body condition, environmental parameters and species competition) and the factors responsible for inducing heterothermy are more variable in non-Holarctic species. As well as being a regular adaptation to seasonality, heterothermy can also be employed as a response to unpredictability in environmental parameters and as a response to emergency situations. Non-Holarctic heterotherms also challenge the notion that regular inter-bout arousals during hibernation are obligatory and suggest all that is necessary to maintain proper functioning during hibernation is an occasional passive return to—or maintenance of—a relatively high body temperature. The study of non-Holarctic heterotherms has led to the conclusion that heterothermy must be defined on the basis of mechanistic, physiological parameters, and not solely by body temperature; yet we are still limited in our abilities to record such mechanistic parameters in the field. It is now believed that homeothermy in mammals evolved in hot climates via an ancestral heterothermic state. Similar to extant warm-climate heterotherms, early mammals could have relied mainly on passive body temperature regulation with a capacity for short- to longer-term up-regulation of metabolism when needed. Hibernation, as seen in temperate and arctic species may then be a derived state of this ancestral heterothermy, and the study of torpor in warm climates can provide potential models for the energetics of early mammals.
As predicted by sexual selection theory, males are larger than females in most polygynous mammals, but recent studies found that ecology and life history traits also affect sexual size dimorphism (SSD) through evolutionary changes in either male size, female size, or both. The primates of Madagascar (Lemuriformes) represent the largest group of mammals without male-biased SSD. The eco-evo-devo hypothesis posited that adaptations to unusual climatic unpredictability on Madagascar have ultimately reduced SSD in lemurs after dispersing to Madagascar, but data have not been available for comparative tests of the corresponding predictions that SSD is also absent in other terrestrial Malagasy mammals and that patterns of SSD changed following the colonization of Madagascar. We used phylogenetic methods and new body mass data to test these predictions among the four endemic radiations of Malagasy primates, carnivorans, tenrecs, and rodents. In support of our prediction, we found that male-biased SSD is generally absent among all Malagasy mammals. Phylogenetic comparative analyses further indicated that after their independent colonization of Madagascar, SSD decreased in primates and tenrecs, but not in the other lineages or when analyzed across all species. We discuss several mechanisms that may have generated these patterns and conclude that neither the eco-evo-devo hypothesis, founder effects, the island rule nor sexual selection theory alone can provide a compelling explanation for the observed patterns of SSD in Malagasy mammals.
Since the time of Charles Dar win, com par a-tive bi ol ogy has been pre oc cu pied with de scrib-ing the evo lu tion ary his tory of or gan isms. This pro gram has re quired a search for char ac ters that are suf fi ciently "con ser va tive" to re flect an-ces try and not so mal lea ble that they re flect the con di tions in the en vi ron ment that spe cies face. [1] Acta Theriologica 51 (2): 000-000, 2006.. 2006. The evo lu tion of energetics in eutherian "insectivorans": an al ter nate ap proach. Acta Theriologica 51: 113-000. An anal y sis of stan dard energetics in 57 spe cies of "insectivorans", small eutherians that pref er en tially feed on soil in ver te brates, in di cated that a com bi na tion of cli mate, the use of tor por, sub strate, food hab its, and log 10 body mass ac counted for 92.5% of the vari a tion in log 10 basal rate of me tab o lism in insectivorans, whereas log 10 body mass alone ac counted for 76.7% of the vari a tion. With the ad di tion of subfamily af fil i a tion, this anal y sis ac counted for 95.5% of the vari a tion in log 10 basal rate, the most dis tinc tive subfamilies be ing Soricinae and the Talpinae, which have equally high basal rates. Sorex spe cies have basal rates that av er age 2.5 times those of trop i cal crocidurines, re flect ing an ap proach by Sorex to life in cold cli mates that does not in clude the use of tor por, a strat a gem widely used by crocidurines in warm-tem per ate and trop i cal cli mates. The ab sence of tor por in Sorex may fa cil i tate a high re pro duc tive rate through a high basal rate of me tab o lism, a com bi na tion that may be in com pat i ble with a small mass, in sec tiv o rous food hab its, and life in the low land trop ics, but re quired in cold-tem per ate en vi ron ments. Insectivorans other than shrews, moles, and cold-tem per a ture hedge hogs have low basal rates prin ci pally in as so ci a tion with trop i cal dis tri bu tions and the use of tor por. Basal rate of me tab o lism in insectivorans also cor re lated with or di nal, fa mil ial, subfamilial, and tribal af fil i a tions. The sug ges tion that phy log eny is an im por tant de ter mi nant of per for mance char ac ters like rate of me tab o lism ig nores the re quire ment that per for mance must be com pat i ble with con di tions in the en vi ron ment and with a spe cies' other char ac ter is tics. The prin ci pal rea son why per for mance char ac ters are cor re lated with tax o nomic af fil i a tion is that many clades con sist of spe cies that share a com mon ap proach to the en vi ron ment. Thus, clades not only rep re sent evo lu tion ary his to ries, they also are crude mea sures of phys i o log i cal and be hav ioral per for mances. De part ment of Zo ol ogy, Uni ver sity of Florida, Key words: Afrotheria, basal rate of me tab o lism, body tem per a ture, cli mate, Lipotyphla, food hab its, hab i tat, phy log eny, tor por
Over a 2½-yr period, the effects of season and food availability on daily torpor patterns were compared in wild-caught members of two southeastern species of Peromyscus with different elevational distributions. Animals were housed in large outdoor cages either in the mountains (P. maniculatus nubiterrae, n = 59) or in the foothills (P. leucopus leucopus, n = 52), and were continuously monitored biotelemetrically. All mice received food and water ad lib. for 2 wk, followed by a short period (4-6 days) of food restriction (75% of daily ration). The highest incidence of spontaneous torpor in each species occurred during winter and in the presence of lower . No interspecific differences in the frequency, mean duration, and mean minimum of spontaneous torpor bouts were found in any season. Food restriction increased the incidence of torpor in both species. However, the montane P. maniculatus were more likely to enter torpor in response to food restriction, and torpor episodes in this species were longer than those displayed by its lowland congener. These findings imply that mice living in the more stressful montane environment may be subjected to greater selection for the use of torpor as a survival mechanism to counter short-term starvation pressure.
Short-day (9 light:15 dark), cold-acclimated Peromyscus leucopus known to enter torpor (no. = 24) and P. leucopus never observed in torpor (no. = 12) were compared with and without a 5-g nest at 13, 7, and 1 C over 9 wk. Oxygen consumption and body temperature were monitored approximately hourly for 2-3 days under each treatment. A second group of short-day, cold-acclimated mice (13 torpid and 14 nontorpid) were monitored for oxygen consumption with and without a 5-g nest at 13 C, first individually and 10 days later as huddles of three. For individual mice, the time required to enter torpor (3.0-4.5 h), duration of torpor (4-5 h), and minimum body temperature during torpor (21-23 C) remained fairly constant at different ambient temperatures. The metabolic rate [cm³O₂/(g · h)] necessary to maintain minimum body temperature during torpor without a nest was 2.1 at 13, 3.0 at 7, and 3.7 at 1 C, while metabolic rates during the normothermic period at these temperatures were 4.8, 5.5, and 6.7, respectively. A similar trend, but with lower values, occurred with a nest. Without a nest, torpid mice had a mean daily metabolic rate which was 20% less at 13, 21% at 7, and 9% at 1 C than the corresponding value of nontorpid animals. Torpid mice with a 5-g nest reduced metabolic rate at those temperatures by 43%, 44%, and 34%, respectively, relative to nontorpid mice without a nest. Daily torpor and huddling together provided a 58% energetic saving at 13 C relative to individually housed, nontorpid mice. The addition of a nest fostered a 74% daily energy savings versus nontorpid, individual mice without a nest.
This study compared the effects of photoperiod and temperature on populations of Peromyscus leucopus from two different latitudes. Laboratory-reared mice which were descendants of Connecticut (CT) or Georgia (GA) wild-caught animals were exposed to either a long (16L:8D) or short (9L:15D) photoperiod for 12 wk. All mice were kept at 23 C for the first 6 wk, then half of each group was exposed to 13 C for the remaining 6 wk. Nesting was assessed during week 10 and spontaneous torpor during weeks 11-12. At the end of week 12, all mice were killed and examined for the presence of winter pelage. Testicular index, testes weight, seminal vesicle weight, spermatogenic index in males, and reproductive tract weight and follicular index in females were determined. Short days caused gonadal involution, molts to winter pelage, and torpor at both temperatures in CT mice. In contrast, the majority of GA mice remained reproductively competent, and thermoregulatory adjustments were less pronounced. At 23 C, short-day exposed GA mice did not become torpid, and only one animal (6%) molted. AT 13 C 27% of the GA short-day animals entered torpor and 20% molted. Nesting was increased by both short days and cold in CT mice, but only by cold in GA mice. These results indicate that in P. leucopus there is considerable intraspecific variation in the use of photoperiod and temperature as environmental cues.
This chapter discusses the concept of hibernation in mammals. Many of the so-called hibernators do not encounter very low ambient temperatures because they can retreat to microenvironments where very low ambient temperatures are not encountered or they live in regions of moderate climate. Some of these species are diurnal, and they are confronted with problems of high ambient temperature where water is also limited. If any of these species are seldom seen during the hot, dry periods, it is frequently assumed they are dormant. Such species have been called estivators. The only example of a mammal torpid exclusively during the hot, dry period with the dormancy thought to be induced directly as a result of high water shortage is the white-footed mouse Peromyscus eremicus. Many small mammals lower their body temperature for short periods of time, in some cases spontaneously and in others as a consequence of food deprivation and can spontaneously return to normothermic temperature levels. There is considerable variation in depth to which they permit their body temperatures to drop. Some of these species also hibernate. Heterothermy has often been used to describe the wide fluctuations in body temperature, which may be a kind of daily torpor. The wide spectrum of physiological features among various types of hibernators reflect the habitat to which the species is adapted, and in view of the difficulty of delineating hibernation, estivation, and daily torpor, it is useful to use a more general term such as torpidity.
Over a territory of 587,000 square kilometres with a north-south extension of over 1500 km, with physical features comprising low-lying coastal plains, mountains exceeding 2500 metres in height and areas of medium altitude ranging between 800 and 1500 metres closely juxtaposed, it will be readily understood that wide climatic diversity can exist. Of course, by virtue of its position, Madagascar is dominated by tropical weather features, the major influence being the trade wind. However, the island is also the meeting place, and hence the point of conflict, of various influences, some originating from low latitudes and others from the temperate and subpolar regions. The interplay of the large peripheral centres of action and the character of the air masses traversing the country are profoundly disturbed by the geographical conditions of the country. It is necessary to examine the climatic mechanisms from this viewpoint before embarking on a study of the regional differences. This study will illustrate the great diversity of climates, a diversity which is evident as much in the context of a separative analysis of the fundamental meteorological elements as in that of an attempt at an overall synthesis of these elements to give a true picture of the climate through the seasons.