Foraging in a dynamic environment: movement and stable isotope ecology of marine top predators breeding at the Prince Edward Archipelago

Marine ecosystems are experiencing rapid changes due to climate change. The associated temporal and spatial changes in resource distribution impacts on the foraging behaviour of marine top predators. If these changes negatively affect the ability of marine predators to forage efficiently, there may be dire consequences for their populations. However, evidence of foraging plasticity during adverse conditions, or generalist foraging behaviour, can allow inference about the resilience of species to environmental change and provide essential knowledge towards effective and proactive conservation measures. I examined plasticity in the trophic ecology of 12 marine predator species breeding on Marion Island, southern Indian Ocean, over three years (2015 – 2018), a period characterized by pronounced environmental variability. Firstly, I correlated behavioural states inferred along the GPS tracks of incubating wandering, grey-headed, sooty and light-mantled albatrosses to environmental variables that are indicative of biologically productive oceanographic features. Secondly, I analysed δ13C and δ15N blood values in 12 marine predator species (the afore-mentioned albatrosses as well as king, gentoo, macaroni and eastern rockhopper penguins, northern and southern giant petrels and Antarctic and sub-Antarctic fur seals) over two seasons: summer and autumn. My results revealed that the foraging behaviour of all the species is, to some degree, either plastic (temporally variable isotopic niche) or general (large isotopic niche which remained similar over time), except for the king penguin (small isotopic niche which remained similar over time), a known foraging specialist. Furthermore, despite their dynamic foraging behaviour, resource partitioning among the predators was maintained over time. Due to the ease and relatively low cost of collecting tissues for stable isotope analysis it has the potential to be a powerful tool to monitor the trophic ecology of marine predators. I thus used my simultaneously collected dataset of GPS tracks with the stable isotope blood compositions to investigate some of the assumptions underlying the inferences made from marine predator δ13C and δ15N blood values. I reconstructed species- and guild- specific δ13C and δ15N isoscapes for eight seabird species. Following this, I coupled individual-based movement models of northern giant petrels with global marine isotope models to explore the sensitivity of tissue δ13C values to a range of extrinsic (environmental) and intrinsic (behavioural, physiological) drivers. My results demonstrate the strong influence of reference isoscapes on the inference of stable isotope compositions of marine predators. Furthermore, I show that caution should be used when using non-species-specific or temporally inaccurate isoscapes. I furthermore demonstrate that biological interactions, such as competition for food resources, either past or present, as well as spatio-temporal distribution of food patches strongly influence the foraging behaviour of marine predators. These findings highlight the importance of integrating biological interactions in species distribution models which are used to predict possible distributional shifts of marine predators in the context of global changes. My thesis further developed previously available methods and presents a novel approach to investigate sources of variance in the stable isotopic composition of animals’ tissues

Foraging ecology of the gentoo penguin, pygoscelis papua, at Marion Island

The distribution and subsequent availability of marine predators’ prey is highly variable and is linked to fluctuating oceanographic parameters. It is well documented that annual breeding success of seabirds is related to the temporal availability of prey. Knowledge of a seabird’s diet and at sea distribution is therefore critical in deducing the effect of a fluctuating environment on a seabirds’ population and, furthermore, to understand seabirds role in the environment. The gentoo penguin population at sub-Antarctic Marion Island experienced a decline of 52% between 1994 and 2012. It has been speculated that long term changes in the local marine environment, due to a southward shift of the sub-Antarctic Front (SAF), and subsequent changes in prey availability is the ultimate causal factor. Therefore, this thesis investigates the temporal variation in the diet these birds over three years, through the use of stomach content samples. It then investigates whether the composition of the diet has changed over the long term (approximately 18 years). Additionally, the at sea distribution of these birds was investigated using temperature-depth recorders (TDRs) and global positioning system (GPS) devices. This study represents the first to investigate variation in the diet over three years and over the long term. It is also the first study to track these birds fine scale movement. Over three years, the diet exhibited a high degree of variability. The birds primarily foraged on the fish, Lepidonotothen larseni and the crustaceans, Nauticaris marionis and Euphausia vallentiniy. Over three years, L. larseni became increasingly more important during the breeding season. This was attributed to an increase in availability of these fish during this time, as this time corresponded to the transition of these fish from the larval pelagic phase to the benthic adult phase. Furthermore, the proportions of N. marionis and E. vallentini in the diet varied significantly among years. This variation is possibly a result of the highly variable latitudinal position of the SAF. The diet changed over the long term. There was significantly less N. marionis and more E. vallentini in the diet during more recent years. The long term southward shift of the SAF is considered to be a leading cause of these significant changes in the diet. The shallow inter-island shelf between Marion and Prince Edward Island was an important foraging area possibly due to predictable prey resources. In addition, these birds exhibited an important and possibly unique foraging strategy. They performed short self-maintenance trips where after they return to land to roost for the night. The following day these trips were followed by a longer foraging trip that was followed by chick provisioning. This strategy is unique among seabirds longer trips are associated with self-maintenance and not chick provisioning. This study has provided important knowledge of the foraging ecology of the gentoo penguin at sub-Antarctic Marion Island. It highlights the necessity for continuation of diet and tracking studies of these birds if we are to fully understand the ultimate factors that are causing the decline in their breeding success and population numbers

Foraging in a dynamic environment: movement and stable isotope ecology of marine top predators breeding at the Prince Edward Archipelago

Marine ecosystems are experiencing rapid changes due to climate change. The associated temporal and spatial changes in resource distribution impacts on the foraging behaviour of marine top predators. If these changes negatively affect the ability of marine predators to forage efficiently, there may be dire consequences for their populations. However, evidence of foraging plasticity during adverse conditions, or generalist foraging behaviour, can allow inference about the resilience of species to environmental change and provide essential knowledge towards effective and proactive conservation measures. I examined plasticity in the trophic ecology of 12 marine predator species breeding on Marion Island, southern Indian Ocean, over three years (2015 – 2018), a period characterized by pronounced environmental variability. Firstly, I correlated behavioural states inferred along the GPS tracks of incubating wandering, grey-headed, sooty and light-mantled albatrosses to environmental variables that are indicative of biologically productive oceanographic features. Secondly, I analysed δ13C and δ15N blood values in 12 marine predator species (the afore-mentioned albatrosses as well as king, gentoo, macaroni and eastern rockhopper penguins, northern and southern giant petrels and Antarctic and sub-Antarctic fur seals) over two seasons: summer and autumn. My results revealed that the foraging behaviour of all the species is, to some degree, either plastic (temporally variable isotopic niche) or general (large isotopic niche which remained similar over time), except for the king penguin (small isotopic niche which remained similar over time), a known foraging specialist. Furthermore, despite their dynamic foraging behaviour, resource partitioning among the predators was maintained over time. Due to the ease and relatively low cost of collecting tissues for stable isotope analysis it has the potential to be a powerful tool to monitor the trophic ecology of marine predators. I thus used my simultaneously collected dataset of GPS tracks with the stable isotope blood compositions to investigate some of the assumptions underlying the inferences made from marine predator δ13C and δ15N blood values. I reconstructed species- and guild- specific δ13C and δ15N isoscapes for eight seabird species. Following this, I coupled individual-based movement models of northern giant petrels with global marine isotope models to explore the sensitivity of tissue δ13C values to a range of extrinsic (environmental) and intrinsic (behavioural, physiological) drivers. My results demonstrate the strong influence of reference isoscapes on the inference of stable isotope compositions of marine predators. Furthermore, I show that caution should be used when using non-species-specific or temporally inaccurate isoscapes. I furthermore demonstrate that biological interactions, such as competition for food resources, either past or present, as well as spatio-temporal distribution of food patches strongly influence the foraging behaviour of marine predators. These findings highlight the importance of integrating biological interactions in species distribution models which are used to predict possible distributional shifts of marine predators in the context of global changes. My thesis further developed previously available methods and presents a novel approach to investigate sources of variance in the stable isotopic composition of animals’ tissues

Ectoparasite burdens of the Damaraland mole-rat (Fukomys damarensis) from Southern Africa

Damaraland mole-rats (Fukomys damarensis) of the family Bathyergidae are widely distributed subterranean rodents in sub-Saharan Africa. No parasites have ever been reported for this species and only 1 ectoparasite is described for the entire genus. In the current study ectoparasites were collected from individuals captured at 3 localities in South Africa and Namibia to document the ectoparasite community of F. damarensis, investigate their aggregation patterns and evaluate the influence of season on ectoparasite burden. A total of 2,071 arthropods from 9 mite taxa and 1 louse species (Eulinognathus hilli) were collected from 293 hosts sampled. Of these 5 mite species (Androlaelaps scapularis, A. capensis, A. tauffliebi, Radfordia sp. and unidentified chiggers) and the louse were parasites while the remainder were soil mites. All ectoparasites were highly aggregated and the species richness as well as the prevalence and abundance of 4 of them were significantly greater in summer compared to winter, possibly as a result of seasonal changes in rainfall patterns affecting the ectoparasites and/or host behavior.NRF-SARChI chair for Mammalian Behavioural Ecology and Physiology, the NRF and the University of Pretoria.http://digitalcommons.unl.edu/jrnlparasitologyhb201

Habitat preferences of Phoebetria albatrosses in sympatry and allopatry

Aim: Competition is often proposed to drive niche segregation along multiple axes in speciose communities. Understanding spatial partitioning of foraging areas is particularly important in species that are constrained to a central place. We present a natural experiment examining variation in habitat preferences of congeneric Southern Ocean predators in sympatry and allopatry. Our aim was to ascertain consistency of habitat preferences within species, and to test whether preferences changed in the presence of the congener. Location: Southern Hemisphere. Taxon: Multiple colonies of both species within the genus Phoebetria (sooty albatrosses). Methods: The two Phoebetria albatrosses breed on islands located from ~37–55°S – sooty albatrosses (P. fusca) in the north and light-mantled albatrosses (P. palpebrata) in the south – with sympatric overlap at locations ~46–49°S. We analysed GPS and PTT tracks from 87 individuals and multiple remotely sensed environmental variables using GAMs, to determine and compare the key factors influencing habitat preference for each species at each breeding colony. Results While foraging habitat preferences are consistent in light-mantled albatrosses, there is divergence of preferences in sooty albatrosses depending on whether they are in sympatry with their congener or in allopatry. Main Conclusions This study represents the most comprehensive work on this genus to date and highlights how habitat preferences and behavioural plasticity may influence species distributions under different competitive conditions

A critical assessment of marine predator isoscapes within the southern Indian Ocean

Background: Precise and accurate retrospective geolocation of marine predators via their tissues' isotopic composition relies on quality reference maps of relevant isotopic gradients ("isoscapes"). Additionally, a good working knowledge of any discrimination factors that may offset a marine predator's isotopic composition from baseline isotopic values, as well as tissue specific retention rates, are imperative. We provide a critical assessment of inter-specific differences among marine predator-level isoscapes within the Indian Sector of the Southern Ocean. Methods: We combined fine-scale GPS tracking data and concurrent blood plasma δ13C and δ15N values of eight seabird species (three albatross, two giant petrel and three penguin species) breeding at Marion Island to produce species- and guild-specific isoscapes. Results: Overall, our study revealed latitudinal spatial gradients in both δ13C and δ15N for far-ranging seabirds (albatrosses and giant petrels) as well as inshore-offshore gradients for near-ranging seabirds (penguins). However, at the species level, latitudinal spatial gradients were not reflected in the δ13C and δ15N isoscapes of two and three, respectively, of the five far-ranging species studied. It is therefore important when possible to estimate and apply species-specific isoscapes or have a good understanding of any factors and pathways affecting marine predators' isotopic composition when estimating the foraging distribution of marine predators via their tissues' stable isotope compositions. Conclusions: Using a multi-species approach, we provide evidence of large and regional scale systematic spatial variability of δ13C and δ15N at the base of the marine food web that propagates through trophic levels and is reflected in the isotopic composition of top predators' tissues.</p

Ectoparasite burdens of the Damaraland mole-rat (Fukomys Damarensis) from Southern Africa

Damaraland mole-rats (Fukomys damarensis) of the family Bathyergidae are widely distributed subterranean rodents in sub-Saharan Africa. No parasites have ever been reported for this species and only 1 ectoparasite is described for the entire genus. In the current study ectoparasites were collected from individuals captured at 3 localities in South Africa and Namibia to document the ectoparasite community of F. damarensis, investigate their aggregation patterns, and evaluate the influence of season on ectoparasite burden. A total of 2,071 arthropods from 9 mite taxa and 1 louse species (Eulinognathus hilli) were collected from 293 hosts sampled. Of these, 5 mite species (Androlaelaps scapularis, Androlaelaps capensis, Androlaelaps tauffliebi, Radfordia sp., and unidentified chiggers) and the louse were parasites while the remainder was soil mites. All ectoparasites were highly aggregated and the species richness as well as the prevalence and abundance of 4 of them were significantly greater in summer compared to winter, possibly as a result of seasonal changes in rainfall patterns affecting the ectoparasites, host behavior, or bot

Foraging behaviour and habitat-use drives niche segregation in sibling seabird species: Niche segregation in giant petrels

To mediate competition, similar sympatric species are assumed to use different resources, or the same but geographically separated resources. The two giant petrels (Macronectes spp.) are intriguing in that they are morphologically similar seabirds with overlapping diets and distributions. To better understand the mechanisms allowing their coexistence, we investigated intra- and interspecific niche segregation at Marion Island (Southern Indian Ocean), one of the few localities where they breed in sympatry. We used GPS tracks from 94 individuals and remote-sensed environmental data to quantify habitat use, combined with blood carbon and nitrogen stable isotope ratios from 90 individuals to characterize their foraging habitat and trophic ecology. Females of both species made distant at-sea foraging trips and fed at a similar trophic level. However, they used distinct pelagic habitats. By contrast, males of both species mainly foraged on or near land, resulting in significant sexual segregation, but high interspecific habitat and diet overlap. However, some males showed flexible behavioural strategies, also making distant, pelagic foraging trips. Using contemporaneous tracking, environmental and stable isotope data we provide a clear example of how sympatric sibling species can be segregated along different foraging behaviour dimensions.</p

Sensitivity of δ¹³C values of seabird tissues to combined spatial, temporal and ecological drivers: a simulation approach

Biologging technologies have revolutionised our understanding of the foraging ecology and life history traits of marine predators, allowing for high resolution information about location, and in some cases, foraging behaviour of wild animals. At the same time, stable isotope ecologists have independently developed methods to infer location and foraging ecology (trophic geography). To date, relatively few studies have combined these two approaches, despite the potential wealth of complementary information. In marine systems, spatial and trophic information are coded in the isotopic composition of carbon and nitrogen in animal tissues, but interpretation of isotope values is limited by both the lack of reference maps (isoscapes) needed to relate the isotopic composition of an animal's tissues to a location, and the relatively large number of variables that could influence tissue isotope compositions. Simulation modelling can help to interpret measured tissue isotope compositions of migratory animals in the context of spatio-temporally dynamic isotopic baselines. Here, we couple individual-based movement models with global marine isotope models to explore the sensitivity of tissue δ13C values to a range of extrinsic (environmental) and intrinsic (behavioural, physiological) drivers. We use in-silico experiments to simulate isotopic compositions expected for birds exhibiting different movement and foraging behaviours and compare these simulated data to isotopic data recovered from biologger-equipped female northern giant petrels Macronectes halli incubating eggs on sub-Antarctic Marion Island. Our simulations suggest that in the studied system, time is a strong driver of isotopic variance. Accordingly, this implies that caution should be used when comparing δ13C values of marine predators’ tissues between seasons and years. We show how an in-silico experimental approach can be used to explore the sensitivity of animal tissue isotopic compositions to complex and often interacting drivers. Appreciation of the principle drivers behind isotopic variance specific to a given animal and geographic context can enhance inferences of geolocation as well as foraging behaviour, and can be applied to any mobile predator. Models can be relativey simple or complex and multi-layered depending on the level of ecological realism required. Future investigations can use other isoscapes, including terrestrial isoscapes and more complex or different movement models.</p