The biology and ecology of the ocean sunfish Mola mola: a review of current knowledge and future research perspectives

Relatively little is known about the biology and ecology of the world's largest (heaviest) bony fish, the ocean sunfish Mola mola, despite its worldwide occurrence in temperate and tropical seas. Studies are now emerging that require many common perceptions about sunfish behaviour and ecology to be re-examined. Indeed, the long-held view that ocean sunfish are an inactive, passively drifting species seems to be entirely misplaced. Technological advances in marine telemetry are revealing distinct behavioural patterns and protracted seasonal movements. Extensive forays by ocean sunfish into the deep ocean have been documented and broad-scale surveys, together with molecular and laboratory based techniques, are addressing the connectivity and trophic role of these animals. These emerging molecular and movement studies suggest that local distinct populations may be prone to depletion through bycatch in commercial fisheries. Rising interest in ocean sunfish, highlighted by the increase in recent publications, warrants a thorough review of the biology and ecology of this species. Here we review the taxonomy, morphology, geography, diet, locomotion, vision, movements, foraging ecology, reproduction and species interactions of M. mola. We present a summary of current conservation issues and suggest methods for addressing fundamental gaps in our knowledge.

Influence of vegetation on the nocturnal foraging behaviors and vertebrate prey capture by endangered Burrowing Owls

Restrictions in technology have limited past habitat selection studies for many species to the home-range level, as a finer-scale understanding was often not possible. Consequently, these studies may not identify the true mechanism driving habitat selection patterns, which may influence how such results are applied in conservation. We used GPS dataloggers with digital video recorders to identify foraging modes and locations in which endangered Burrowing Owls (Athene cunicularia) captured prey. We measured the coarse and fine-scale characteristics of vegetation at locations in which owls searched for, versus where they caught, vertebrate prey. Most prey items were caught using hover-hunting. Burrowing Owls searched for, and caught, vertebrate prey in all cover types, but were more likely to kill prey in areas with sparse and less dense vegetative cover. Management strategies designed to increase Burrowing Owl foraging success in the Canadian prairies should try to ensure a mosaic of vegetation heights across cover types.

Ontogeny of movements and foraging ranges in the Australian sea lion

This study tracked the movements of Australian sea lion (Neophoca cinerea) pups, juveniles, and adult females to identify home ranges and determine if young sea lions accompanied their mothers at sea. Satellite tags were deployed on nine 15- mo-old pups, nine 23-mo-old juveniles, and twenty-nine adult female Australian sea lions at Seal Bay Conservation Park, Kangaroo Island, South Australia. Females did not travel with their offspring at sea, suggesting young Australian sea lions learn foraging behaviors independently. Although home ranges increased with age,  23-mo-old juveniles had not developed adult movement capacity and their range was only 40.6% of the adult range. Juveniles traveled shorter distances (34.8 ± 5.5 km) at slower speeds (2.0 ± 0.3 km/h) than adults (67.9 ± 3.5 km and 3.9 ± 0.3 km/h). Young sea lions also stayed in shallower waters; sea floor depths of mean locations were 48±7m for juveniles and 74±2m for females. Restricted to shallow coastal waters, pups and juveniles are more likely to be disproportionately impacted by human activities. With limited available foraging habitat, young Australian sea lions appear particularly vulnerable to environmental alterations resulting from fisheries or climate change.

Bathymetry and frontal system interactions influence seasonal foraging movements of lactating subantarctic fur seals from Marion Island

Sixteen lactating subantarctic fur seals Arctocephalus tropicalis were satellite-tracked during the winter of 2006 (n = 6), summer of 2006/07 (n = 6) and autumn/winter (n = 4) of 2007, from Marion Island, Southern Ocean. Despite varied individual movement patterns, a favoured foraging area lay to the northeast of the island. In contrast to findings for populations at similar latitudes, seals from Marion Island did not undertake short overnight foraging trips, but trips consistently went beyond 300 km from the island. This aligns with the at-sea duration of lactating seals’ foraging trips from temperate Amsterdam Island, but differs from subantarctic Crozet and Macquarie islands. Time spent at sea, maximum distances travelled and movement variation of tracks from the island varied seasonally. Faecal analysis suggests the diet comprised primarily myctophid fish with limited seasonal variation. Well-defined areas of restricted movement coincided with significant bathymetric features to the west/northwest of the Crozet Plateau, with the Del Caño Rise clearly being important. Positive and negative sea-surface height anomalies (compared to the mean) appeared to be preferred by most seals across seasons. Higher summer sea-surface temperatures correlated with the movements of some seals. Higher chlorophyll a concentrations dictated transit and foraging areas during summer. Bathymetrically influenced oceanographic variables likely explain these preferred long-distance eastward movements. The Îles Crozet and Marion island subantarctic fur seals differ in their foraging ecology despite being neighbours. Conversely, the subantarctic fur seal populations from the distant Amsterdam and Marion islands appear to be similarly influenced by such environmental factors.

Foraging behaviour of two rodent species inhabiting a kopje (rocky outcrop) in Tsavo West National Park, Kenya

We employed patch use theory to evaluate how several environmental factors influence the foraging behaviour of two rodent species: Grammomys dolichurus and Acomys cahirinus. Foraging efficiency was determined by measuring the remaining food in artificial food patches (giving-up densities: GUDs) from two experiments. In the first experiment, we placed patches in different microhabitat types (cover vs open) and at varying distances from cover. This experiment was conducted during three moon stages (waxing, full, waning). We found that the rodents had higher GUDs (lower foraging efficiency) in the open microhabitat. The distance from nearest shelter had a marginally significant positive effect on GUDs. GUDs were higher in both microhabitat types during the waxing and full phases, but decreased sharply once the moon began to rise after sunset. These results are likely due to higher predation risk away from cover and in more illuminated environments. In the second experiment, we examined mouse responses to seeds impregnated with plant toxins. Seeds impregnated with oxalic acid were avoided by the rodents, while seeds soaked in tannic acid did not differ significantly from control seeds. Our results highlight important ecological factors affecting the foraging behaviour of these rodents.

Molecular sex-typing in shorebirds: a review of an essential method for research in evolution, ecology and conservation

Knowing the correct sex of individuals is essential both for research in evolutionary ecology and for practical conservation. Recent molecular advances have produced cheap, quick and reliable methods for sexing birds including chicks, juveniles, immatures and adults. Shorebird researchers have not yet fully utilised these advances. Here we provide an overview of work in this area to date with two objectives: (i) to review the major applications of molecular sexing and findings of shorebird research so far, and (ii) to provide an essential guide on how to carry out molecular sexing using current methods whilst avoiding methodological pitfalls. We encourage shorebird researchers to make better use of molecular sex-typing techniques in studies of conservation, migration, foraging ecology and breeding behaviour.

The biology and ecology of the ocean sunfish Mola mola : a review of current knowledge and future research perspectives

Relatively little is known about the biology and ecology of the world’s largest (heaviest) bony fish, the ocean sunfish Mola mola, despite its worldwide occurrence in temperate and tropical seas. Studies are now emerging that require many common perceptions about sunfish behaviour and ecology to be re-examined. Indeed, the long-held view that ocean sunfish are an inactive, passively drifting species seems to be entirely misplaced. Technological advances in marine telemetry are revealing distinct behavioural patterns and protracted seasonal movements. Extensive forays by ocean sunfish into the deep ocean have been documented and broad-scale surveys, together with molecular and laboratory based techniques, are addressing the connectivity and trophic role of these animals. These emerging molecular and movement studies suggest that local distinct populations may be prone to depletion through bycatch in commercial fisheries. Rising interest in ocean sunfish, highlighted by the increase in recent publications, warrants a thorough review of the biology and ecology of this species. Here we review the taxonomy, morphology, geography, diet, locomotion, vision, movements, foraging ecology, reproduction and species interactions of M. mola. We present a summary of current conservation issues and suggest methods for addressing fundamental gaps in our knowledge.

Jellyfish aggregations and leatherback turtle foraging patterns in a temperate coastal environment

Leatherback turtles (Dermochelys coriacea) are obligate predators of gelatinous zooplankton. However, the spatial relationship between predator and prey remains poorly understood beyond sporadic and localized reports. To examine how jellyfish (Phylum Cnidaria: Orders Semaeostomeae and Rhizostomeae) might drive the broad-scale distribution of this wide ranging species, we employed aerial surveys to map jellyfish throughout a temperate coastal shelf area bordering the northeast Atlantic. Previously unknown, consistent aggregations of Rhizostoma octopus extending over tens of square kilometers were identified in distinct coastal “hotspots” during consecutive years (2003–2005). Examination of retrospective sightings data (>50 yr) suggested that 22.5% of leatherback distribution could be explained by these hotspots, with the inference that these coastal features may be sufficiently consistent in space and time to drive long-term foraging associations.

Diving deeper into individual foraging specializations of a large marine predator, the southern sea lion

Despite global declines in the abundance of marine predators, knowledge of foraging ecology, necessary to predict the ecological consequences of large changes in marine predator abundance, remains enigmatic for many species. Given that populations suffering severe declines are of conservation concern, we examined the foraging ecology of southern sea lions (SSL) (Otaria flavescens)-one of the least studied otariids (fur seal and sea lions)-which have declined by over 90 % at the Falkland Islands since the 1930s. Using a combination of biologging devices and stable isotope analysis of vibrissae, we redress major gaps in the knowledge of SSL ecology and quantify patterns of individual specialization. Specifically, we revealed two discrete foraging strategies, these being inshore (coastal) and offshore (outer Patagonian Shelf). The majority of adult female SSL (72 % or n = 21 of 29 SSL) foraged offshore. Adult female SSL that foraged offshore travelled further (92 ± 20 vs. 10 ± 4 km) and dived deeper (75 ± 23 vs. 21 ± 8 m) when compared to those that foraged inshore. Stable isotope analysis revealed long-term fidelity (years) to these discrete foraging habitats. In addition, we found further specialization within the offshore group, with adult female SSL separated into two clusters on the basis of benthic or mixed (benthic and pelagic) dive behavior (benthic dive proportion was 76 ± 9 vs. 51 ± 8 %, respectively). We suggest that foraging specialization in depleted populations such as SSL breeding at the Falkland Islands, are influenced by foraging site fidelity, and could be independent of intraspecific competition. Finally, the behavioral differences we describe are crucial to understanding population-level dynamics, impediments to population recovery, and threats to population persistence.

Breeding short-tailed shearwaters buffer local environmental variability in south-eastern Australia by foraging in Antarctic waters

BACKGROUND: Establishing patterns of movements of free-ranging animals in marine ecosystems is crucial for a better understanding of their feeding ecology, life history traits and conservation. As central place foragers, the habitat use of nesting seabirds is heavily influenced by the resources available within their foraging range. We tested the prediction that during years with lower resource availability, short-tailed shearwaters (Puffinus tenuirostris) provisioning chicks should increase their foraging effort, by extending their foraging range and/or duration, both when foraging in neritic (short trips) and distant oceanic waters (long trips). Using both GPS and geolocation data-loggers, at-sea movements and habitat use were investigated over three breeding seasons (2012-14) at two colonies in southeastern Australia. RESULTS: Most individuals performed daily short foraging trips over the study period and inter-annual variations observed in foraging parameters where mainly due to few individuals from Griffith Island, performing 2-day trips in 2014. When performing long foraging trips, this study showed that individuals from both colonies exploited similar zones in the Southern Ocean. The results of this study suggest that individuals could increase their foraging range while exploiting distant feeding zones, which could indicate that short-tailed shearwaters forage in Antarctic waters not only to maintain their body condition but may also do so to buffer against local environmental stochasticity. Lower breeding performances were associated with longer foraging trips to distant oceanic waters in 2013 and 2014 indicating they could mediate reductions in food availability around the breeding colonies by extending their foraging range in the Southern Ocean. CONCLUSIONS: This study highlights the importance of foraging flexibility as a fundamental aspect of life history in coastal/pelagic marine central place foragers living in highly variable environments and how these foraging strategies are use to buffer this variability.

Determinants of individual foraging specialization in large marine vertebrates, the Antarctic and subantarctic fur seals

The degree of individual specialization in resource use differs widely among wild populations where individuals range from fully generalized to highly specialized. This interindividual variation has profound implications in many ecological and evolutionary processes. A recent review proposed four main ecological causes of individual specialization: interspecific and intraspecific competition, ecological opportunity and predation. Using the isotopic signature of subsampled whiskers, we investigated to what degree three of these factors (interspecific and intraspecific competition and ecological opportunity) affect the population niche width and the level of individual foraging specialization in two fur seal species, the Antarctic and subantarctic fur seals (Arctocephalus gazella and Arctocephalus tropicalis), over several years. Population niche width was greater when the two seal species bred in allopatry (low interspecific competition) than in sympatry or when seals bred in high-density stabilized colonies (high intraspecific competition). In agreement with the niche variation hypothesis (NVH), higher population niche width was associated with higher interindividual niche variation. However, in contrast to the NVH, all Antarctic females increased their niche width during the interbreeding period when they had potential access to a wider diversity of foraging grounds and associated prey (high ecological opportunities), suggesting they all dispersed to a similar productive area. The degree of individual specialization varied among populations and within the annual cycle. Highest levels of interindividual variation were found in a context of lower interspecific or higher intraspecific competition. Contrasted results were found concerning the effect of ecological opportunity. Depending on seal species, females exhibited either a greater or lower degree of individual specialization during the interbreeding period, reflecting species-specific biological constraints during that period. These results suggest a significant impact of ecological interactions on the population niche width and degree of individual specialization. Such variation at the individual level may be an important factor in the species plasticity with significant consequences on how it may respond to environmental variability.

Eating locally: Australasian gannets increase their foraging effort in a restricted range

During the breeding season, seabirds adopt a central place foraging strategy and are restricted in their foraging range by the fasting ability of their partner/chick and the cost of commuting between the prey resources and the nest. Because of the spatial and temporal variability of marine ecosystems, individuals must adapt their behaviour to increase foraging success within these constraints. The at-sea movements, foraging behaviour and effort of the Australasian gannet (Morus serrator) was determined over three sequential breeding seasons of apparent differing prey abundance to investigate how the species adapts to inter-annual fluctuations in food availability. GPS and tri-axial accelerometer data loggers were used to compare the degree of annual variation within two stages of breeding (incubation and chick rearing) at a small gannet colony situated between two larger, nearby colonies. Interestingly, neither males nor females increased the total distance travelled or duration of foraging trip in any breeding stage (P>0.05 in all cases) despite apparent low prey availability. However, consistently within each breeding stage, mean vectorial dynamic body acceleration (an index of energy expenditure) was greater in years of poorer breeding success (increased by a factor of three to eight), suggesting birds were working harder within their range. Additionally, both males and females increased the proportion of a foraging trip spent foraging in a poorer year across both breeding stages. Individuals from this colony may be limited in their ability to extend their range in years of low prey availability due to competition from conspecifics in nearby colonies and, consequently, increase foraging effort within this restricted foraging area.

From video recordings to whisker stable isotopes: a critical evaluation of timescale in assessing individual foraging specialisation in Australian fur seals

Estimating the degree of individual specialisation is likely to be sensitive to the methods used, as they record individuals' resource use over different time-periods. We combined animal-borne video cameras, GPS/TDR loggers and stable isotope values of plasma, red cells and sub-sampled whiskers to investigate individual foraging specialisation in female Australian fur seals (Arctocephalus pusillus doriferus) over various timescales. Combining these methods enabled us to (1) provide quantitative information on individuals' diet, allowing the identification of prey, (2) infer the temporal consistency of individual specialisation, and (3) assess how different methods and timescales affect our estimation of the degree of specialisation. Short-term inter-individual variation in diet was observed in the video data (mean pairwise overlap = 0.60), with the sampled population being composed of both generalist and specialist individuals (nested network). However, the brevity of the temporal window is likely to artificially increase the level of specialisation by not recording the entire diet of seals. Indeed, the correlation in isotopic values was tighter between the red cells and whiskers (mid- to long-term foraging ecology) than between plasma and red cells (short- to mid-term) (R (2) = 0.93-0.73 vs. 0.55-0.41). δ(13)C and δ(15)N values of whiskers confirmed the temporal consistency of individual specialisation. Variation in isotopic niche was consistent across seasons and years, indicating long-term habitat (WIC/TNW = 0.28) and dietary (WIC/TNW = 0.39) specialisation. The results also highlight time-averaging issues (under-estimation of the degree of specialisation) when calculating individual specialisation indices over long time-periods, so that no single timescale may provide a complete and accurate picture, emphasising the benefits of using complementary methods.

Navigating uncertain waters: a critical review of inferring foraging behaviour from location and dive data in pinnipeds

In the last thirty years, the emergence and progression of biologging technology has led to great advances in marine predator ecology. Large databases of location and dive observations from biologging devices have been compiled for an increasing number of diving predator species (such as pinnipeds, sea turtles, seabirds and cetaceans), enabling complex questions about animal activity budgets and habitat use to be addressed. Central to answering these questions is our ability to correctly identify and quantify the frequency of essential behaviours, such as foraging. Despite technological advances that have increased the quality and resolution of location and dive data, accurately interpreting behaviour from such data remains a challenge, and analytical methods are only beginning to unlock the full potential of existing datasets. This review evaluates both traditional and emerging methods and presents a starting platform of options for future studies of marine predator foraging ecology, particularly from location and two-dimensional (time-depth) dive data. We outline the different devices and data types available, discuss the limitations and advantages of commonly-used analytical techniques, and highlight key areas for future research. We focus our review on pinnipeds - one of the most studied taxa of marine predators - but offer insights that will be applicable to other air-breathing marine predator tracking studies. We highlight that traditionally-used methods for inferring foraging from location and dive data, such as first-passage time and dive shape analysis, have important caveats and limitations depending on the nature of the data and the research question. We suggest that more holistic statistical techniques, such as state-space models, which can synthesise multiple track, dive and environmental metrics whilst simultaneously accounting for measurement error, offer more robust alternatives. Finally, we identify a need for more research to elucidate the role of physical oceanography, device effects, study animal selection, and developmental stages in predator behaviour and data interpretation.