Capital and income breeding: the role of food supply.

An aspect of life history that has seen increasing attention in recent years is that of strategies for financing the costs of offspring production. These strategies are often described by a continuum ranging from capital breeding, in which costs are met purely from endogenous reserves, to income breeding, in which costs are met purely from concurrent intake. A variety of factors that might drive strategies toward a given point on the capital-income continuum has been reviewed, and assessed using analytical models. However, aspects of food supply, including seasonality and unpredictability, have often been cited as important drivers of capital and income breeding, but are difficult to assess using analytical models. Consequently, we used dynamic programming to assess the role of the food supply in shaping offspring provisioning strategies. Our model is parameterized for a pinniped (one taxon remarkable for the range of offspring-provisioning strategies that it illustrates). We show that increased food availability, increased seasonality, and, to a lesser extent, increased unpredictability can all favor the emergence of capital breeding. In terms of the conversion of energy into offspring growth, the shorter periods of care associated with capital breeding are considerably more energetically efficient than income breeding, because shorter periods of care are associated with a higher ratio of energy put into offspring growth to energy spent on parent and offspring maintenance metabolism. Moreover, no clear costs are currently associated with capital accumulation in pinnipeds. This contrasts with general assumptions about endotherms, which suggest that income breeding will usually be preferred. Our model emphasizes the role of seasonally high abundances of food in enabling mothers to pursue an energetically efficient capital-breeding strategy. We discuss the importance of offspring development for dictating strategies for financing offspring production.

Global seabird response to forage fish depletion--one-third for the birds.

Determining the form of key predator-prey relationships is critical for understanding marine ecosystem dynamics. Using a comprehensive global database, we quantified the effect of fluctuations in food abundance on seabird breeding success. We identified a threshold in prey (fish and krill, termed "forage fish") abundance below which seabirds experience consistently reduced and more variable productivity. This response was common to all seven ecosystems and 14 bird species examined within the Atlantic, Pacific, and Southern Oceans. The threshold approximated one-third of the maximum prey biomass observed in long-term studies. This provides an indicator of the minimal forage fish biomass needed to sustain seabird productivity over the long term.

Beaked whales respond to simulated and actual navy sonar.

Beaked whales have mass stranded during some naval sonar exercises, but the cause is unknown. They are difficult to sight but can reliably be detected by listening for echolocation clicks produced during deep foraging dives. Listening for these clicks, we documented Blainville's beaked whales, Mesoplodon densirostris, in a naval underwater range where sonars are in regular use near Andros Island, Bahamas. An array of bottom-mounted hydrophones can detect beaked whales when they click anywhere within the range. We used two complementary methods to investigate behavioral responses of beaked whales to sonar: an opportunistic approach that monitored whale responses to multi-day naval exercises involving tactical mid-frequency sonars, and an experimental approach using playbacks of simulated sonar and control sounds to whales tagged with a device that records sound, movement, and orientation. Here we show that in both exposure conditions beaked whales stopped echolocating during deep foraging dives and moved away. During actual sonar exercises, beaked whales were primarily detected near the periphery of the range, on average 16 km away from the sonar transmissions. Once the exercise stopped, beaked whales gradually filled in the center of the range over 2-3 days. A satellite tagged whale moved outside the range during an exercise, returning over 2-3 days post-exercise. The experimental approach used tags to measure acoustic exposure and behavioral reactions of beaked whales to one controlled exposure each of simulated military sonar, killer whale calls, and band-limited noise. The beaked whales reacted to these three sound playbacks at sound pressure levels below 142 dB re 1 µPa by stopping echolocation followed by unusually long and slow ascents from their foraging dives. The combined results indicate similar disruption of foraging behavior and avoidance by beaked whales in the two different contexts, at exposures well below those used by regulators to define disturbance.

Capital breeding and income breeding: their meaning, measurement, and worth.

The life histories of organisms can show pronounced variation in the way that the costs of reproduction are financed. To facilitate discussions of this variation, two terms are increasing in use: "capital breeding" describes the situation in which reproduction is financed using stored capital; "income breeding" refers to the use of concurrent intake to pay for a reproductive attempt. We consider the value of the capital and income typology with reference to three functions that it might serve: description, explanation, and prediction. We find that interpretations of the terms have diversified and lack rigidity, leading to subjectivity in their definition. We recognize that time frames of interest will vary among taxa, but we urge consistency of use within those taxa. We also urge consistency in the use of a single metric designed to measure the reliance of an organism on capital. The concepts of capital and income breeding have served well as proximate explanations for behavioral or physiological diversity, but efforts to explain their adaptive value have been disproportionately focused on individual taxa. Mapping cause to effect is difficult in ecology. Nevertheless, further analyses, based on consistently applied measures of reliance on stored capital, may reveal which of the putative ecological, morphological, and physiological drivers have the most consistent and widespread effects. The capital-income typology has yet to be applied to the question of prediction, and thus, it remains to be seen whether these concepts will be of use in identifying the likely responses of different populations to changes in their environment.

The scaling of diving time budgets: insights from an optimality approach.

Simple scaling arguments suggest that, among air-breathing divers, dive duration should scale approximately with mass to the one-third power. Recent phylogenetic analyses appear to confirm this. The same analyses showed that duration of time spent at the surface between dives has scaling very similar to that of dive duration, with the result that the ratio of dive duration to surface pause duration is approximately mass invariant. This finding runs counter to other arguments found in the diving literature that suggest that surface pause duration should scale more positively with mass, leading to a negative scaling of the dive-pause ratio. We use a published model of optimal time allocation in the dive cycle to show that optimal decisions can predict approximate mass invariance in the dive-pause ratio, especially if metabolism scales approximately with mass to the two-thirds power (as indicated by some recent analyses) and oxygen uptake is assumed to have evolved to supply the body tissues at the required rate. However, emergent scaling rules are sensitive to input parameters, especially to the relationship between the scaling of metabolism and oxygen uptake rate at the surface. Our results illustrate the utility of an optimality approach for developing predictions and identifying key areas for empirical research on the allometry of diving behavior.

Ascent exhalations of Antarctic fur seals: a behavioural adaptation for breath-hold diving?

Novel observations collected from video, acoustic and conductivity sensors showed that Antarctic fur seals consistently exhale during the last 50-85% of ascent from all dives (10-160 m, n > 8000 dives from 50 seals). The depth of initial bubble emission was best predicted by maximum dive depth, suggesting an underlying physical mechanism. Bubble sound intensity recorded from one seal followed predictions of a simple model based on venting expanding lung air with decreasing pressure. Comparison of air release between dives, together with lack of variation in intensity of thrusting movement during initial descent regardless of ultimate dive depth, suggested that inhaled diving lung volume was constant for all dives. The thrusting intensity in the final phase of ascent was greater for dives in which ascent exhalation began at a greater depth, suggesting an energetic cost to this behaviour, probably as a result of loss of buoyancy from reduced lung volume. These results suggest that fur seals descend with full lung air stores, and thus face the physiological consequences of pressure at depth. We suggest that these regular and predictable ascent exhalations could function to reduce the potential for a precipitous drop in blood oxygen that would result in shallow-water blackout.

Exploring the relationship between parental relatedness and male reproductive success in the Antarctic fur seal Arctocephalus gazella.

Recent genetic studies of natural populations have shown that heterozygosity and other genetic estimates of parental relatedness correlate with a wide variety of fitness traits, from juvenile survival and parasite resistance to male reproductive success. Many of these traits involve health and survival, where the underlying mechanism may involve changes in the effectiveness of the immune system. However, for traits such as reproductive success, the likely mechanisms remain less obvious. In this paper, we examine the relationship between heterozygosity and a range of traits that contribute to male reproductive success, including time spent on territories and competitiveness. Our analysis is based on observational and genetic data from eight consecutive breeding seasons at a colony of the Antarctic fur seal, Arctocephalus gazella. Overall, male reproductive success was found to correlate strongly with internal relatedness (IR, a form of heterozygosity). When different components of success were analyzed, we found that IR correlates independently with reproductive longevity, time spent ashore, and competitive ability per unit mating opportunity on the study beach, with more heterozygous males being more successful. Behavioral observations were sufficiently detailed to allow examination of how daily mean IR values for males present on the beach varied within seasons and from year to year. Again, significant variation was found both among and within seasons, with more homozygous males appearing less able to hold territories in poor seasons when pup production is low and, within a season, at both the start of the season and to some extent around the peak of female estrus. Finally, we tested whether the benefits of high heterozygosity are due mainly to a genomewide effect (e.g. inbreeding depression) or to single locus heterosis by asking whether the relationship between IR and male success was robust to the removal of any single locus or to any pair of loci. Since the relationship remained significant in all cases, we favor a multilocus explanation for the effects we report.

Evolution of mammals: lactation helps mothers to cope with unreliable food supplies.

Lactation is a ubiquitous feature of mammalian reproduction. Because lactating females can draw on their nutrient reserves for milk production, it offers mothers and their dependent young independence from fluctuations in their food supplies. However, converting food to reserves and milk is relatively inefficient at delivering nutrients to offspring. We use dynamic programming to contrast the performance of mothers that provision dependent, refuge-bound offspring optimally from their nutrient reserves with otherwise equivalent mothers that do so directly from the food they find. In this way, we demonstrate formally that the selective advantage to lactating mothers, who can provision--at a cost--without having found food recently, can be substantial with uncertain food supplies and few opportunities for future reproduction under a wide range of circumstances. Hence, it is likely that unreliability associated with the lifestyles of the small, primitive mammal-like reptiles that evolved extended maternal care, selected for fully-developed milk production and consumption, prompting the evolution of true mammals. Moreover, this work suggests that selection for coping with unreliable food access during provisioning may underlie key life-history differences between birds and mammals because the mass constraints imposed by flight restrict the level of reserves that mothers can carry and provision from.

Male reproductive strategy and the importance of maternal status in the Antarctic fur seal Arctocephalus gazella.

Although mammalian mating systems are classically characterized in terms of male competition and polygyny, it is becoming increasingly apparent that alternative male strategies and female choice may play important roles. For example, females who mate with males from a dominant dynasty risk producing inbred offspring. Many pinnipeds are highly polygynous, but in some species alternative male strategies such as aquatic mating appear to be important, even when behavioral observations suggest strong polygyny. Here, we analyze male reproductive success in the Antarctic fur seal Arctocephalus gazella, an otariid described behaviorally as being highly polygynous, by combining a microsatellite paternity analysis spanning seven consecutive breeding seasons with detailed behavioral data on both sexes. Territorial males fathered 59% of 660 pups analyzed from our study colony. Male reproductive skew was considerable, with a quarter of all paternities assigned to just 12 top individuals on a beach where mean annual pup production was 635. Most males were successful for only a single season, but those able to return over successive years enjoyed rapidly increasing success with each additional season of tenure. We found no evidence of alternative male reproductive tactics such as aquatic or sneaky terrestrial mating. However, paternity was strongly influenced by maternal status. Females observed on the beach without a pup were significantly less likely to conceive to a sampled territorial male than equivalent females that did pup. In addition, their pups carried combinations of paternal alleles that were less likely to be found on the study beach and exhibited lower levels of shared paternity. Thus, from a territorial male's perspective, not all females offer equal opportunities for fertilization.