Torpor in dark times: patterns of heterothermy are associated with the lunar cycle in a nocturnal bird

Many studies have shown that endotherms become more heterothermic when the costs of thermoregulation are high and/or when limited energy availability constrains thermoregulatory capacity. However, the roles of many ecological variables, including constraints on foraging opportunities and/or success, remain largely unknown. To test the prediction that thermoregulatory patterns should be related to foraging opportunities in a heterothermic endotherm, we examined the relationship between the lunar cycle and heterothermy in Freckled Nightjars (Caprimulgus tristigma), which are visually orienting, nocturnal insectivores that are dependent on ambient light to forage. This model system provides an opportunity to assess whether variation in foraging opportunities influences the expression of heterothermy. The nightjars were active and foraged for insects when moonlight was available but became inactive and heterothermic in the absence of moonlight. Lunar illumination was a much stronger predictor of the magnitude of heterothermic responses than was air temperature (T(a)). Our data suggest that heterothermy was strongly related to variation in foraging opportunities associated with the lunar cycle, even though food abundance appeared to remain relatively high throughout the study period. Patterns of thermoregulation in this population of Freckled Nightjars provide novel insights into the environmental and ecological determinants of heterothermy, with the lunar cycle, and not T(a), being the strongest predictor of torpor use.     

Long-term Population Trends in White-Footed Mice and the Impact of Supplemental Food and Shelter

Central to most models of population regulation is the ideathat the degree of intraspecific competition is in some wayproportional to the availability of limiting resources. Althoughlaboratory research has demonstrated a number of proximate mechanismsby which behavior might affect population growth, little isknown about the resources that are actually limiting populationdensity in the field or about how animals might compete forthem. Long-term field studies reveal that the white-footed mouse,Peromyscus leucopus, exhibits two types of pronounced changesin density: intra-annual (seasonal) and inter-annual. The formerseem to be due ultimately to climate and the lack of winterbreeding, but populations often decline sharply in late summerin the midst of plentiful food; fall recruitment of new animalsis density-dependent and usually poor. Differences in peak densitiesfrom one year to the next as high as 13-fold have been recorded. Weather, shelter, and food are possible ultimate limiting resources.Food has received themost attention, but supplemental feedingexperiments have yielded mixed results. A review of the socialbehavior of this polygnous species suggests that each sex islimited by different combinations of factors. Females may defenda food source and nest sites; males may search actively forfemales at low adult densities, covering large areas, and defendaccess to females at high adult densities. Additional long-term field studies are needed, both to providedirection to laboratory research on proximate mechanisms andto provide the data base for understanding the role of weather,food, and shelter as ultimate limiting factors. Enough short-termstudies have been published to permit comparisons across habitatsand through time which will give a better perspective on climateand habitat variables. Field experiments are necessary to demonstratethe operation of proximate behavioral, physiological, and geneticmechanisms of population regulation in natural populations.     

Seasonal energetic constraints in Mediterranean benthic suspension feeders: effects at different levels of ecological organization

The aim of this work is to examine the role of food as a constraining factor at different levels of ecological organization in benthic littoral ecosystems. In the search for patterns in ecological systems, it has recently been documented that seasonality in the dynamics of benthic suspension feeders (BSF) in the Mediterranean Sea is characterized by summer dormancy. We review recent studies on seston availability in the water column and feeding and respiration by BSF in the Mediterranean. The objective is to assess whether a pattern across particular studies exists that could provide evidence of food as a constraining factor. A pattern emerges from these organism‐level studies, one which indicates the seasonal occurrence of an energy shortage in the taxa exhibiting summer dormancy. This energy shortage is closely related to low food availability and suggests that an energetic constraint underlie the summer dormancy phenomenon. The seasonal occurrence of summer energy shortage also appears to affect the dynamics of BSF at population and community level. In this sense, in late summer 1999, a mass mortality event of BSF affected several hundreds of kilometers in the Ligurian Sea (NW Mediterranean). The fact that the mass mortality event occurred in late summer and especially affected the taxa that exhibit energy shortage – such as anthozoans and sponges – suggests, that energetic constraints may contribute to the understanding of the mass mortality event. The energy shortage phenomenon may provide a mechanism to understand how the occurrence of anomalous climatic conditions may have induced the mass mortality of some BSF taxa. This review points out the existence of a common energy shortage phenomenon mainly related to low food availability as an important determinant of the dynamics of most BSF taxa at organism level in the Mediterranean. But this determinant also affects the dynamics of BSF at population and community level. Therefore, the extant data point up the crucial role of food as a constraining factor for benthic littoral ecosystems in oligotrophic areas like the Mediterranean, with important seasonal variations in seston abundance and composition.     

Surviving the Cold, Dry Period in Africa: Behavioral Adjustments as an Alternative to Heterothermy in the African Lesser Bushbaby (Galago moholi)

Behavioral and physiological adaptations are common and successful strategies used by small endothermic species to adjust to unfavorable seasons. Physiological adaptations, such as heterothermy, e.g., torpor, are usually thought to be more effective energy-saving strategies than behavioral adjustments. The African lesser bushbaby, Galago moholi, is physiologically capable of torpor but expresses heterothermy only under conditions of extreme energy limitation, suggesting that it has evolved alternative strategies to compensate energetic bottlenecks. We hypothesized that Galago moholi survives the unfavorable winter period, without —or only rarely— employing torpid phases to save energy, by using behavioral thermoregulation. We compared the ecology and behavior of Galago moholi in summer and winter by telemetric tracking and examined food availability by determination of arthropod and gum availability. We found a significant increase in huddling behavior and a significant increase in the use of enclosed and insulated sleeping sites during winter, as well as a reduction in nightly activity. Galago moholi hunted for insects significantly less in winter than in summer, and increased gum intake in winter, when gum showed an increase in energy content. The availability of high-quality food, albeit in low quantities, presumably enables Galago moholi to stay normothermic throughout the cold, dry period and to focus on reproduction activities. We propose that Galago moholi favors ecological and behavioral adjustments over torpor because these are sufficient to meet energy requirements of this species, and their advantages (flexibility, unrestricted activity, and reproduction) outweigh the energetic benefits of heterothermy.     

What has stopped the cycles of sub-Arctic animal populations? Predators or food?

The populations of many species of sub-Arctic animals have recently ceased to fluctuate cyclically. The ultimate cause of this would seem to be changes in the weather, and the proximate cause has been credited to less winter snow allowing predators better access to their prey, thus enabling them to prevent surges in the prey's abundance. But there is evidence that this is not so; that, rather, the numbers of predators are limited by the abundance of their prey. Furthermore, there is alternative evidence that suggests that changes in the cyclical availability of food, brought about by changing weather conditions, may be dampening fluctuations in the abundance of these populations. On the wider ecological front, the evidence presented here further supports the commonality of how a shortage of food of a quality that can support breeding, not the action of predators, generally limits the abundance of populations of both prey and predator.     

Should I stay or should I go now? Patch use by African army ant colonies in relation to food availability and predation

Army ant colonies do not have permanent nests but frequently move to new patches. Local food depletion is considered the ultimate cause of this nomadic behaviour, but the proximate causes are not well understood. We tested if and how patch departure time of the aboveground-hunting army ant Dorylus molestus under field conditions is influenced by food availability and nest attacks by predators. In the first food supplement experiment, colonies receiving additional food throughout an entire nest stay did not reside in their nests for longer periods than control colonies. However, the distances travelled by colonies after nest stays during which colonies obtained food were shorter than those before these nest stays, indicating that colonies do assess food availability and avoid moving too far away from patches of high food availability. In the second food supplement experiment, in which colonies were given even larger amounts of food in the second half of their nest stay to mimic a rich unpredictable food source that these highly polyphagous predators are likely to encounter sometimes, patch departure times likewise did not differ between treated and control colonies. Either patch departure time is independent of food availability or there is another, as yet unappreciated proximate cause of colony movements in this species which we were unable to control for in our field experiments. One possibility is that encounters between neighbouring colonies influence patch departure time. In the experiment on the effect of predation, colonies responded to simulated nest attacks by mammals by leaving nests almost instantaneously and thus much earlier than control colonies. Rapid nest evacuation is likely a response to minimize the probability of repeat attacks by predators which cannot be repelled in other ways. Future studies will be necessary to definitively determine whether food availability influences patch departure times and to elucidate the consequences of colony encounters.     

The role of energy availability in Mammalian hibernation: a cost-benefit approach

Hibernation is widely regarded as an adaptation to seasonal energy shortage, but the actual influence of energy availability on hibernation patterns is rarely considered. Here we review literature on the costs and benefits of torpor expression to examine the influence that energy may have on hibernation patterns. We first establish that the dichotomy between food- and fat-storing hibernators coincides with differences in diet rather than body size and show that small or large species pursuing either strategy have considerable potential scope in the amount of torpor needed to survive winter. Torpor expression provides substantial energy savings, which increase the chance of surviving a period of food shortage and emerging with residual energy for early spring reproduction. However, all hibernating mammals periodically arouse to normal body temperatures during hibernation. The function of these arousals has long been speculated to involve recovery from physiological costs accumulated during metabolic depression, and recent physiological studies indicate these costs may include oxidative stress, reduced immunocompetence, and perhaps neuronal tissue damage. Using an optimality approach, we suggest that trade-offs between the benefits of energy conservation and the physiological costs of metabolic depression can explain both why hibernators periodically arouse from torpor and why they should use available energy to minimize the depth and duration of their torpor bouts. On the basis of these trade-offs, we derive a series of testable predictions concerning the relationship between energy availability and torpor expression. We conclude by reviewing the empirical support for these predictions and suggesting new avenues for research on the role of energy availability in mammalian hibernation.     

Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction?

A major challenge in biology is understanding how organisms partition limited resources among physiological processes. For example, offspring production and self-maintenance are important for fitness and survival, yet these critical processes often compete for resources. While physiological trade-offs between reproduction and immune function have been documented, their regulation remains unclear. Most current evidence suggests that physiological changes during specific reproductive states directly suppress various components of the immune system; however, some studies have not found this clear relationship. We performed two experiments in female tree lizards (Urosaurus ornatus) that demonstrate the presence of trade-offs between the reproductive and immune systems under controlled laboratory conditions. These results also support the hypothesis that these trade-offs are a facultative response to resource availability and are not obligatory responses to physiological changes during reproduction. We found that (1) experimentally increasing reproductive investment under limited resources resulted in suppressed immune function and (2) experimentally limiting resources resulted in immunosuppression but only during resource costly reproductive activities. There seems to be a critical balance of resources that is maintained between multiple processes, and changes in the balance between energy intake and output can have major consequences for immune function.     

Increased energy promotes size-based niche availability in marine mollusks

Variation in chemical energy, that is food availability, is posited to cause variation in body size. However, examinations of the relationship are rare and primarily limited to amniotes and zooplankton. Moreover, the relationship between body size and chemical energy may be impacted by phylogenetic history, clade-specific ecology, and heterogeneity of chemical energy in space and time. Considerable work remains to both document patterns in body size over gradients in food availability and understanding the processes potentially generating them. Here, we examine the functional relationship between body size and chemical energy availability over a broad assortment of marine mollusks varying in habitat and mobility. We demonstrate that chemical energy availability is likely driving body size patterns across habitats. We find that lower food availability decreases size-based niche availability by setting hard constraints on maximum size and potentially on minimum size depending on clade-specific ecology. Conversely, higher food availability promotes greater niche availability and potentially promotes evolutionary innovation with regard to size. We posit based on these findings and previous work that increases in chemical energy are important to the diversification of Metazoans through size-mediated niche processes.     

Effects of food supplementation on the physiological ecology of female Western diamond-backed rattlesnakes (<Emphasis Type="Italic">Crotalus atrox</Emphasis>)

Food availability is an important factor in the life histories of organisms because it is often limiting and thus can affect growth, mass change, reproduction, and behaviors such as thermoregulation, locomotion, and mating. Experimental studies in natural settings allow researchers to examine the effects of food on these parameters while animals are free to behave naturally. The wide variation among organisms in energy demands and among environmental food resources suggest that responses to changes in food availability may vary among organisms. Since most supplemental feeding field experiments have been conducted on species with high energy demands, we conducted a supplemental feeding study on free-ranging, female Western diamond-backed rattlesnakes (Crotalus atrox), a species with low energy demands and infrequent reproductive investment. Snakes were offered thawed rodents 1–4 times per week. Over two active seasons, we collected data on surface activity, home range size, growth, mass change, and reproduction of supplementally fed and control snakes. Fed and control snakes did not differ in surface activity levels (proportion of time encountered above versus below ground) or home range size. Fed snakes grew and gained mass faster, and had a dramatically higher occurrence of reproduction than control snakes. Also, fed snakes were in better body condition following reproduction than snakes that were not fed. However, litter characteristics such as offspring number and size were not increased by feeding, suggesting that these characteristics may be fixed. These data experimentally demonstrate that food availability can directly impact some life history traits (i.e., growth and reproduction for C. atrox), but not others (i.e., surface activity and home range size for C. atrox). The relationship between food availability and life history traits is affected in a complex way by ecological traits and physiological constraints, and thus interspecific variation in this relationship is likely to be high.     

Absence of heterothermy in the European red squirrel (Sciurus vulgaris)

The European red squirrel Sciurus vulgaris inhabits areas which undergo profound seasonal declines in food availability and ambient temperature. We measured the body temperature (T_b) of free-ranging S. vulgaris over the course of one year to examine its thermoregulatory strategies and found no evidence of heterothermy, with T_b never dropping below 36.7 °C. A lower average T_b and a reduced active phase are likely to have resulted in some energetic savings, sufficient for survival during the particularly mild winter with unhindered access to food stores. We cannot exclude that a different T_b pattern may be seen in energetically more demanding years, but we can confirm that heterothermy is not an obligatory behaviour in this species to counter energetic bottlenecks. Either S. vulgaris is indeed a strict homeotherm, or the need for torpor is flexibly adjusted.     

Proximate Cues for a Short-Distance Migratory Species: an Application of Survival Analysis

ABSTRACT Investigation of bird migration has often highlighted the importance of external factors in determining timing of migration. However, little distinction has been made between short- and long-distance migrants and between local and flight birds (passage migrants) in describing migration chronology. In addition, measures of food abundance as a proximate factor influencing timing of migration are lacking in studies of migration chronology. To address the relationship between environmental variables and timing of migration, we quantified the relative importance of proximate external factors on migration chronology of local American woodcock (Scolopax minor), a short distance migrant, using event-time analysis methods (survival analysis). We captured 1,094 woodcock local to our study sites in Michigan, Minnesota, and Wisconsin (USA) during autumn 2002–2004 and documented 786 departure dates for these birds. Photoperiod appeared to provide an initial proximate cue for timing of departure. Moon phase was important in modifying timing of departure, which may serve as a navigational aid in piloting and possibly orientation. Local synoptic weather variables also contributed to timing of departure by changing the rate of departure from our study sites. We found no evidence that food availability influenced timing of woodcock departure. Our results suggest that woodcock use a conservative photoperiod-controlled strategy with proximate modifiers for timing of migration rather than relying on abundance of their primary food, earthworms. Managing harvest pressure on local birds by adjusting season lengths may be an effective management tool with consistent migration patterns from year to year based on photoperiod.     

The autumnal fattening of the long-distance migratory garden warbler (Sylvia borin) is stimulated by intermittent fasting

To investigate the proximate influence of a changing food availability on the seasonal fattening of migratory birds, garden warblers (Sylvia borin) following postnuptial moult were food restricted once a week. Body mass, food intake, plasma hormone and metabolite levels were measured and compared to birds which always had ad libitum food access. The food-restricted birds increased their body mass significantly earlier than the controls. The accelerated fattening was initially not accompanied by hyperphagia and may be due to either an increased food utilisation efficiency or a reduced metabolic rate. An increase of basal glucagon and corticosterone and a decrease of insulin levels prior to fattening were not significant, however, they resulted in a significant decrease of the insulin:glucagon ratio. This ratio was also lower in food-restricted birds than in control birds and may account for the difference in the fattening progress. We conclude that seasonal fattening may be stimulated by a catabolic impulse which could be imposed in free-living birds by a decrease of food availability and/or by an increase of energy expenditure. A negative energy balance is hypothesised to be a common proximate factor affecting migratory as well as winter fattening. Accepted: 24 August 2000     

Tropical heterothermy is “cool”: The expression of daily torpor and hibernation in primates

Living nonhuman primates generally inhabit tropical forests, and torpor is regarded as a strategy employed by cold‐adapted organisms. Yet, some primates employ daily torpor or hibernation (heterothermy) under obligatory, temporary, or emergency circumstances. Though heterothermy is present in most mammalian lineages, there are only three extant heterothermic primate lineages: bushbabies from Africa, lorises from Asia, and dwarf and mouse lemurs from Madagascar. Here, we analyze their phenotypes in the general context of tropical mammalian heterothermy. We focus on Malagasy lemurs as they have been the most intensively studied and also show an unmatched range of flexibility in their heterothermic responses. We discuss the evidence for whether heterothermy should be considered an ancestral or derived condition in primates. This consideration is particularly intriguing given that an understanding of the underlying mechanisms for hibernation in lemurs opens the possibility for insight into genotype‐phenotype interactions, including those with biomedical relevance for humans.     

Investment into Defensive Traits by Anuran Prey (Lithobates pipiens) Is Mediated by the Starvation-Predation Risk Trade-Off

Prey can invest in a variety of defensive traits when balancing risk of predation against that of starvation. What remains unknown is the relative costs of different defensive traits and how prey reconcile investment into these traits when energetically limited. We tested the simple allocation model of prey defense, which predicts an additive effect of increasing predation risk and resource availability, resulting in the full deployment of defensive traits under conditions of high risk and resource saturation. We collected morphometric, developmental, and behavioural data in an experiment using dragonfly larvae (predator) and Northern leopard frog tadpoles (prey) subject to variable levels of food availability and predation risk. Larvae exposed to food restriction showed limited response to predation risk; larvae at food saturation altered behaviour, development, and growth in response to predation risk. Responses to risk varied through time, suggesting ontogeny may affect the deployment of particular defensive traits. The observed negative correlation between body size and activity level for food-restricted prey – and the absence of a similar response among adequately-fed prey – suggests that a trade-off exists between behavioural and growth responses when energy budgets are limited. Our research is the first to demonstrate how investment into these defensive traits is mediated along gradients of both predation risk and resource availability over time. The interactions we demonstrate between resource availability and risk level on deployment of inducible defenses provide evidence that both internal condition and extrinsic risk factors play a critical role in the production of inducible defenses over time.     

Nutritional availability and larval density dependence in Aedes aegypti

1. Density dependence is the effect of density on population growth. Density dependence is an aggregate term for a suite of complex interactions between animals and their environment. 2. Mechanistic studies of density dependence in mosquito ecology are sparse, and the role of environmental factors is poorly understood. 3. Two empirical study designs were compared to consider the interaction between nutritional availability and density in Aedes aegypti. First, larvae were fed per capita. Second, larvae were fed a fixed amount of food unadjusted for the number of individuals; therefore, at higher densities, individuals received less per capita. 4. Survivorship, wing length, and development rate were lower at high densities when larvae were fed a fixed, unadjusted amount of food. The opposite was observed when food was adjusted per capita, suggesting that high densities may be beneficial for larval development when per capita nutrition is held constant 5. These results demonstrate that negative associations between Ae. aegypti larval density and larval development are a manifestation of decreased per capita nutrient uptake at high densities. 6. Population regulation is a proportional response to environmental variability in Ae. aegypti. Increased survivorship at high densities when larvae were fed per capita demonstrates that nutritional availability is not the only mechanism of density dependence in mosquitoes. Further studies should characterise density dependence in mosquitoes by using mechanistic study designs across diverse environmental conditions.     

An energetic correlate between colony size and foraging effort in seabirds, an example of the Adélie penguin Pygoscelis adeliae

Central-place foraging seabirds alter the availability of their prey around colonies, forming a "halo" of reduced prey access that ultimately constrains population size. This has been indicated indirectly by an inverse correlation between colony size and reproductive success, numbers of conspecifics at other colonies within foraging range, foraging effort (i.e. trip duration), diet quality and colony growth rate. Although ultimately mediated by density dependence relative to food through intraspecific exploitative or interference competition, the proximate mechanism involved has yet to be elucidated. Herein, we show that Adélie penguin Pygoscelis adeliae colony size positively correlates to foraging trip duration and metabolic rate, that the metabolic rate while foraging may be approaching an energetic ceiling for birds at the largest colonies, and that total energy expended increases with trip duration although uncompensated by increased mass gain. We propose that a competition-induced reduction in prey availability results in higher energy expenditure for birds foraging in the halo around large colonies, and that to escape the halo a bird must increase its foraging distance. Ultimately, the total energetic cost of a trip determines the maximum successful trip distance, as on longer trips food acquired is used more for self maintenance than for chick provisioning. When the net cost of foraging trips becomes too high, with chicks receiving insufficient food, chick survival suffers and subsequent colony growth is limited. Though the existence of energetic studies of the same species at multiple colonies is rare, because foraging metabolic rate increases with colony size in at least two other seabird species, we suggest that an energetic constraint to colony size may generally apply to other seabirds.     

不同温度下黑线仓鼠应对食物短缺的能量学对策

食物资源的不确定性是动物在自然环境中面临的重要挑战之一."代谢率转换"假说认为,动物应对食物短缺的能量学策略在于降低代谢率以减少能量支出.然而在不同环境温度下非冬眠小型哺乳动物应对食物短缺的"代谢率转换"策略,尚不明确.为探究这一问题,将成年雄性黑线仓鼠在低温(5.0℃)、室温(21.0℃)和高温(32.5℃)下断食处...     

Seasonal Energetic Stress in a Tropical Forest Primate: Proximate Causes and Evolutionary Implications

Animals facing seasonal variation in food availability experience selective pressures that favor behavioral adjustments such as migration, changes in activity, or shifts in diet. Eclectic omnivores such as many primates can process low-quality fallback food when preferred food is unavailable. Such dietary flexibility, however, may be insufficient to eliminate constraints on reproduction even for species that live in relatively permissive environments, such as moist tropical forests. Focusing on a forest-dwelling primate with a flexible diet (Cercopithecus mitis) we investigated whether females experience seasonal energetic stress and how it may relate to reproductive seasonality. We used fecal glucocorticoids (fGCs) as an indicator of energetic stress, controlling for the potentially confounding effects of social interactions and reproductive state. We modeled within-female fGC variation with General Linear Mixed Models, evaluating changes in feeding behavior and food availability as main effects. Regardless of reproductive state, fGCs increased when females shifted their diet towards fallback foods (mature leaves and other non-preferred items) and when they spent more time feeding, while fGCs decreased with feeding time on preferred items (insects, fruits, young leaves) and with the availability of young leaves. Changes in fruit availability had no general effects on fGCs, likely because fruits were sought out regardless of availability. As predicted, females in the energetically demanding stages of late pregnancy and early lactation showed greater increases in fGCs between periods of low versus high availability of fruits and young leaves than females in other reproductive states. Potential social stressors had no measurable effects on fGCs. Preliminary evidence suggests that seasonal energetic stress may affect the timing of infant independence from mothers and contribute to unusually long inter-birth intervals compared to closely related species of similar body size. Our findings highlight how the study of stress responses can provide insights into the proximate control of reproductive strategies.     

Density dependence forces divergent population growth rates and alters occupancy patterns of a central place foraging Antarctic seabird

Density‐dependent regulation is an important process in spatio‐temporal population dynamics because it can alter the effects of synchronizing processes operating over large spatial scales. Most frequently, populations are regulated by density dependence when higher density leads to reduced individual fitness and population growth, but inverse density dependence can also occur when small populations are subject to higher extinction risks. We investigate whether density‐dependent regulation influences population growth for the Antarctic breeding Adélie penguin Pygoscelis adeliae. Understanding the prevalence and nature of density dependence for this species is important because it is considered a sentinel species reflecting the impacts of fisheries and environmental change over large spatial scales in the Southern Ocean, but the presence of density dependence could introduce uncertainty in this role. Using data on population growth and indices of resource availability for seven regional Adélie penguin populations located along the East Antarctic coastline, we find compelling evidence that population growth is constrained at some locations by the amount of breeding habitat available to individuals. Locations with low breeding habitat availability had reduced population growth rates, higher overall occupancy rates, and higher occupancy of steeper slopes that are sparsely occupied or avoided at other locations. Our results are consistent with evolutionary models of avian breeding habitat selection where individuals search for high‐quality nest sites to maximize fitness returns and subsequently occupy poorer habitat as population density increases. Alternate explanations invoking competition for food were not supported by the available evidence, but strong conclusions on food‐related density dependence were constrained by the paucity of food availability data over the large spatial scales of this region. Our study highlights the importance of incorporating nonconstant conditions of species–environment relationships into predictive models of species distributions and population dynamics, and provides guidance for improved monitoring of fisheries and climate change impacts in the Southern Ocean.