Lucy Hawkes | University of Exeter (original) (raw)

Papers by Lucy Hawkes

Research paper thumbnail of How will sea turtles cope with climate change?

Abstract It is now widely accepted that climate change is a significant threat to biodiversity, e... more Abstract It is now widely accepted that climate change is a significant threat to biodiversity, especially to species like sea turtles whose life histories are sensitive to fluctuating environmental conditions. A growing number of studies have begun to investigate and ...

Research paper thumbnail of New findings about the spatial and temporal use of the Eastern Atlantic Ocean by large juvenile loggerhead turtles

Aims Effective conservation of threatened or endangered species requires a robust understanding o... more Aims Effective conservation of threatened or endangered species requires a robust understanding of their spatio-temporal distribution. Although a huge amount is known about the movements of Atlantic adult sea turtles, much less is known about juvenile turtles, and much of the life history model is therefore inferred. We set out to describe the spatio-temporal distribution of juvenile loggerheads turtles found around the Canary Islands.
Location Eastern North Atlantic Ocean.
Methods Between 1999 and 2012, we satellite-tracked 24 healthy large juvenile loggerhead turtles (mean straight carapace length = 47.4 cm, range = 34.6– 54.5 cm) captured in the waters around the Canary Islands. We describe their regional distribution, identify high-use areas and create a model for habitat suitability using minimum convex polygons, density rasters and ensemble ecological niche modelling, integrated with physical and biological environmental data.
Results Turtles used a huge oceanic area (2.5 million km2) with particularly high usage around the Canary Islands, Spain, Portugal, Morocco and Western Sahara. In spring and summer, turtles generally moved further north towards the Iberian Peninsula. Ecological niche modelling identified sea surface temperature as the most important contributory variable to the habitat models. We also recorded three juvenile turtles making westward migrations away from the eastern Atlantic Ocean, presumably back towards their original natal beaches near sexual maturity. Main conclusions The results of the present study provide insight into a significant knowledge gap on the spatio-temporal distribution of large juvenile loggerhead turtles in the eastern Atlantic Ocean. The data highlight that turtles occupy a vast open oceanic area, which hampers the ability of static conservation approaches to afford effective protection. However, ensemble ecological niche modelling highlights key suitable habitat for juvenile loggerhead turtles, which could be used in dynamic conservation protection.

Research paper thumbnail of Evaluating the landscape of fear between apex predatory sharks and mobile sea turtles across a large dynamic seascape

Ecology, 2015

The ‘‘landscape of fear’’ model has been proposed as a unifying concept in ecology, describing, i... more The ‘‘landscape of fear’’ model has been proposed as a unifying concept in ecology, describing, in part, how animals behave and move about in their environment. The basic model predicts that as an animal’s landscape changes from low to high risk of predation, prey species will alter their behavior to risk avoidance. However, studies investigating and evaluating the landscape of fear model across large spatial scales (tens to hundreds of thousands of square kilometers) in dynamic, open, aquatic systems involving apex predators and highly mobile prey are lacking. To address this knowledge gap, we investigated predator–prey relationships between tiger sharks (Galeocerdo cuvier) and loggerhead turtles (Caretta caretta) in the North Atlantic Ocean. This included the use of satellite tracking to examine shark and turtle distributions as well as their surfacing behaviors under varying levels of home range overlap. Our findings revealed patterns that deviated from our a priori predictions based on the landscape of fear model. Specifically, turtles did not alter their surfacing behaviors to risk avoidance when overlap in shark–turtle core home range was high. However, in areas of high overlap with turtles, sharks exhibited modified surfacing behaviors that may enhance predation opportunity. We suggest that turtles may be an important factor in determining shark distribution, whereas for turtles, other life history trade-offs may play a larger role in defining their habitat use. We propose that these findings are a result of both biotic and physically driven factors that independently or synergistically affect predator–prey interactions in this system. These results have implications for evolutionary biology, community ecology, and wildlife conservation. Further, given the difficulty in studying highly migratory marine species, our approach and conclusions may be applied to the study of other predator–prey systems.

Research paper thumbnail of Stable Isotopes Suggest Low Site Fidelity in Bar-Headed Geese ( Anser indicus ) in Mongolia: Implications for Disease Transmission

Waterbirds, 2015

Population connectivity is an important consideration in studies of disease transmission and biol... more Population connectivity is an important consideration in studies of disease transmission and biological conservation, especially with regard to migratory species. Determining how and when different subpopulations intermingle during different phases of the annual cycle can help identify important geographical regions or features as targets for conservation efforts and can help inform our understanding of continental-scale disease transmission. In this study, stable isotopes of hydrogen and carbon in contour feathers were used to assess the degree of molt-site fidelity among Bar-headed Geese (Anser indicus) captured in north-central Mongolia. Samples were collected from actively molting Bar-headed Geese (n = 61), and some individual samples included both a newly grown feather (still in sheath) and an old, worn feather from the bird's previous molt (n = 21). Although there was no difference in mean hydrogen isotope ratios for the old and new feathers, the isotopic variance in old feathers was approximately three times higher than that of the new feathers, which suggests that these birds use different and geographically distant molting locations from year to year. To further test this conclusion, online data and modeling tools from the isoMAP website were used to generate probability landscapes for the origin of each feather. Likely molting locations were much more widespread for old feathers than for new feathers, which supports the prospect of low molt-site fidelity. This finding indicates that population connectivity would be greater than expected based on data from a single annual cycle, and that disease spread can be rapid even in areas like Mongolia where Bar-headed Geese generally breed in small isolated groups.

Research paper thumbnail of Investigating the potential impacts of climate change on a marine turtle population

Global Change Biology

Recent increases in global temperatures have affected the phenology and survival of many species ... more Recent increases in global temperatures have affected the phenology and survival of many species of plants and animals. We investigated a case study of the effects of potential climate change on a thermally sensitive species, the loggerhead sea turtle, at a breeding location at the northerly extent of the range of regular nesting in the United States. In addition to the physical limits imposed by temperature on this ectothermic species, sea turtle primary sex ratio is determined by the temperature experienced by eggs during the middle third of incubation. We recorded sand temperatures and used historical air temperatures (ATs) at Bald Head Island, NC, to examine past and predict future sex ratios under scenarios of warming. There were no significant temporal trends in primary sex ratio evident in recent years and estimated mean annual sex ratio was 58% female. Similarly, there were no temporal trends in phenology but earlier nesting and longer nesting seasons were correlated with wa...

Research paper thumbnail of An assessment of marine turtles in The Gambia Phase I Report

Page 1. An Assessment of Marine Turtles in The Gambia Phase I Report Lucy A. Hawkes1, Matthew J. ... more Page 1. An Assessment of Marine Turtles in The Gambia Phase I Report Lucy A. Hawkes1, Matthew J. Witt1,Ibrahima Mat Dia2, Ousaynou Touray3 & Brendan J. Godley1 1 Marine Turtle Research Group, University of Exeter, Cornwall Campus, ...

Research paper thumbnail of Oceanic loggerhead turtles Caretta caretta associate with thermal fronts: evidence from the Canary Current Large Marine Ecosystem

Marine Ecology Progress Series, 2015

ABSTRACT Oceanographic fronts are physical interfaces between water masses that differ in propert... more ABSTRACT Oceanographic fronts are physical interfaces between water masses that differ in properties such as temperature, salinity, turbidity and chlorophyll a enrichment. Bio-physical coupling along fronts can lead to the development of pelagic biodiversity hotspots. A diverse range of marine vertebrates have been shown to associate with fronts, using them as foraging and migration habitats. Elucidation of the ecological significance of fronts generates a better understanding of marine ecosystem functioning, conferring opportunities to improve management of anthropogenic activities in the oceans. This study presents novel insights into the oceanographic drivers of habitat use in a population of marine turtles characterised by an oceanic-neritic foraging dichotomy. Using satellite tracking data from adult female loggerhead turtles Caretta caretta nesting at Cape Verde (n = 12), we tested the hypothesis that oceanic-foraging loggerheads associate with mesocale (10s to 100s of km) thermal fronts. We used high-resolution (1 km) composite front mapping to characterise frontal activity in the Canary Current Large Marine Ecosystem over 2 temporal scales: (1) seasonal front frequency and (2) 7 d front metrics. Our use-availability analysis indicated that oceanic loggerheads show a preference for the highly productive upwelling region between Cape Verde and mainland Africa, an area of intense frontal activity. Within the upwelling region, turtles appear to forage epipelagically around mesoscale thermal fronts, exploiting profitable foraging opportunities resulting from physical aggregation of prey.

Research paper thumbnail of How Bar-Headed Geese Fly Over the Himalayas

Physiology (Bethesda, Md.), 2015

Bar-headed geese cross the Himalayas on one of the most iconic high-altitude migrations in the wo... more Bar-headed geese cross the Himalayas on one of the most iconic high-altitude migrations in the world. Heart rates and metabolic costs of flight increase with elevation and can be near maximal during steep climbs. Their ability to sustain the high oxygen demands of flight in air that is exceedingly oxygen-thin depends on the unique cardiorespiratory physiology of birds in general along with several evolved specializations across the O2 transport cascade.

Research paper thumbnail of On the Front Line: frontal zones as priority at-sea conservation areas for mobile marine vertebrates

Journal of Applied Ecology, 2014

ABSTRACT 1.Identifying priority areas for marine vertebrate conservation is complex because speci... more ABSTRACT 1.Identifying priority areas for marine vertebrate conservation is complex because species of conservation concern are highly mobile, inhabit dynamic habitats and are difficult to monitor. 2.Many marine vertebrates are known to associate with oceanographic fronts – physical interfaces at the transition between water masses – for foraging and migration, making them important candidate sites for conservation. Here, we review associations between marine vertebrates and fronts and how they vary with scale, regional oceanography and foraging ecology. 3.Accessibility, spatiotemporal predictability and relative productivity of front-associated foraging habitats are key aspects of their ecological importance. Predictable mesoscale (10s–100s km) regions of persistent frontal activity (‘frontal zones’) are particularly significant. 4.Frontal zones are hotspots of overlap between critical habitat and spatially explicit anthropogenic threats, such as the concentration of fisheries activity. As such, they represent tractable conservation units, in which to target measures for threat mitigation. 5.Front mapping via Earth observation (EO) remote sensing facilitates identification and monitoring of these hotspots of vulnerability. Seasonal or climatological products can locate biophysical hotspots, while near-real-time front mapping augments the suite of tools supporting spatially dynamic ocean management. 6.Synthesis and applications. Frontal zones are ecologically important for mobile marine vertebrates. We surmise that relative accessibility, predictability and productivity are key biophysical characteristics of ecologically significant frontal zones in contrasting oceanographic regions. Persistent frontal zones are potential priority conservation areas for multiple marine vertebrate taxa and are easily identifiable through front mapping via EO remote sensing. These insights are useful for marine spatial planning and marine biodiversity conservation, both within Exclusive Economic Zones and in the open oceans

Research paper thumbnail of Supplementary Information: The roller coaster flight strategy of bar-headed geese conserves energy during Himalayan migrations

Research paper thumbnail of Biochemical Indices and Life Traits of Loggerhead Turtles (Caretta caretta) from Cape Verde Islands

PLoS ONE, 2014

The loggerhead turtle (Caretta caretta) is an endangered marine reptile for whom assessing popula... more The loggerhead turtle (Caretta caretta) is an endangered marine reptile for whom assessing population health requires knowledge of demographic parameters such as individual growth rate. In Cape Verde, as within several populations, adult female loggerhead sea turtles show a size-related behavioral and trophic dichotomy. While smaller females are associated with oceanic habitats, larger females tend to feed in neritic habitats, which is reflected in their physiological condition and in their offspring. The ratio of RNA/DNA provides a measure of cellular protein synthesis capacity, which varies depending on changes in environmental conditions such as temperature and food availability. The purpose of this study was to evaluate the combined use of morphometric data and biochemical indices as predictors of the physiological condition of the females of distinct sizes and hatchlings during their nesting season and how temperature may influence the physiological condition on the offspring. Here we employed biochemical indices based on nucleic acid derived indices (standardized RNA/DNA ratio-sRD, RNA concentration and DNA concentration) in skin tissue as a potential predictor of recent growth rate in nesting females and hatchling loggerhead turtles. Our major findings were that the physiological condition of all nesting females (sRD) decreased during the nesting season, but that females associated with neritic habitats had a higher physiological condition than females associated with oceanic habitats. In addition, the amount of time required for a hatchling to right itself was negatively correlated with its physiological condition (sRD) and shaded nests produced hatchlings with lower sRD. Overall, our results showed that nucleic acid concentrations and ratios of RNA to DNA are an important tool as potential biomarkers of recent growth in marine turtles. Hence, as biochemical indices of instantaneous growth are likely temperature-, size- and age-dependent, the utility and validation of these indices on marine turtles stocks deserves further study.

Research paper thumbnail of The potential future influence of sea level rise on leatherback turtle nests

Journal of Experimental Marine Biology and Ecology, 2014

ABSTRACT Climate change models predict sea level rise and increased intensity of storms and hurri... more ABSTRACT Climate change models predict sea level rise and increased intensity of storms and hurricanes in tropical sea turtle nesting areas. These factors could significantly increase beach inundation and erosion, thus affecting water content of sea turtle nesting beaches. Here, we conducted a field and laboratory study of how sand water content is related to embryonic development and hatching success of leatherback turtle nests. Moreover, we have experimentally incubated eggs of this species in beach sand under standardized conditions, but at different realistic levels of sand water content, varying from 1% to 12%. On the beaches, females nested from the intertidal zone to the lower part of the sand vegetation dunes, where nests were exposed to a wide range of sand water contents that ranged from 0.8% to 22%. However, both field and experimental studies revealed a strong negative correlation between sand water content and emergence success (field study: r = − 0.73, P < 0.0001; experiment: r = − 0.84, P < 0.0001). In the field, mean emergence success varied from 0% for the wettest nests to 64% for the driest ones. Nests in wet sand suffered higher mortality, primarily in the earlier developmental stages. Eggs incubated in the driest sand lost mass, but there were no significant effects on hatchling mass or run speed compared to eggs that gained water during incubation. However, hatchling straight carapace length (SCL) was greater in eggs from the driest treatment. The results of the present study inform management of change under future climate change sea level rise scenarios, suggesting that leatherback turtle nesting success should be expected to decrease.

Research paper thumbnail of The impacts of climate change on marine turtle reproductive success

Coastal Conservation, 2013

Research paper thumbnail of High rates of growth recorded for hawksbill sea turtles in Anegada, British Virgin Islands

Management of species of conservation concern requires knowledge of demographic parameters, such ... more Management of species of conservation concern requires knowledge of demographic parameters, such as rates of recruitment, survival, and growth. In the Caribbean, hawksbill turtles (Eretmochelys imbricata) have been historically exploited in huge numbers to satisfy trade in their shells and meat. In the present study, we estimated growth rate of juvenile hawksbill turtles around Anegada, British Virgin Islands, using capture-mark-recapture of 59 turtles over periods of up to 649 days. Turtles were recaptured up to six times, having moved up to 5.9 km from the release location. Across all sizes, turtles grew at an average rate of 9.3 cm year À1 (range 2.3-20.3 cm year À1 ), and gained mass at an average of 3.9 kg year À1 (range 850 g-16.1 kg year À1 ). Carapace length was a significant predictor of growth rate and mass gain, but there was no relationship between either variable and sea surface temperature. These are among the fastest rates of growth reported for this species, with seven turtles growing at a rate that would increase their body size by more than half per year (51-69% increase in body length). This study also demonstrates the importance of shallow water reef systems for the developmental habitat for juvenile hawksbill turtles. Although growth rates for posthatching turtles in the pelagic, and turtles larger than 61 cm, are not known for this population, the implications of this study are that Caribbean hawksbill turtles in some areas may reach body sizes suggesting sexual maturity in less time than previously considered.

Research paper thumbnail of Contextualising the Last Survivors: Population Structure of Marine Turtles in the Dominican Republic

PLoS ONE, 2013

Nesting by three species of marine turtles persists in the Dominican Republic, despite historic t... more Nesting by three species of marine turtles persists in the Dominican Republic, despite historic threats and long-term population decline. We conducted a genetic survey of marine turtles in the Dominican Republic in order to link them with other rookeries around the Caribbean. We sequenced a 740bp fragment of the control region of the mitochondrial DNA of 92 samples from three marine turtle species [hawksbill (n = 48), green (n = 2) and leatherback (n = 42)], and incorporated published data from other nesting populations and foraging grounds. The leatherback turtle (Dermochelys coriacea) in the Dominican Republic appeared to be isolated from Awala-Yalimapo, Cayenne, Trinidad and St. Croix but connected with other Caribbean populations. Two distinct nesting populations of hawksbill turtles (Eremochelys imbricata) were detected in the Dominican Republic and exhibited interesting patterns of connectivity with other nesting sites and juvenile and adult male foraging aggregations. The green sea turtle (Chelonia mydas) has almost been extirpated from the Dominican Republic and limited inference could be made from our samples. Finally, results were compared with Lagrangian drifting buoys and published Lagrangian virtual particles that travelled through the Dominican Republic and Caribbean waters. Conservation implications of sink-source effects or genetic isolation derived from these complex inter-connections are discussed for each species and population.

Research paper thumbnail of The roller coaster flight strategy of bar-headed geese conserves energy during Himalayan migrations

Research paper thumbnail of Modelling the niche for a marine vertebrate: a case study incorporating behavioural plasticity, proximate threats and climate change

Th e integration of satellite telemetry, remotely sensed environmental data, and habitat/environm... more Th e integration of satellite telemetry, remotely sensed environmental data, and habitat/environmental modelling has
provided for a growing understanding of spatial and temporal ecology of species of conservation concern. Th e Republic of
Cape Verde comprises the only substantial rookery for the loggerhead turtle Caretta caretta in the eastern Atlantic. A size
related dichotomy in adult foraging patterns has previously been revealed for adult sea turtles from this population with a
proportion of adults foraging neritically, whilst the majority forage oceanically. Here we describe observed habitat use and
employ ecological niche modelling to identify suitable foraging habitats for animals utilising these two distinct behavioural
strategies. We also investigate how these predicted habitat niches may alter under the influence of climate change induced
oceanic temperature rises. We further contextualise our niche models with fisheries catch data and knowledge of fisheries
‘ hotspots ’ to infer threat from fisheries interaction to this population, for animals employing both strategies.
Our analysis revealed repeated use of coincident oceanic habitat, over multiple seasons, by all smaller loggerhead
turtles, whilst larger neritic foraging turtles occupied continental shelf waters. Modelled habitat niches were spatially
distinct, and under the influence of predicted sea surface temperature rises, there was further spatial divergence of
suitable habitats. Analysis of fisheries catch data highlighted that the observed and modelled habitats for oceanic and neritic
loggerhead turtles could extensively interact with intensive fisheries activity within oceanic and continental shelf waters
of northwest Africa. We suggest that the development and enforcement of sustainable management strategies, specifically multi-national fisheries policy, may begin to address some of these issues; however, these must be flexible and adaptive to accommodate potential range shift for this species.

Research paper thumbnail of Maximum Running Speed of Captive Bar-Headed Geese Is Unaffected by Severe Hypoxia

PLoS ONE, 2014

While bar-headed geese are renowned for migration at high altitude over the Himalayas, previous w... more While bar-headed geese are renowned for migration at high altitude over the Himalayas, previous work on captive birds suggested that these geese are unable to maintain rates of oxygen consumption while running in severely hypoxic conditions. To investigate this paradox, we re-examined the running performance and heart rates of bar-headed geese and barnacle geese (a low altitude species) during exercise in hypoxia. Bar-headed geese (n = 7) were able to run at maximum speeds (determined in normoxia) for 15 minutes in severe hypoxia (7% O 2 ; simulating the hypoxia at 8500 m) with mean heart rates of 46668 beats min 21 . Barnacle geese (n = 10), on the other hand, were unable to complete similar trials in severe hypoxia and their mean heart rate (316 beats.min 21 ) was significantly lower than bar-headed geese. In bar-headed geese, partial pressures of oxygen and carbon dioxide in both arterial and mixed venous blood were significantly lower during hypoxia than normoxia, both at rest and while running. However, measurements of blood lactate in bar-headed geese suggested that anaerobic metabolism was not a major energy source during running in hypoxia. We combined these data with values taken from the literature to estimate (i) oxygen supply, using the Fick equation and (ii) oxygen demand using aerodynamic theory for bar-headed geese flying aerobically, and under their own power, at altitude. This analysis predicts that the maximum altitude at which geese can transport enough oxygen to fly without environmental assistance ranges from 6,800 m to 8,900 m altitude, depending on the parameters used in the model but that such flights should be rare.

Research paper thumbnail of Foraging habitats and migration corridors utilized by a recovering subpopulation of adult female loggerhead sea turtles: implications for conservation

Research paper thumbnail of Satellite tracking derived insights into migration and foraging strategies of male loggerhead turtles in the eastern Atlantic

Journal of Experimental Marine Biology and Ecology, 2013

ABSTRACT In recent years, information about the movements and timing of migration by male sea tur... more ABSTRACT In recent years, information about the movements and timing of migration by male sea turtles has begun to be unraveled. Here, we present the first satellite tracking of male loggerhead sea turtles (Caretta caretta) in the eastern Atlantic. Satellite linked transmitters were attached to five adult males, captured in the near shore waters off Boavista, Republic of Cape Verde. This archipelago hosts the single most important breeding site of loggerhead turtles in the eastern Atlantic. Animals were tracked for periods ranging between 48 and 537 days, including a probable annual remigration to the vicinity of the nesting ground for one turtle. Males showed a variety of movement patterns both during and after the breeding season. Of three males that transmitted for 85, 329 and 537 days, two (the smallest) migrated east and remained in oceanic waters for the tracking period and another (larger turtle) migrated 810 km northeast, to neritic waters off the coast of Mauritania, Western Africa. Results suggest males may show the same size-linked dichotomy in migratory strategies, as has been shown for females from this population.

Research paper thumbnail of How will sea turtles cope with climate change?

Abstract It is now widely accepted that climate change is a significant threat to biodiversity, e... more Abstract It is now widely accepted that climate change is a significant threat to biodiversity, especially to species like sea turtles whose life histories are sensitive to fluctuating environmental conditions. A growing number of studies have begun to investigate and ...

Research paper thumbnail of New findings about the spatial and temporal use of the Eastern Atlantic Ocean by large juvenile loggerhead turtles

Aims Effective conservation of threatened or endangered species requires a robust understanding o... more Aims Effective conservation of threatened or endangered species requires a robust understanding of their spatio-temporal distribution. Although a huge amount is known about the movements of Atlantic adult sea turtles, much less is known about juvenile turtles, and much of the life history model is therefore inferred. We set out to describe the spatio-temporal distribution of juvenile loggerheads turtles found around the Canary Islands.
Location Eastern North Atlantic Ocean.
Methods Between 1999 and 2012, we satellite-tracked 24 healthy large juvenile loggerhead turtles (mean straight carapace length = 47.4 cm, range = 34.6– 54.5 cm) captured in the waters around the Canary Islands. We describe their regional distribution, identify high-use areas and create a model for habitat suitability using minimum convex polygons, density rasters and ensemble ecological niche modelling, integrated with physical and biological environmental data.
Results Turtles used a huge oceanic area (2.5 million km2) with particularly high usage around the Canary Islands, Spain, Portugal, Morocco and Western Sahara. In spring and summer, turtles generally moved further north towards the Iberian Peninsula. Ecological niche modelling identified sea surface temperature as the most important contributory variable to the habitat models. We also recorded three juvenile turtles making westward migrations away from the eastern Atlantic Ocean, presumably back towards their original natal beaches near sexual maturity. Main conclusions The results of the present study provide insight into a significant knowledge gap on the spatio-temporal distribution of large juvenile loggerhead turtles in the eastern Atlantic Ocean. The data highlight that turtles occupy a vast open oceanic area, which hampers the ability of static conservation approaches to afford effective protection. However, ensemble ecological niche modelling highlights key suitable habitat for juvenile loggerhead turtles, which could be used in dynamic conservation protection.

Research paper thumbnail of Evaluating the landscape of fear between apex predatory sharks and mobile sea turtles across a large dynamic seascape

Ecology, 2015

The ‘‘landscape of fear’’ model has been proposed as a unifying concept in ecology, describing, i... more The ‘‘landscape of fear’’ model has been proposed as a unifying concept in ecology, describing, in part, how animals behave and move about in their environment. The basic model predicts that as an animal’s landscape changes from low to high risk of predation, prey species will alter their behavior to risk avoidance. However, studies investigating and evaluating the landscape of fear model across large spatial scales (tens to hundreds of thousands of square kilometers) in dynamic, open, aquatic systems involving apex predators and highly mobile prey are lacking. To address this knowledge gap, we investigated predator–prey relationships between tiger sharks (Galeocerdo cuvier) and loggerhead turtles (Caretta caretta) in the North Atlantic Ocean. This included the use of satellite tracking to examine shark and turtle distributions as well as their surfacing behaviors under varying levels of home range overlap. Our findings revealed patterns that deviated from our a priori predictions based on the landscape of fear model. Specifically, turtles did not alter their surfacing behaviors to risk avoidance when overlap in shark–turtle core home range was high. However, in areas of high overlap with turtles, sharks exhibited modified surfacing behaviors that may enhance predation opportunity. We suggest that turtles may be an important factor in determining shark distribution, whereas for turtles, other life history trade-offs may play a larger role in defining their habitat use. We propose that these findings are a result of both biotic and physically driven factors that independently or synergistically affect predator–prey interactions in this system. These results have implications for evolutionary biology, community ecology, and wildlife conservation. Further, given the difficulty in studying highly migratory marine species, our approach and conclusions may be applied to the study of other predator–prey systems.

Research paper thumbnail of Stable Isotopes Suggest Low Site Fidelity in Bar-Headed Geese ( Anser indicus ) in Mongolia: Implications for Disease Transmission

Waterbirds, 2015

Population connectivity is an important consideration in studies of disease transmission and biol... more Population connectivity is an important consideration in studies of disease transmission and biological conservation, especially with regard to migratory species. Determining how and when different subpopulations intermingle during different phases of the annual cycle can help identify important geographical regions or features as targets for conservation efforts and can help inform our understanding of continental-scale disease transmission. In this study, stable isotopes of hydrogen and carbon in contour feathers were used to assess the degree of molt-site fidelity among Bar-headed Geese (Anser indicus) captured in north-central Mongolia. Samples were collected from actively molting Bar-headed Geese (n = 61), and some individual samples included both a newly grown feather (still in sheath) and an old, worn feather from the bird's previous molt (n = 21). Although there was no difference in mean hydrogen isotope ratios for the old and new feathers, the isotopic variance in old feathers was approximately three times higher than that of the new feathers, which suggests that these birds use different and geographically distant molting locations from year to year. To further test this conclusion, online data and modeling tools from the isoMAP website were used to generate probability landscapes for the origin of each feather. Likely molting locations were much more widespread for old feathers than for new feathers, which supports the prospect of low molt-site fidelity. This finding indicates that population connectivity would be greater than expected based on data from a single annual cycle, and that disease spread can be rapid even in areas like Mongolia where Bar-headed Geese generally breed in small isolated groups.

Research paper thumbnail of Investigating the potential impacts of climate change on a marine turtle population

Global Change Biology

Recent increases in global temperatures have affected the phenology and survival of many species ... more Recent increases in global temperatures have affected the phenology and survival of many species of plants and animals. We investigated a case study of the effects of potential climate change on a thermally sensitive species, the loggerhead sea turtle, at a breeding location at the northerly extent of the range of regular nesting in the United States. In addition to the physical limits imposed by temperature on this ectothermic species, sea turtle primary sex ratio is determined by the temperature experienced by eggs during the middle third of incubation. We recorded sand temperatures and used historical air temperatures (ATs) at Bald Head Island, NC, to examine past and predict future sex ratios under scenarios of warming. There were no significant temporal trends in primary sex ratio evident in recent years and estimated mean annual sex ratio was 58% female. Similarly, there were no temporal trends in phenology but earlier nesting and longer nesting seasons were correlated with wa...

Research paper thumbnail of An assessment of marine turtles in The Gambia Phase I Report

Page 1. An Assessment of Marine Turtles in The Gambia Phase I Report Lucy A. Hawkes1, Matthew J. ... more Page 1. An Assessment of Marine Turtles in The Gambia Phase I Report Lucy A. Hawkes1, Matthew J. Witt1,Ibrahima Mat Dia2, Ousaynou Touray3 & Brendan J. Godley1 1 Marine Turtle Research Group, University of Exeter, Cornwall Campus, ...

Research paper thumbnail of Oceanic loggerhead turtles Caretta caretta associate with thermal fronts: evidence from the Canary Current Large Marine Ecosystem

Marine Ecology Progress Series, 2015

ABSTRACT Oceanographic fronts are physical interfaces between water masses that differ in propert... more ABSTRACT Oceanographic fronts are physical interfaces between water masses that differ in properties such as temperature, salinity, turbidity and chlorophyll a enrichment. Bio-physical coupling along fronts can lead to the development of pelagic biodiversity hotspots. A diverse range of marine vertebrates have been shown to associate with fronts, using them as foraging and migration habitats. Elucidation of the ecological significance of fronts generates a better understanding of marine ecosystem functioning, conferring opportunities to improve management of anthropogenic activities in the oceans. This study presents novel insights into the oceanographic drivers of habitat use in a population of marine turtles characterised by an oceanic-neritic foraging dichotomy. Using satellite tracking data from adult female loggerhead turtles Caretta caretta nesting at Cape Verde (n = 12), we tested the hypothesis that oceanic-foraging loggerheads associate with mesocale (10s to 100s of km) thermal fronts. We used high-resolution (1 km) composite front mapping to characterise frontal activity in the Canary Current Large Marine Ecosystem over 2 temporal scales: (1) seasonal front frequency and (2) 7 d front metrics. Our use-availability analysis indicated that oceanic loggerheads show a preference for the highly productive upwelling region between Cape Verde and mainland Africa, an area of intense frontal activity. Within the upwelling region, turtles appear to forage epipelagically around mesoscale thermal fronts, exploiting profitable foraging opportunities resulting from physical aggregation of prey.

Research paper thumbnail of How Bar-Headed Geese Fly Over the Himalayas

Physiology (Bethesda, Md.), 2015

Bar-headed geese cross the Himalayas on one of the most iconic high-altitude migrations in the wo... more Bar-headed geese cross the Himalayas on one of the most iconic high-altitude migrations in the world. Heart rates and metabolic costs of flight increase with elevation and can be near maximal during steep climbs. Their ability to sustain the high oxygen demands of flight in air that is exceedingly oxygen-thin depends on the unique cardiorespiratory physiology of birds in general along with several evolved specializations across the O2 transport cascade.

Research paper thumbnail of On the Front Line: frontal zones as priority at-sea conservation areas for mobile marine vertebrates

Journal of Applied Ecology, 2014

ABSTRACT 1.Identifying priority areas for marine vertebrate conservation is complex because speci... more ABSTRACT 1.Identifying priority areas for marine vertebrate conservation is complex because species of conservation concern are highly mobile, inhabit dynamic habitats and are difficult to monitor. 2.Many marine vertebrates are known to associate with oceanographic fronts – physical interfaces at the transition between water masses – for foraging and migration, making them important candidate sites for conservation. Here, we review associations between marine vertebrates and fronts and how they vary with scale, regional oceanography and foraging ecology. 3.Accessibility, spatiotemporal predictability and relative productivity of front-associated foraging habitats are key aspects of their ecological importance. Predictable mesoscale (10s–100s km) regions of persistent frontal activity (‘frontal zones’) are particularly significant. 4.Frontal zones are hotspots of overlap between critical habitat and spatially explicit anthropogenic threats, such as the concentration of fisheries activity. As such, they represent tractable conservation units, in which to target measures for threat mitigation. 5.Front mapping via Earth observation (EO) remote sensing facilitates identification and monitoring of these hotspots of vulnerability. Seasonal or climatological products can locate biophysical hotspots, while near-real-time front mapping augments the suite of tools supporting spatially dynamic ocean management. 6.Synthesis and applications. Frontal zones are ecologically important for mobile marine vertebrates. We surmise that relative accessibility, predictability and productivity are key biophysical characteristics of ecologically significant frontal zones in contrasting oceanographic regions. Persistent frontal zones are potential priority conservation areas for multiple marine vertebrate taxa and are easily identifiable through front mapping via EO remote sensing. These insights are useful for marine spatial planning and marine biodiversity conservation, both within Exclusive Economic Zones and in the open oceans

Research paper thumbnail of Supplementary Information: The roller coaster flight strategy of bar-headed geese conserves energy during Himalayan migrations

Research paper thumbnail of Biochemical Indices and Life Traits of Loggerhead Turtles (Caretta caretta) from Cape Verde Islands

PLoS ONE, 2014

The loggerhead turtle (Caretta caretta) is an endangered marine reptile for whom assessing popula... more The loggerhead turtle (Caretta caretta) is an endangered marine reptile for whom assessing population health requires knowledge of demographic parameters such as individual growth rate. In Cape Verde, as within several populations, adult female loggerhead sea turtles show a size-related behavioral and trophic dichotomy. While smaller females are associated with oceanic habitats, larger females tend to feed in neritic habitats, which is reflected in their physiological condition and in their offspring. The ratio of RNA/DNA provides a measure of cellular protein synthesis capacity, which varies depending on changes in environmental conditions such as temperature and food availability. The purpose of this study was to evaluate the combined use of morphometric data and biochemical indices as predictors of the physiological condition of the females of distinct sizes and hatchlings during their nesting season and how temperature may influence the physiological condition on the offspring. Here we employed biochemical indices based on nucleic acid derived indices (standardized RNA/DNA ratio-sRD, RNA concentration and DNA concentration) in skin tissue as a potential predictor of recent growth rate in nesting females and hatchling loggerhead turtles. Our major findings were that the physiological condition of all nesting females (sRD) decreased during the nesting season, but that females associated with neritic habitats had a higher physiological condition than females associated with oceanic habitats. In addition, the amount of time required for a hatchling to right itself was negatively correlated with its physiological condition (sRD) and shaded nests produced hatchlings with lower sRD. Overall, our results showed that nucleic acid concentrations and ratios of RNA to DNA are an important tool as potential biomarkers of recent growth in marine turtles. Hence, as biochemical indices of instantaneous growth are likely temperature-, size- and age-dependent, the utility and validation of these indices on marine turtles stocks deserves further study.

Research paper thumbnail of The potential future influence of sea level rise on leatherback turtle nests

Journal of Experimental Marine Biology and Ecology, 2014

ABSTRACT Climate change models predict sea level rise and increased intensity of storms and hurri... more ABSTRACT Climate change models predict sea level rise and increased intensity of storms and hurricanes in tropical sea turtle nesting areas. These factors could significantly increase beach inundation and erosion, thus affecting water content of sea turtle nesting beaches. Here, we conducted a field and laboratory study of how sand water content is related to embryonic development and hatching success of leatherback turtle nests. Moreover, we have experimentally incubated eggs of this species in beach sand under standardized conditions, but at different realistic levels of sand water content, varying from 1% to 12%. On the beaches, females nested from the intertidal zone to the lower part of the sand vegetation dunes, where nests were exposed to a wide range of sand water contents that ranged from 0.8% to 22%. However, both field and experimental studies revealed a strong negative correlation between sand water content and emergence success (field study: r = − 0.73, P < 0.0001; experiment: r = − 0.84, P < 0.0001). In the field, mean emergence success varied from 0% for the wettest nests to 64% for the driest ones. Nests in wet sand suffered higher mortality, primarily in the earlier developmental stages. Eggs incubated in the driest sand lost mass, but there were no significant effects on hatchling mass or run speed compared to eggs that gained water during incubation. However, hatchling straight carapace length (SCL) was greater in eggs from the driest treatment. The results of the present study inform management of change under future climate change sea level rise scenarios, suggesting that leatherback turtle nesting success should be expected to decrease.

Research paper thumbnail of The impacts of climate change on marine turtle reproductive success

Coastal Conservation, 2013

Research paper thumbnail of High rates of growth recorded for hawksbill sea turtles in Anegada, British Virgin Islands

Management of species of conservation concern requires knowledge of demographic parameters, such ... more Management of species of conservation concern requires knowledge of demographic parameters, such as rates of recruitment, survival, and growth. In the Caribbean, hawksbill turtles (Eretmochelys imbricata) have been historically exploited in huge numbers to satisfy trade in their shells and meat. In the present study, we estimated growth rate of juvenile hawksbill turtles around Anegada, British Virgin Islands, using capture-mark-recapture of 59 turtles over periods of up to 649 days. Turtles were recaptured up to six times, having moved up to 5.9 km from the release location. Across all sizes, turtles grew at an average rate of 9.3 cm year À1 (range 2.3-20.3 cm year À1 ), and gained mass at an average of 3.9 kg year À1 (range 850 g-16.1 kg year À1 ). Carapace length was a significant predictor of growth rate and mass gain, but there was no relationship between either variable and sea surface temperature. These are among the fastest rates of growth reported for this species, with seven turtles growing at a rate that would increase their body size by more than half per year (51-69% increase in body length). This study also demonstrates the importance of shallow water reef systems for the developmental habitat for juvenile hawksbill turtles. Although growth rates for posthatching turtles in the pelagic, and turtles larger than 61 cm, are not known for this population, the implications of this study are that Caribbean hawksbill turtles in some areas may reach body sizes suggesting sexual maturity in less time than previously considered.

Research paper thumbnail of Contextualising the Last Survivors: Population Structure of Marine Turtles in the Dominican Republic

PLoS ONE, 2013

Nesting by three species of marine turtles persists in the Dominican Republic, despite historic t... more Nesting by three species of marine turtles persists in the Dominican Republic, despite historic threats and long-term population decline. We conducted a genetic survey of marine turtles in the Dominican Republic in order to link them with other rookeries around the Caribbean. We sequenced a 740bp fragment of the control region of the mitochondrial DNA of 92 samples from three marine turtle species [hawksbill (n = 48), green (n = 2) and leatherback (n = 42)], and incorporated published data from other nesting populations and foraging grounds. The leatherback turtle (Dermochelys coriacea) in the Dominican Republic appeared to be isolated from Awala-Yalimapo, Cayenne, Trinidad and St. Croix but connected with other Caribbean populations. Two distinct nesting populations of hawksbill turtles (Eremochelys imbricata) were detected in the Dominican Republic and exhibited interesting patterns of connectivity with other nesting sites and juvenile and adult male foraging aggregations. The green sea turtle (Chelonia mydas) has almost been extirpated from the Dominican Republic and limited inference could be made from our samples. Finally, results were compared with Lagrangian drifting buoys and published Lagrangian virtual particles that travelled through the Dominican Republic and Caribbean waters. Conservation implications of sink-source effects or genetic isolation derived from these complex inter-connections are discussed for each species and population.

Research paper thumbnail of The roller coaster flight strategy of bar-headed geese conserves energy during Himalayan migrations

Research paper thumbnail of Modelling the niche for a marine vertebrate: a case study incorporating behavioural plasticity, proximate threats and climate change

Th e integration of satellite telemetry, remotely sensed environmental data, and habitat/environm... more Th e integration of satellite telemetry, remotely sensed environmental data, and habitat/environmental modelling has
provided for a growing understanding of spatial and temporal ecology of species of conservation concern. Th e Republic of
Cape Verde comprises the only substantial rookery for the loggerhead turtle Caretta caretta in the eastern Atlantic. A size
related dichotomy in adult foraging patterns has previously been revealed for adult sea turtles from this population with a
proportion of adults foraging neritically, whilst the majority forage oceanically. Here we describe observed habitat use and
employ ecological niche modelling to identify suitable foraging habitats for animals utilising these two distinct behavioural
strategies. We also investigate how these predicted habitat niches may alter under the influence of climate change induced
oceanic temperature rises. We further contextualise our niche models with fisheries catch data and knowledge of fisheries
‘ hotspots ’ to infer threat from fisheries interaction to this population, for animals employing both strategies.
Our analysis revealed repeated use of coincident oceanic habitat, over multiple seasons, by all smaller loggerhead
turtles, whilst larger neritic foraging turtles occupied continental shelf waters. Modelled habitat niches were spatially
distinct, and under the influence of predicted sea surface temperature rises, there was further spatial divergence of
suitable habitats. Analysis of fisheries catch data highlighted that the observed and modelled habitats for oceanic and neritic
loggerhead turtles could extensively interact with intensive fisheries activity within oceanic and continental shelf waters
of northwest Africa. We suggest that the development and enforcement of sustainable management strategies, specifically multi-national fisheries policy, may begin to address some of these issues; however, these must be flexible and adaptive to accommodate potential range shift for this species.

Research paper thumbnail of Maximum Running Speed of Captive Bar-Headed Geese Is Unaffected by Severe Hypoxia

PLoS ONE, 2014

While bar-headed geese are renowned for migration at high altitude over the Himalayas, previous w... more While bar-headed geese are renowned for migration at high altitude over the Himalayas, previous work on captive birds suggested that these geese are unable to maintain rates of oxygen consumption while running in severely hypoxic conditions. To investigate this paradox, we re-examined the running performance and heart rates of bar-headed geese and barnacle geese (a low altitude species) during exercise in hypoxia. Bar-headed geese (n = 7) were able to run at maximum speeds (determined in normoxia) for 15 minutes in severe hypoxia (7% O 2 ; simulating the hypoxia at 8500 m) with mean heart rates of 46668 beats min 21 . Barnacle geese (n = 10), on the other hand, were unable to complete similar trials in severe hypoxia and their mean heart rate (316 beats.min 21 ) was significantly lower than bar-headed geese. In bar-headed geese, partial pressures of oxygen and carbon dioxide in both arterial and mixed venous blood were significantly lower during hypoxia than normoxia, both at rest and while running. However, measurements of blood lactate in bar-headed geese suggested that anaerobic metabolism was not a major energy source during running in hypoxia. We combined these data with values taken from the literature to estimate (i) oxygen supply, using the Fick equation and (ii) oxygen demand using aerodynamic theory for bar-headed geese flying aerobically, and under their own power, at altitude. This analysis predicts that the maximum altitude at which geese can transport enough oxygen to fly without environmental assistance ranges from 6,800 m to 8,900 m altitude, depending on the parameters used in the model but that such flights should be rare.

Research paper thumbnail of Foraging habitats and migration corridors utilized by a recovering subpopulation of adult female loggerhead sea turtles: implications for conservation

Research paper thumbnail of Satellite tracking derived insights into migration and foraging strategies of male loggerhead turtles in the eastern Atlantic

Journal of Experimental Marine Biology and Ecology, 2013

ABSTRACT In recent years, information about the movements and timing of migration by male sea tur... more ABSTRACT In recent years, information about the movements and timing of migration by male sea turtles has begun to be unraveled. Here, we present the first satellite tracking of male loggerhead sea turtles (Caretta caretta) in the eastern Atlantic. Satellite linked transmitters were attached to five adult males, captured in the near shore waters off Boavista, Republic of Cape Verde. This archipelago hosts the single most important breeding site of loggerhead turtles in the eastern Atlantic. Animals were tracked for periods ranging between 48 and 537 days, including a probable annual remigration to the vicinity of the nesting ground for one turtle. Males showed a variety of movement patterns both during and after the breeding season. Of three males that transmitted for 85, 329 and 537 days, two (the smallest) migrated east and remained in oceanic waters for the tracking period and another (larger turtle) migrated 810 km northeast, to neritic waters off the coast of Mauritania, Western Africa. Results suggest males may show the same size-linked dichotomy in migratory strategies, as has been shown for females from this population.