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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
... Interactions between marine apex predators may have a significant role on the structuring and functioning of their communities (Ritchie and Johnson, 2009;Baum and Worm, 2009). Given that both dolphins and gannets play a key role in driving ecological interactions Machovsky-Capuska et al., 2016b) and serve as bio-monitor species (Srinivasan et al., 2015;Stockin et al., 2021a, b), an understanding of the extent of these relations and their ecological role, is important to preserve healthy marine ecosystems. Our study provides nutritional and ethological perspectives, that reveal how foraging strategies of dolphins shape these multispecies interactions while feeding on patchily distributed marine prey. ...
... Thus, a lack of current information on stocks of jack mackerel, grey mullet, and pilchard prevents a comprehensive understanding of the sustainability of these marine predator populations within the region (Hauraki Gulf Forum, 2020). Understanding the foraging strategies and nutritional requirements of marine predators is critical to predict how these species adjust to changes in prey composition and availability in heterogenous environments (Österblom et al., 2008;Machovsky-Capuska et al., 2016b). While our results showed no differences in the nutritional composition of diets, both predators relied on the consumption of species with high en-ergy content, high % L and low P:L. ...
... For instance, dolphins relied on grey mullet ( 5.3 kJ g -1 , 6.5% L, and P:L = 2.6) and gannets on yellow eye mullet (5.1 kJ g -1 , 6.1% L, and P:L = 2.8), that were also mixed with low energy content, low %L, high P:L prey to achieve their respective intakes. The ability to combine nutritionally complementary prey (species with different P:L) to achieve similar diet intakes has previously been reported in gannets (Machovsky-Capuska et al., 2016b), mink (Mustela vision, Mayntz et al., 2009), and juvenile white sharks (Carcharodon carcharias, Grainger et al., 2020). Such findings are furthermore, consistent with prior studies that suggest the likelihood that prey selection in aquatic predators is likely to be driven by macronutrient balance instead of energy acquisition Machovsky-Capuska et al., 2016b, c;Machovsky-Capuska and Raubenheimer, 2020). ...
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Prey detection and subsequent capture is considered a major hypothesis to explain feeding associations between common dolphins and Australasian gannets. However, a current lack of insight on nutritional strategies with respect to foraging behaviours of both species has until now, prevented any detailed understanding of this conspecific relationship. Here we combine stomach content analysis (SCA), nutritional composition of prey, a multidimensional nutritional niche framework (MNNF) and videography to provide a holistic dietary, nutritional, and behavioural assessment of the feeding association between dolphins and gannets in the Hauraki Gulf, New Zealand. Dolphins consumed ten prey species, including grey mullet (Mugil cephalus) as the most representative by wet mass (33.4%). Gannets preyed upon six species, with pilchards (Sardinops pilchardus) contributing most of the diet by wet mass (32.4%) to their diet. Both predators jointly preyed upon pilchard, jack mackerel (Trachurus spp.), arrow squid (genus Nototodarus), and anchovy (Engraulis australis). Accordingly, the MNNF revealed a moderate overlap in the prey composition niche (0.42) and realized nutritional niche (0.52) between dolphins and gannets. This suggests that both predators coexist in a similar nutritional space, while simultaneously reducing interspecific competition and maximizing the success of both encountering and exploiting patchily distributed prey. Behavioural analysis further indicated that dolphin and gannets feeding associations are likely to be mutually beneficial, with a carouselling foraging strategy and larger pod sizes of dolphins, influencing the diving altitude of gannets. Our approach provides a new, more holistic understanding of this iconic foraging relationship, which until now has been poorly understood.
... some web-building spiders) 1,15,[18][19][20][21][22] . In addition, carnivores in the wild have been observed to select prey non-randomly from the environment [23][24][25] , selectively consume specific tissues/organs of prey 10 , and achieve consistent pattens in macronutrient intake [26][27][28] . The latter has been seen in Australasian gannets (Morus serrator) for example, where males consistently consumed a diet that had higher protein-to-lipid ratios compared to their female counterparts, possibly in response to sex-specific nutrient requirements 26 . ...
... In addition, carnivores in the wild have been observed to select prey non-randomly from the environment [23][24][25] , selectively consume specific tissues/organs of prey 10 , and achieve consistent pattens in macronutrient intake [26][27][28] . The latter has been seen in Australasian gannets (Morus serrator) for example, where males consistently consumed a diet that had higher protein-to-lipid ratios compared to their female counterparts, possibly in response to sex-specific nutrient requirements 26 . Although these studies have documented selection of nutrients from the environment, they have not demonstrated selection towards a nutrient intake target, and so it is unknown whether these cases of selective foraging represent selective foraging for a fitness advantage. ...
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In nutritional ecology the intake target is the diet that maximises consumer fitness. A key hypothesis of nutritional ecology is that natural selection has acted upon the behavioural and physiological traits of consumers to result in them Selectively Consuming prey to match the Intake Target (SCIT). SCIT has been documented in some herbivores and omnivores, which experience strong heterogeneity in the nutritional quality of available foods. Although carnivores experience a prey community with a much more homogeneous nutrient composition, SCIT by carnivores has nevertheless been deemed highly likely by some researchers. Here we test for SCIT for micronutrients (amino acids) in two freshwater carnivores: the river blackfish and the two-spined blackfish. Although both blackfishes exhibited non-random consumption of prey from the environment, this resulted in non-random consumption of amino acids in only one species, the river blackfish. Non-random consumption of amino acids by river blackfish was not SCIT, but instead an artefact of habitat-specific foraging. We present hypotheses to explain why wild populations of freshwater carnivores may not exhibit SCIT for amino acids. Our work highlights the need for careful, critical tests of the hypotheses and assumptions of nutritional ecology and its application to wild populations.
... 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.
... Female masked boobies lay two eggs (Lerma, Serratosa, et al., 2020), whereas red-footed boobies only lay one (Lormee et al., 2005). Female masked boobies might thus have higher nutritional demands (Lerma et al., 2022;Machovsky-Capuska et al., 2016) and adapt their foraging to compensate for their initial investment in reproduction. Fourth, we studied incubating individuals, but most studies found differences during the chick-rearing period, particularly for red-footed boobies. ...
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Animals that co‐occur in a region (sympatry) may share the same environment (syntopy), and niche differentiation is expected among closely related species competing for resources. The masked booby ( Sula dactylatra ) and smaller congeneric red‐footed booby ( Sula sula ) share breeding grounds. In addition to the inter‐specific size difference, females of both species are also larger than the respective males (reversed sexual size dimorphism). Although both boobies consume similar prey, sometimes in mixed‐species flocks, each species and sex may specialize in terms of their diet or foraging habitats. We examined inter‐ and intra‐specific differences in isotopic values (δ ¹³ C and δ ¹⁵ N) in these pelagically feeding booby species during the incubation period at Clarion Island, Mexico, to quantify the degrees of inter‐ and intra‐specific niche partitioning throughout the annual cycle. During incubation, both species preyed mainly on flyingfish and squid, but masked boobies had heavier food loads than red‐footed boobies. There was no overlap in isotopic niches between masked and red‐footed boobies during breeding (determined from whole blood), but there was slight overlap during the non‐breeding period (determined from body feathers). Female masked boobies had a higher trophic position than conspecific males during breeding; however, no such pattern was detected in red‐footed boobies. These results provide evidence of inter‐ and intra‐specific niche partitioning in these tropical seabird species, particularly during the breeding period and in the more‐dimorphic species. Our results suggest that these closely related species use different strategies to cope with the same tropical marine environment.
... 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]. ...
Article
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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.
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