Costs of anorexia during pregnancy in a viviparous snake (Vipera aspis)

Spontaneous anorexia has been documented in various animal species and is usually associated with activities competing with food intake. In natural conditions, most female aspic vipers (Vipera aspis) stop feeding during the two months of pregnancy. We carried out a simple experiment on 40 pregnant females to determine whether anorexia was obligatory or facultative, and to investigate the energetic consequence of fasting on post-partum body condition and litter traits. Three diet treatments were applied during gestation: no food, one feeding occasion, and two feeding occasions. Twelve nonpregnant, unfed females were used as a control group. Most gravid females accepted captive mice during gestation, suggesting that anorexia reported in the field was a side effect of the tremendous changes in activity pattern associated with pregnancy. Mass loss was high for unfed reproductive females, indicating high energy expenditure associated with embryo maintenance. Prey consumption allowed compensation for metabolic expenditure and enhanced post-partum female body condition, but had no effects on litter characteristics. The magnitude of the metabolic expenditure during gestation appeared to be independent of fecundity.     

The effect of social context and reproductive status on the metabolic rates of dwarf seahorses (Hippocampus zosterae).

Although we are beginning to understand the conditions in which monogamy is favored over a more promiscuous lifestyle, little is known about the proximate effects of monogamous pair bonding, and subsequent reproduction, on general metabolism. I determined the effects of these factors on the metabolic rates of dwarf seahorses (Hippocampus zosterae), recognized for their monogamous lifestyle and unique male care of offspring, in a sealed brood pouch where embryos develop until birth. Resting routine oxygen consumption rates were measured in newly-paired and reproductive adults using a continuous flow respirometer, and then compared to metabolic rates of sexually-isolated fish. Sex differences were observed in the relationship between log(10)mass and log(10)oxygen consumption, with pair-bonded females exhibiting a significantly higher slope than either pair-bonded males, or sexually-isolated fish. Mass-specific metabolic rates in sexually-isolated fish were 15% higher than in pair-bonded fish, indicating that social conditions can strongly influence metabolic rate. Specific metabolic rates only differed by gender during male pregnancy, when male metabolic rate increased from 10 to 52% over pre-gravid levels. A male's developing brood only explained 4-31% of this increase, suggesting that increased metabolic demands on fathers accounts for most of the increase in metabolic rate during gestation. This study suggests that pair bonding can strongly affect the general metabolism of organisms, with potential differences between males and females that increase with age.     

Climate affects embryonic development in a viviparous snake, Vipera aspis

Climatic conditions during embryonic development can exert profound and long-term effects on many types of organisms, but most previous research on this topic has focussed on endothermic vertebrates (birds and mammals). Although viviparity in ectothermic taxa allows the reproducing female to buffer ambient thermal variation for her developing offspring, even an actively thermoregulating female may be unable to provide optimal incubation regimes in severe weather conditions. We examined the extent to which fluctuations in natural thermal conditions during pregnancy affect reproduction in a temperate viviparous snake, the aspic viper (Vipera aspis). Data gathered from a long term field study demonstrated that ambient thermal conditions influenced (1) female body temperatures and (2) gestation length, embryo viability, and offspring phenotypes. Interestingly, thermal conditions during each of the three months of gestation affected different aspects of reproduction. Hotter weather early in gestation (June) increased ventral scale counts (=number of body segments) of neonates; hotter weather mid-gestation (July) hastened development and thus the date of parturition; and hotter weather late in gestation (August) reduced the incidence of stillborn neonates. The population that we studied is close to the northern limit of the species' range, and embryonic thermal requirements may prevent Vipera aspis from extending into cooler conditions further north.     

Bioenergetics of reproduction and pup development in a subterranean rodent (Ctenomys talarum)

The objective of this study was to evaluate the maternal costs of reproduction and pup development in the subterranean rodent Ctenomys talarum (Thomas 1898). Statistical differences were detected in whole-animal metabolic rates between nonreproductive and pregnant or lactating females. Whole-animal metabolic rates during pregnancy and lactation were 128% and 151% of the resting metabolic rate (RMR) observed in nonreproductive females. The total additional energy cost of reproduction (above the nonreproductive level) was similar for both the gestation and lactation periods. Mass-specific RMR revealed an upregulation of cell or tissue metabolism during lactation but not during gestation. The mass-specific metabolic rate of pups was 237% of the adults' metabolic rates. No differences were observed in body temperature among nonreproductive, pregnant, or lactating females. No differences were detected in body mass at birth among pups from litters with different numbers of nestlings. Pups increased their body temperature, reaching adult temperature at 30 d of age, when they were near weaning. Milk constituted the exclusive food for pups until they started eating solid food at 10 d old. Suckling time decreased with age of pups, and at the same time, mother chases directed toward their pups increased. These reproductive characteristics may contribute to successful existence in a subterranean habitat.     

Oxygen consumption of gestating femaleSebastes schlegeli: Estimating the reproductive costs of livebearing

Synopsis During gestation, live-bearing fishes incur physiological energy costs, including provision of energy and respiratory gases to the developing embryos and removal of waste products. Fecundity in the genusSebastes is high, and the ovaries represent a significant portion of the weight of gestating females. In this study, we compare oxygen consumption of gestating females with non-gestating females and males of kurosoi,Sebastes schlegeli, to estimate these costs. Oxygen consumption by pregnant females is significantly higher than that of males and immature females at similar sizes and weights. We estimate that a 1.5 kg gestating female consumes 68% more oxygen than a non-gestating fish during the 51.5-day period of gestation. Such an increase in oxygen consumption rates may have important implications to the metabolic scope of gestating alone, suggesting that costs of increased gill ventilation, ionic and osmotic regulation and cardiac output are relatively high. Such energetic costs represent a quantifiable expense of the viviparous mode of reproduction inSebastes as compared with oviparous species.     

Influence of pregnancy on locomotor and feeding performances of the skink, Mabuya multifasciata: why do females shift thermal preferences when pregnant?

It has been documented in the many-lined sun skink (Mabuya multifasciata) that pregnant females select lower body temperatures (27.6–30.8 °C) than do nonpregnant females and adult males (29.7–35.7 °C). We therefore used the skink to test the hypothesis that the maximization of reproductive benefits should be achieved in pregnant females by shifting thermal preferences towards the levels optimal for embryonic development but entailing relatively small costs of reproduction. Data on adult males showed that temperatures maximizing swimming stamina (indicative of locomotor endurance) fell within the range of body temperatures selected by nonpregnant females and adult males. Data on swimming stamina and feeding performance of pregnant females, nonpregnant females and adult males measured at 26 and 30 °C showed that: (1) pregnancy impaired locomotor and feeding performances, but such impairments did not persist after parturition; (2) the degree of locomotor impairment during pregnancy was greater at 26 °C than at 30 °C, but the degree of feeding impairment during pregnancy was greater at 30 °C than at 26 °C. Pregnant females of M. multifasciata selecting body temperatures at about 29 °C could not only produce good-quality offspring in a relatively short gestation length but also reduce reproductive costs associated with locomotor and feeding impairments to some extent. Thus, data from M. multifasciata validate the above hypothesis.     

The Effect of Gestational State on Oxygen Consumption and Response to Hypoxia in the Sailfin Molly, Poecilia latipinna

Metabolic activity in livebearing fishes increases with embryonic development so that embryos prior to parturition may have a higher mass-specific oxygen requirement than maternal tissues, temporarily increasing the total routine oxygen requirement of the female. We examined whether females of the livebearing poeciliid Poecilia latipinna (sailfin molly) increase their routine metabolic oxygen consumption during development of their broods. We also quantified effects of gestation on time allocation to aquatic surface respiration (ASR) under hypoxic conditions. Mass-adjusted routine metabolic rate (RMR) of female mollies showed a significant increase during late gestation. The RMR of males did not differ from females that were in their early or mid stage of gestation, but was lower than females in late gestation. Gestating females spent approximately 27% more time conducting ASR than non-gestating females when exposed to chronic hypoxia (1mgl^–1), further supporting a brood-related increase in oxygen demand. Increased time allocation to ASR may directly affect maternal predation risk in low-oxygen conditions.     

Experimental litter size reduction reveals costs of gestation and delayed effects on offspring in a viviparous lizard

Experimental studies have often been employed to study costs of reproduction, but rarely to study costs of gestation. Disentangling the relative importance of each stage of the reproductive cycle should help to assess the costs and benefits of different reproductive strategies. To that end, we experimentally reduced litter size during gestation in a viviparous lizard. We measured physiological and behavioural parameters during gestation and shortly after parturition, as well as survival and growth of females and their offspring. This study showed four major results. First, the experimental litter size reduction did not significantly affect the cellular immune response, the metabolism and the survival of adult females. Second, females with reduced litter size decreased their basking time. Third, these females also had an increased postpartum body condition. As postpartum body condition is positively related to future reproduction, this result indicates a gestation cost. Fourth, even though offspring from experimentally reduced litters had similar weight and size at birth as other offspring, their growth rate after birth was significantly increased. This shows the existence of a maternal effect during gestation with delayed consequences. This experimental study demonstrates that there are some costs to gestation, but it also suggests that some classical trade-offs associated with reproduction may not be explained by gestation costs.     

Serum 17,20 beta-dihydroxy-4-pregnen-3-one Levels in pregnant and non-pregnant female rockfish, Sebastes schlegeli, viviparous teleost, and its production by post-ovulatory follicles

Changes in serum 17 alpha,20 beta-dihydroxy-4-pregnen-3-one (17,20 beta-DP) levels around the gestation time of normal pregnant and experimentally non-pregnant females were investigated in the black rockfish, Sebastes schlegeli, a viviparous teleost. The serum 17,20 beta-DP in both females showed similar changes and levels, increasing from the early to late gestation periods and declining just before parturition in pregnant females and egg-release in non-pregnant females, respectively. These results suggest that the maintenance of high serum levels of 17,20 beta-DP after oocyte maturation is not correlated with gestation or parturition, but occurs spontaneously in this species. The decline of 17,20 beta-DP levels prior to egg-release in non-pregnant females tended to occur one week earlier than those prior to parturition in pregnant females, suggesting that both a decline in 17,20 beta-DP levels in mothers and some response from embryos are needed for a smooth parturition. The post-ovulatory follicles were maintained throughout the gestation period and produced a considerable amount of 17,20 beta-DP in vitro (3.44-6.96 pg/ml/mg tissue), but little estradiol-17beta (0.92-1.66 pg/ml/mg tissue). The production of 17,20 beta-DP tended to be enhanced by the addition of a precursor steroid, pregnenolone, in the pre-, early and mid-gestation periods. These results strongly suggest that the follicle cells in black rockfish have the ability to synthesize 17,20 beta-DP during the post-ovulatory period, and high serum 17,20 beta-DP during gestation is supplied by the post-ovulatory follicles, which in Sebastes are considered to be functionally homologous to the mammalian corpus luteum.     

Factors Affecting Date of Implantation,Parturition, and Den Entry Estimated from Activity and Body Temperature in Free-Ranging Brown Bears

Knowledge of factors influencing the timing of reproduction is important for animal conservation and management. Brown bears (Ursus arctos) are able to vary the birth date of their cubs in response to their fat stores, but little information is available about the timing of implantation and parturition in free-ranging brown bears. Body temperature and activity of pregnant brown bears is higher during the gestation period than during the rest of hibernation and drops at parturition. We compared mean daily body temperature and activity levels of pregnant and nonpregnant females during preimplantation, gestation, and lactation. Additionally we tested whether age, litter size, primiparity, environmental conditions, and the start of hibernation influence the timing of parturition. The mean date of implantation was 1 December (SD = 12), the mean date of parturition was 26 January (SD = 12), and the mean duration of the gestation period was 56 days (SD = 2). The body temperature of pregnant females was higher during the gestation and lactation periods than that of nonpregnant bears. The body temperature of pregnant females decreased during the gestation period. Activity recordings were also used to determine the date of parturition. The parturition dates calculated with activity and body temperature data did not differ significantly and were the same in 50% of the females. Older females started hibernation earlier. The start of hibernation was earlier during years with favorable environmental conditions. Dates of parturition were later during years with good environmental conditions which was unexpected. We suggest that free-ranging pregnant brown bears in areas with high levels of human activities at the beginning of the denning period, as in our study area, might prioritize investing energy in early denning than in early parturition during years with favorable environmental conditions, as a strategy to prevent disturbances caused by human.     

The tradeoff between torpor use and reproduction in little brown bats (Myotis lucifugus)

In mammals, reproduction, especially for females is energetically demanding. Therefore, during the reproductive period females could potentially adjust patterns of thermoregulation and foraging in concert to minimise the energetic constraints associated with pregnancy and lactation. We assessed the influence of pregnancy, lactation, and post-lactation on torpor use and foraging behaviour by female little brown bats, Myotis lucifugus. We measured thermoregulation by recording skin temperature and foraging by tracking bats which carried temperature-sensitive radio-tags. We found that individuals, regardless of reproductive condition, used torpor, but the patterns of torpor use varied significantly between reproductive (pregnant and lactating) females and post-lactating females. As we predicted, reproductive females entered torpor for shorter bouts than post-lactating females. Although all females used torpor frequently, pregnant females spent less time in torpor, and maintained higher skin temperatures than either lactating or post-lactating females. This result suggests that delayed offspring development which has been associated with torpor use during pregnancy, may pose a higher risk to an individual’s reproductive success than reduced milk production during lactation. Conversely, foraging behaviour of radio-tagged bats did not vary with reproductive condition, suggesting that even short, shallow bouts of torpor produce substantial energy savings, likely obviating the need to spend more time foraging. Our data clearly show that torpor use and reproduction are not mutually exclusive and that torpor use (no matter how short or shallow) is an important means of balancing the costs of reproduction for M. lucifugus.     

Reproductive biology of the mosquitofish in a permanent natural lagoon in south-west Spain: two tactics for one species

Introduced Gambusia holbrooki in a natural lagoon of southern Spain consisted of two age groups: 1992 cohort, 7-11 months old and 1993 cohort, <4 months old. In the 1992 cohort, females grew even during the gestation period at about 0·30 mm day^-1. In the 1993 cohort, females displayed a high growth rate (0·55 mm day^-1) and reached reproductive size in a few weeks, but stopped growing when they matured. All the 1992 cohort reproduced from mid-May to mid-June, but only 50% of the 1993 cohort reproduced, from mid-August to mid-September. Reproducing females were significantly larger in the 1992 cohort (39·8 mm) than in the 1993 one (34·8 mm). The largest 1992 females cohort had reproduced previously; the 1993 cohort had not. The mean dry weight of intra-ovarian embryos decreased to a minimum immediately before birth. These metabolic costs represented 29·8 and 31·4% of the initial weights of the 1992 and 1993 embryos, respectively. Mean dry weight of full-term embryo was significantly higher in the 1992 cohort (0·80 ± 0·129 mg; 95% CL) than in the 1993 one (0·70 ± 0·086 mg; 95% CL). With more females in 1992, cohort fecundity was considerably higher (number of embryos=7151; 63%) than in the 1993 (4193; 37%) cohort. The population completed two generations each year (spring and summer). The spring stock grew slower than the summer one but continued to grow during the gestation period, reaching larger final lengths, with more synchronous reproduction and clearer evidence of a second reproductive event. Each reproductive stock displayed its own life-history characteristics, with significant differences between mean length of reproducing females, growth rate, mean brood size, offspring size, standard fecundity and minimum length at reproduction.     

Metabolic costs of viviparity in yellowtail rockfish,Sebastes flavidus

Synopsis We estimated the energy utilized by developing embryos and larvae of yellowtail rockfish,Sebastes flavidus, by determining the routine metabolic rate of adult females throughout gestation and subtracting the mean metabolic rate of non-gestating fish. The pattern of maternal oxygen consumption during gestation was such that metabolic demands did not become significantly elevated until intra-ovarian embryos had hatched and larvae were being incubated (i.e. 24–28 d post-fertilization). Metabolic rates of females in this latter stage of gestation were 82% higher than spent females and 101% higher than those of non-reproductive males. We determined that 0.08996 cal embryo^-1 was consumed during gestation as compared to the change in energy content of embryos from fertilization to birth which was 0.08690 cal embryo^-1. The difference between the energy consumed and the energy lost during the 29 d gestation period indicated that extra embryonic sources contributed only 3.4% or 0.00306 cal embryo^-1 of the energy utilized after fertilization. Our observations agree with previous work which determined that embryos and larvae ofS. flavidus are primarily lecithotrophic and that the relatively high fecundity ofS. flavidus coupled with a small egg size, rapid embryogenesis and brief gestation period characterize this species as a relative r-strategist within a genus whose species range broadly over the K end of the r-K continuum.     

The energy costs of sexual dimorphism in mole-rats are morphological not behavioural

Different reproductive strategies of males and females may lead to the evolution of differences in their energetic costs of reproduction, overall energetic requirements and physiological performances. Sexual dimorphism is often associated with costly behaviours (e.g. large males might have a competitive advantage in fighting, which is energetically expensive). However, few studies of mammals have directly compared the energy costs of reproductive activities between sexes. We compared the daily energy expenditure (DEE) and resting metabolic rate (RMR) of males and females of two species of mole-rat, Bathyergus janetta and Georychus capensis (the former is sexually dimorphic in body size and the latter is not) during a period of intense digging when males seek females. We hypothesized that large body size might be indicative of greater digging or fighting capabilities, and hence greater mass-independent DEE values in males of the sexually dimorphic species. In contrast to this prediction, although absolute values of DEE were greater in B. janetta males, mass-independent values were not. No differences were apparent between sexes in G. capensis. By comparison, although RMR values were greater in B. janetta than G. capensis, no differences were apparent between the sexes for either species. The energy cost of dimorphism is most likely to be the cost of maintenance of a large body size, and not the cost of behaviours performed when an individual is large.     

Energy consumption by embryos of a viviparous lizard, Eulamprus tympanum, during development

Energy consumption during development has been measured in many oviparous lizards, but not in viviparous lizards in utero. It has always been assumed that energy consumption by embryos of viviparous lizards during development is similar to that of oviparous species. Estimation of energy consumption of viviparous lizards in vivo are confounded by the possible influence of pregnancy on maternal metabolism. Here we separated maternal and embryonic metabolism in measurements of pregnant Eulamprus tympanum throughout pregnancy. Our data support the hypothesis that the energetic cost of development in viviparous lizards (19.8 kJ g(-1)) is similar to that in oviparous lizards (mean 16.2 kJ g(-1)), at least for a species with a simple placenta. An increase in maternal metabolism of 29% above that for non-pregnant E. tympanum goes to maintain pregnancy, and represents an important component of the reproductive effort in E. tympanum.     

Breathing with big babies: ventilation and oxygen consumption during pregnancy in the lizard Tiliqua rugosa

We determined the effects of high gestational loads on ventilation and the rate of oxygen consumption (VO2) in the scincid lizard Tiliqua rugosa. Tiliqua rugosa is a large viviparous lizard that gives birth to one to four young after 6-7 mo gestation. Pregnant females gave birth to large young, weighing 89.5+/-5.9 g, which represents 21.6%+/-2.6% of maternal body mass. As the embryos developed, they occupied an increasingly large proportion of the body cavity, decreasing food consumption and compressing the gastrointestinal tract. Computerized axial tomography scans demonstrated that the lungs were compressed and/or regionally collapsed by the developing embryos, potentially compromising ventilation. Both minute ventilation (VE) and tidal volume decreased as gestation progressed, but no compensatory changes in breathing frequency or in the duration of the nonventilatory period were observed. The total rate of VO2, consisting of contributions from both maternal and fetal tissues, did not change during gestation, suggesting that maternal VO2 decreases as fetal VO2 increases. Pregnant females demonstrated a decreased ventilatory response to increased respiratory drive (triggered via inhalation of hypoxic hypercapnic gas), which may be associated with the increased energetic cost of ventilating a compressed lung or the desensitization of chemoreceptors during gestation. The decreased ability of the respiratory system to respond to increased respiratory drive may have important consequences for locomotor performance and predator avoidance in pregnant lizards.     

Stress and the pregnant female: Impact on hippocampal cell proliferation, but not affective-like behaviors

Fifteen percent of women worldwide develop postpartum depression; however, many women also suffer from mood disorders during pregnancy. Our knowledge of how these stress-related disorders affect the neurobiology of the mother is very limited. In animal models, depressive-like behavior is often associated with repeated stress and alterations in adult neurogenesis in the hippocampus. However, research has yet to investigate the effect of stress on affective-like behavior and hippocampal neurogenesis in the pregnant female. The aim of the present study was to determine whether stress during gestation alters affective-like behaviors, corticosterone levels, and hippocampal cell proliferation and new cell survival in the pregnant female, and whether these effects differ from virgin females. Age-matched pregnant and virgin Sprague-Dawley rats were divided into two conditions: 1) stress and 2) control. Females in the stress condition were repeatedly restrained during gestation, and at matched time points in virgin females. Affective-like behaviors were assessed at the end of gestation, and at matched time points in virgin females. Results demonstrate that regardless of repeated restraint stress, pregnant females have increased anxiety-like behavior, decreased depressive-like behavior, and lower corticosterone levels, compared to non-stressed, and at times stressed, virgin females. In addition, stressed virgin females have lower levels of depressive-like behavior compared to control virgin females. Interestingly, hippocampal cell proliferation was increased in both virgin and pregnant females after stress. Understanding how stress affects the female during different reproductive states will aid in improving the health and well being of the mother and child.     

Delayed parturition: constraint or coping mechanism in a viviparous gekkonid?

The extended gestation of fully developed embryos in viviparous reptiles can be the consequence of a lack of appropriate environmental conditions and/or an adaptive contribution to increased offspring viability. I examined the cause and effects of extended gestation in a gekkonid lizard Hoplodactylus maculatus , which delays parturition of developed embryos for up to 9 months from autumn into a second spring. Comparisons of microhabitat temperatures showed that thermal opportunities were equally conducive to birth in autumn and spring. The responsiveness of females to a hormonal stimulant for parturition also did not differ between these seasons. Multiple offspring traits were measured, including body size, locomotory ability and lipid reserves, and were found not to increase with extended gestation. Incorporating these results with previously published evidence for microhabitat thermal variation, I discuss whether delayed parturition may be an adaptive mechanism maintained by the selective pressures of an uncertain thermal environment on components of reproduction, including vitellogenesis, maternal birthing cues and neonatal survival.     

Bioenergetic components of reproductive effort in viviparous snakes: costs of vitellogenesis exceed costs of pregnancy

Reproductive effort has been defined as the proportion of an organism's energy budget that is allocated to reproduction over a biologically meaningful time period. Historically, studies of reproductive bioenergetics considered energy content of gametes, but not costs of gamete production. Although metabolic costs of vitellogenesis (MCV) fundamentally reflect the primary bioenergetic cost of reproductive allocation in female reptiles, the few investigations that have considered costs of reproductive allocation have focused on metabolic costs of pregnancy (MCP) in viviparous species. We define MCP as energetic costs incurred by pregnant females, including all costs of maintaining gestation conditions necessary for embryogenesis. MCP by our definition do not include fetal costs of embryogenesis. We measured metabolic rates in five species of viviparous snakes (Agkistrodon contortrix, Boa constrictor, Eryx colubrinus, Nerodia sipedon, and Thamnophis sirtalis) during vitellogenesis and pregnancy in order to estimate MCV and MCP. Across all species, MCV were responsible for 30% increases in maternal metabolism. Phylogenetically-independent contrasts showed that MCV were significantly greater in B. constrictor than in other species, likely because B. constrictor yolk energy content was greater than that of other species. Estimates of MCP were not significantly different from zero in any species. In viviparous snakes, MCV appear to represent significant bioenergetic expenditures, while MCP do not. We suggest that MCV, together with yolk energy content, represent the most significant component of reptilian reproductive effort, and therefore deserve greater attention than MCP in studies of reptilian reproductive bioenergetics.     

Changes in embryonic development and hatching in Chionoecetes opilio (snow crab) with variation in incubation temperature

Water temperature affects the distribution, movement, and reproductive potential of female snow crab, Chionoecetes opilio. Ovigerous females of C. opilio from the eastern Bering Sea were held at five temperatures (-1, 0, 1, 3, and 6 degrees C) in the laboratory while their embryos developed from gastrula to hatching. The duration of incubation increased by 105 d (30%) with decreasing temperature; however, a switch to a 2-year duration of embryo incubation was not observed. For females held at 6, 3, and 1 degrees C, their embryos underwent a short period of diapause late in development; no diapause was observed for embryos of females held at 0 or -1 degrees C. Successful extrusion of a subsequent clutch and hatch timing comparable with that observed in the eastern Bering Sea indicated that temperatures of 0 to 3 degrees C may be optimal for multiparous female reproduction. We demonstrated that a switch from 1-year to 2-year reproduction cannot be triggered by changing the thermal regime after several months of embryonic development. The timing of female movement from colder to warmer waters may be important for maintaining population reproductive potential during the recent phase of warming and contraction of cold-water biomes in the Bering Sea.