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Sex-specific macronutrient foraging strategies in a highly successful marine predator: the Australasian gannet

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The foraging challenge for predators is to find and capture food with adequate levels of energy and nutrients. Marine predators require particularly sophisticated foraging strategies that enable them to balance self- and offspring-feeding, and also in many circumstances simultaneously consider the nutritional constraints of their partners. Here we combined the use of dietary analysis, proximate composition and nutritional geometry (right-angled mixture triangle nutritional models) to examine the macronutrient preferences of Australasian gannets (Morus serrator) at Farewell Spit gannetry in New Zealand. Our results showed intra- and inter-specific variation in the protein, lipid and water composition of prey captured by our sample of 111 Australasian gannets. In addition, we observed significant differences in the Australasian gannets’ nutritional niche between seasons. We provide evidence of sex-specific macronutrient foraging strategies in a successful marine predator in the wild. We have shown that in spite of fluctuations in the nutritional composition of foods available to Australasian gannets, males consistently capture prey with higher protein-to-lipid ratios and lower lipid-to-water ratios than females. These results aid to better understand the evolutionary relationship between macronutrient selection and sex-specific traits in wild animals. They also suggest an incentive for these predators to combine individually imbalanced but nutritionally complementary foods to achieve dietary balance, further highlighting the likelihood that prey selection is guided by the balance of macronutrients, rather than energy alone.
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Mar Biol (2016) 163:93
DOI 10.1007/s00227-016-2874-2
ERRATUM
Erratum to: Sex‑specific macronutrient foraging strategies in a
highly successful marine predator: the Australasian gannet
Gabriel E. Machovsky‑Capuska
1,2,3
· Alistair M. Senior
2,4
· Emily C. Benn
3
·
Alice H. Tait
5
· Rob Schuckard
6
· Karen A. Stockin
5
· Willie Cook
6
· Mike Ogle
7
·
Katherine Barna
2
· David Melville
6
· Belinda Wright
1
· Cameron Purvin
5
·
David Raubenheimer
1,2,3
© Springer-Verlag Berlin Heidelberg 2016
Erratum to: Mar Biol (2016) 163:75
DOI 10.1007/s00227‑016‑2841‑y
Unfortunately, the second research question was incorrectly
published in the “Introduction” and “Results” sections of
the original article. The correct question is given below.
Do female and male Australasian gannets target different
prey combinations?
The online version of the original article can be found under
doi:10.1007/s00227-016-2841-y.
* Gabriel E. Machovsky-Capuska
g.machovsky@sydney.edu.au
1
School of Life and Environmental Sciences, Faculty
of Veterinary Sciences, The University of Sydney, Sydney,
Australia
2
Charles Perkins Centre, The University of Sydney, Sydney,
Australia
3
School of Life and Environmental Sciences, The University
of Sydney, Sydney, Australia
4
School of Mathematics and Statistics, The University
of Sydney, Sydney, Australia
5
Institute of Natural and Mathematical Sciences, Massey
University, Auckland, New Zealand
6
Ornithological Society of New Zealand, Wellington,
New Zealand
7
Department of Conservation, Golden Bay Area, Takaka,
New Zealand
... If nutritional information was unavailable for a prey species, average values for closely related taxa (same genus or family) with similar ecological attributes were used (Supplementary Table S7; Eder and Lewis, 2005). To estimate the composition of the diet, the nutritional composition of each stomach content sample (%P, %L, %W) was calculated using the proximate composition of the prey species present, multiplied by their proportional contribution to the total reconstructed mass of the stomach sample (Machovsky-Capuska et al., 2016c). To calculate the energy density of each stomach sample (E density , kJ g −1 reconstructed wet mass stomach content), macronutrients were converted to metabolisable energy using conversion factors of 17 and 37 kJ g −1 for protein and lipid, respectively (NRC, 1989). ...
... To explore whether sex or size influenced dietary nutritional components, separate linear models (LM) were fitted to each of %P, %L, %W, P:L (protein to lipid ratio), E density and E shark (Machovsky-Capuska et al., 2016c). Prior to analysis, %P, %L and %W were logit transformed and P:L was natural log transformed. ...
... For example, batoids and Australian salmon would enable similar high %P intake for both males and females, respectively, albeit with different %L, which could be moderated by mixing with other complementary prey species that were lower in %P and %L. Variation in growth rates, size at maturity and reproduction (Francis, 1996;Pratt, 1996;Hamady et al., 2014;Natanson and Skomal, 2015) likely impose different physiological demands for male and female white sharks, a condition where sex-specific macronutrient foraging might be expected (Machovsky-Capuska et al., 2016c). Indeed, such physiological differences are a proposed driver behind sex-specific occurrences of sub-adult and adult white sharks at pinniped colonies (Bruce and Bradford, 2015). ...
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Establishing diets and dietary generalism in marine top predators is critical for understanding their ecological roles and responses to environmental fluctuations. Nutrition plays a key mediatory role in species-environment interactions, yet descriptions of marine predators’ diets are usually limited to the combinations of prey species consumed. Here we combined stomach contents analysis (n = 40), literature prey nutritional data and a multidimensional nutritional niche framework to establish the diet and niche breadths of white sharks (Carcharodon carcharias; mean ± SD precaudal length = 187.9 ± 46.4 cm, range = 123.8–369.0 cm) caught incidentally off New South Wales (NSW), Australia. Our nutritional framework also facilitated the incorporation of existing literature diet information for South African white sharks to further evaluate nutritional niches across populations and sizes. Although teleosts including pelagic eastern Australian salmon (Arripis trutta) were the predominant prey for juvenile white sharks in NSW, the diversity of benthic and reef-associated species and batoids suggests regular benthic foraging. Despite a small sample size (n = 18 and 19 males and females, respectively), there was evidence of increased batoid consumption by males relative to females, and a potential size-based increase in shark and mammal prey consumption, corroborating established ontogenetic increases in trophic level documented elsewhere for white sharks. Estimated nutritional intakes and niche breadths did not differ among sexes. Niche breadths were also similar between juvenile white sharks from Australia and South Africa. An increase in nutritional niche breadth with shark size was detected, associated with lipid consumption, which we suggest may relate to shifting nutritional goals linked with expanding migratory ranges.
... This nutritionally explicit framework is particularly relevant to marine apex predators known to forage in complex and fluctuating marine environments (Machovsky-Capuska et al., 2016a;Machovsky-Capuska and Raubenheimer, 2020). While the characterization of nutritional niche breadths of marine predators has shown to be critical to trophic interactions, marine pollution, aquaculture, captivity and rehabilitation, climate change, and conservation and management of endangered species (Machovsky-Capuska and , yet the field remains poorly characterized to few species of seabirds (Machovsky-Capuska et al., 2016c, 2016dMiller et al., 2018;Tait et al., 2014), sharks (Grainger et al., 2020;Machovsky-Capuska and Raubenheimer, 2020), turtles , cetaceans (Denuncio et al., 2017;Machovsky-Capuska et al., 2019) and pinnipeds . ...
... The realized nutritional niches (the range of diets composed by feeding on different prey, sensuMachovsky-Capuska et al., 2016a, 2016b, 2016c, 2016d of the South American sea lions (SASL) and South American fur seal (SAFS) from the Warm Temperate Southwestern Atlantic biogeographic province (WTSA). A) PNG ...
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Niche segregation has been recognized as a valuable mechanism for sympatric species to reduce interspecific competition and facilitate coexistence. The differential use of habitats is one of the behavioural mechanisms that may shape coexistence among marine predators. In this study, we provide a dietary and nutritional assessment of two pinnipeds, the South American sea lion (SASL) and the South American fur seal (SAFS) and explore their sympatric coexistence within the Warm Temperate Southwestern Atlantic biogeographic province (WTSA province). Pelagic prey species within the WTSA province showed significantly higher proportional composition of lipids than demersal counterparts, evidencing a nutritional variability in a vertical dimension accessible to marine predators. By modelling the dietary niches of these pinnipeds through a nutritional lens, we showed high overlapping prey composition niche breadths suggesting that both species consumed prey with similar nutritional composition; however, distinct realized nutritional niches showed that diets are likely shaped by differences in foraging behaviours. The SAFS combined pelagic and demersal prey, whereas SASL mostly preyed upon demersal species. This paper provides crucial information on how nutritional variability in the water column likely drives the feeding strategies of both pinnipeds in the WTSA province. Given that this variation can influence the stability of the contrasting population trends shown by these two pinnipeds, nutritional dynamics must be taken into consideration when defining conservation strategies.
... Heavier gannets within each sex made shorter trips in distance and duration, showing that the differences related to sex are not due to size dimorphism (Table 1). Instead, sex differences may relate to competitive exclusion of females , sex-specific dietary requirements (Machovsky-Capuska et al. 2016) leading to habitat selection , or males investing more time in nest defence (Burger 1981). A key finding was that sex differences varied among years (Fig. 1) as observed in other seabird species (Ishikawa & Watanuki 2002, Gladbach et al. 2009, Castillo-Guerrero & Mellink 2011, Paiva et al. 2017). ...
... Males and females may select different prey due to distinct nutritional requirements (Morehouse et al. 2010), leading to isotopic differences. For instance, male Australasian gannets M. serrator feed on fish with a higher protein-to-lipid and water-to-lipid ratio and a higher trophic level than females (Machovsky-Capuska et al. 2016). Nutritional requirements can be linked to size dimorphism, but our results showed that the trophic niche was not driven by mass (Fig. 6). ...
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Sex-specific niche differentiation is common in marine vertebrates, but how this varies long-term is poorly understood. Here we investigated interannual variation in sexual segregation among breeding northern gannets Morus bassanus, wide-ranging central-place foragers with slight sexual dimorphism. Over 11 breeding seasons, we used GPS tracking and/or stable isotopes to test for sex differences in foraging trip characteristics (range, duration and timing); spatial distribution; habitat selection; and carbon and nitrogen isotopes in blood. When combining data from all years, females foraged further and for longer than males, yet despite this, the foraging areas of the sexes almost completely overlapped. Males and females selected foraging habitats that differed in terms of oceanography but not fishing vessel density. We also detected temporal segregation: females were more likely to be at sea during the day than at night, while males were more likely to be at sea during the night. However, foraging behaviour quantified by all GPS analyses varied interannually, with sex differences detected in some years but not others. Finally, males had consistently higher red blood cell δ13C and δ15N than females across all years, which was not driven by size dimorphism, instead likely by prey choice or very fine-scale habitat selection. We conclude that environmental variation influenced short-term sex differences in movement, but sex differences in stable isotopes that integrate behaviour over longer periods reveal more consistent differences. Our results suggest that inferences drawn from single-year studies may not relate to general patterns, highlighting the importance of long-term studies and combining methods.
... Boobies primarily prey on epipelagic fish (Nelson 1978), and epipelagic fish communities are more diverse and heterogeneously distributed in coastal than in oceanic habitats (Hunt Jr. 1990;Angel 1993;Reese et al. 2011;Lewallen et al. 2017). In addition, prey species vary in their nutritional content (waterlipid-protein ratio) (Machovsky-Capuska et al. 2016;Miller et al. 2018;Machovsky-Capuska and Raubenheimer 2020). Female and male seabirds may react to the nutritional content of the available prey by foraging differently to cover their sexspecific nutritional requirements (Lewis et al. 2002;Machovsky-Capuska et al. 2016). ...
... In addition, prey species vary in their nutritional content (waterlipid-protein ratio) (Machovsky-Capuska et al. 2016;Miller et al. 2018;Machovsky-Capuska and Raubenheimer 2020). Female and male seabirds may react to the nutritional content of the available prey by foraging differently to cover their sexspecific nutritional requirements (Lewis et al. 2002;Machovsky-Capuska et al. 2016). The more complex prey community, heterogeneous distribution, and different nutritional content of prey items in coastal habitats may thus promote foraging segregation, whereas oceanic areas, which have a less diverse and more ephemerally distributed prey community, may prevent this (Ashmole 1971). ...
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Sexual segregation in foraging occurs in some species and populations of boobies (Sulidae), but it is not a general pattern. Sexual segregation in foraging may occur to avoid competition for food, and this competition may intensify during specific stages of breeding. We examined sexual segregation in foraging in relation to breeding stage in masked boobies Sula dactylatra at Rapa Nui by tracking simultaneously incubating and chick-rearing birds using GPS recorders (n = 18) and collected a total of 11 regurgitate samples. Stable isotope analyses (δ¹³C and δ¹⁵N) of whole blood samples were carried out in 20 birds. There were no differences in foraging trip parameters or diet between females and males. Both sexes traveled farther and for longer while incubating than while rearing chicks. Isotopic niches (δ¹³C and δ¹⁵N) overlapped to some degree among all groups at all times, but the lowest overlap between sexes occurred during incubation. While preying on ephemerally distributed flying fish, vertical or horizontal competition avoidance may be almost impossible, and thus females and males share their foraging grounds. Since birds were tracked simultaneously, shorter foraging trips of chick-rearing birds must be an effect of the constraints of provisioning the chick. Differences observed in δ¹⁵N and δ¹³C values between sexes may be caused by subtle differences in their foraging behaviors, or by differences in physiology linked to breeding. Our findings suggest that local oceanography and its inherent food distribution are determinants for sexual segregation in foraging patterns in masked boobies and possibly also other booby species. Significance statement In some animals, females and males forage on different areas or prey on different species to avoid competition for food resources. In boobies (Sula sp.), some studies show evidence of sexual segregation in foraging and others do not. Here, we tested if sexual segregation in foraging occurred in masked boobies on the Pacific island of Rapa Nui by studying simultaneously incubating and chick-rearing birds. We found no evidence of sexual segregation on foraging behavior or diet. We discuss that the difference between this and other studies in boobies may be an effect of the local prey availability. When the prey community is more diverse and heterogeneously distributed, each sex may access different resources and thus sexual foraging segregation will occur. In contrast, in areas like Rapa Nui where prey resources are distributed ephemerally, sexual segregation in foraging will not be useful and is thus less likely to occur.
... The animals tend to adjust the macronutrient intake closer to their natural diet, especially by increasing protein consumption in the high-temperature treatment (Fig. 2.7). Such nutrientspecific diet selection is consistent with the ecology of marine organisms, which forage in nutritionally complex and fluctuating marine environments that vary spatially and temporally (Tait et al. 2014;Machovsky-Capuska et al. 2016a, 2018. ...
Chapter
Proteins represent the dominant biomass of aquatic animals; consequently, proteins are significant nutrients and energy sources with digestive efficiencies between 60 and almost 100%. For most aquatic animals, the quantity of prey available is typically the nutritional bottleneck. A deficiency of dietary protein or amino acids has long been known to impair immune function and increase the susceptibility of animals to infectious disease. In addition to function as energy source, free amino acids can act as osmolytes. The average dietary protein requirement of fishes is 42%; that of invertebrates appears to be below this value. Protein requirement depends on environmental factors, such as salinity and temperature, as well as trophic level and content of the other macronutrients. Interactions with other macronutrients, however, are not yet adequately considered. Adverse effects occur in animals fed deficient or excess proteinaceous diets. Biomolecular modes of action of hyperproteic diets are beginning to be understood; impairment of the immune system is central. Finally, this chapter points out gaps of protein nutrition in aquatic animals.
... Alternatively, overriding sex differences may be associated with reproductive processes such as egg synthesis, should fluctuations in isotopic routing and fractionation span multiple months for RBCs [110]. While there was little evidence for a role of diet in driving foraging differences in the two focal sulids, differing nutritional requirements could still influence use of habitats and foraging strategies, as is now being discussed and tested in seabirds [111,112]. ...
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Background Social interactions, reproductive demands and intrinsic constraints all influence foraging decisions in animals. Understanding the relative importance of these factors in shaping the way that coexisting species within communities use and partition resources is central to knowledge of ecological and evolutionary processes. However, in marine environments, our understanding of the mechanisms that lead to and allow coexistence is limited, particularly in the tropics. Methods Using simultaneous data from a suite of animal-borne data loggers (GPS, depth recorders, immersion and video), dietary samples and stable isotopes, we investigated interspecific and intraspecific differences in foraging of two closely-related seabird species (the red-footed booby and brown booby) from neighbouring colonies on the Cayman Islands in the Caribbean. Results The two species employed notably different foraging strategies, with marked spatial segregation, but limited evidence of interspecific dietary partitioning. The larger-bodied brown booby foraged within neritic waters, with the smaller-bodied red-footed booby travelling further offshore. Almost no sex differences were detected in foraging behaviour of red-footed boobies, while male and female brown boobies differed in their habitat use, foraging characteristics and dietary contributions. We suggest that these behavioural differences may relate to size dimorphism and competition: In the small brown booby population ( n < 200 individuals), larger females showed a higher propensity to remain in coastal waters where they experienced kleptoparasitic attacks from magnificent frigatebirds, while smaller males that were never kleptoparasitised travelled further offshore, presumably into habitats with lower kleptoparasitic pressure. In weakly dimorphic red-footed boobies, these differences are less pronounced. Instead, density-dependent pressures on their large population ( n > 2000 individuals) and avoidance of kleptoparasitism may be more prevalent in driving movements for both sexes. Conclusions Our results reveal how, in an environment where opportunities for prey diversification are limited, neighbouring seabird species segregate at-sea, while exhibiting differing degrees of sexual differentiation. While the mechanisms underlying observed patterns remain unclear, our data are consistent with the idea that multiple factors involving both conspecifics and heterospecifics, as well as reproductive pressures, may combine to influence foraging differences in these neighbouring tropical species.
... Sex-specific macronutrient foraging strategies have been previously observed in free-ranging birds (Machovsky-Capuska et al., 2016b). In our study, females in the MN group consumed more P than males (Fig. S4) in a pattern likely related to differences in post-ingestive nutrient processing and reproductive performance (Maklakov et al., 2008). ...
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Producing colored signals often requires consuming dietary carotenoid pigments. Evidence that food deprivation can reduce coloration, however, raises the question of whether other dietary nutrients contribute to signal coloration, and furthermore, whether individuals can voluntarily select food combinations to achieve optimal coloration. We created a 2-way factorial design to manipulate macronutrient and carotenoid access in common mynas ( Acridotheres tristis ) and measured eye patch coloration as a function of the food combinations individuals selected. Mynas had access to either water or carotenoid-supplemented water and could eat either a standard captive diet or choose freely between three nutritionally defined pellets (protein, lipid, carbohydrate). Mynas supplemented with both carotenoids and macronutrient pellets had higher color scores than control birds. Male coloration tended to respond more to nutritional manipulation than females, with color scores improving in macronutrient- and carotenoid-supplemented individuals compared to controls. All mynas consuming carotenoids had higher levels of plasma carotenoids, but only males showed a significant increase by the end of the experiment. Dietary carotenoids and macronutrient intake consumed in combination tended to increase plasma carotenoid concentrations the most. These results demonstrate for the first time that consuming specific combinations of macronutrients along with carotenoids contribute to optimizing a colorful signal and point to sex-specific nutritional strategies. Our findings improve our knowledge of how diet choices affect signal expression and, by extension, how nutritionally impoverished diets, such as those consumed by birds in cities, might affect sexual selection processes and ultimately population dynamics.
... In winter, for example, studies elsewhere show that both sexes forage at sea, when carrion availability on land is low [38,41,83]. Additionally, females may have higher energy requirements following egg-laying, or require specific nutrients, which would influence their foraging behaviour [84,85]. ...
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... Also, the dance ceremony could provide feedback on the nutritional state (e.g. body condition, coloration) of the foraging partner (Machovsky-Capuska et al., 2016) or be tightly linked to the sex-specific foraging behaviour of gannets (not in trip duration but possibly in feeding areas; Lewis et al., 2002). ...
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Social information percolates through a variety of channels to influence animal decision making, with a notable effect on reproductive and feeding success. Colonial central place foragers can reduce time to locate ephemeral food patches and/or increase foraging rate by following their informed peers, parasitizing direction of returning successful foragers, or being intentionally informed on distant food locations at the colony (e.g. the waggle dance of the honey bee). Ceremonial behaviours may also deliver social foraging information between mates, which can spread inadvertently to neighbours. Here we tested for information display in Cape gannets, Morus capensis, a socially monogamous species, during the elaborate dance ceremony performed each time a partner returns to the nest during the breeding season. We tracked fine-scale foraging behaviour of gannets using bird-borne GPS recorders, and video-recorded their subsequent dance ceremony, which involved up to 14 different displays. As we hypothesized, dance characteristics were associated with foraging trip features. Notably, overall dance duration was negatively linked to foraging trip duration, which was highly positively correlated with foraging range, foraging path length and time spent foraging during the trip. Overall dance duration was also negatively linked with distance to the main foraging grounds. Additionally, the duration of preening behaviour was related to the bearing of the main feeding spot. The latter relationship was supported by a Bayesian model averaging analysis, allowing inferences robust to multiple comparisons. Overall, ceremonial behaviour may provide social foraging information on feeding locations, while evidence for further information transfer to the mate or neighbours was not tested here. Frequent updating on prey spatial distribution, inadvertently communicated or not, should be particularly valuable for predators tracking ephemeral prey patches, providing an additional advantage to colonial living. Our results may have strong implications for cultural evolution in animal societies.
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