Abstract
Studies on sex-specific segregation in foraging behaviour and trophic niche have been focussed on large and dimorphic seabirds, with less information on small monomorphic species. Here, we used mini-GPS loggers, habitat suitability models, and stable isotopes to assess sex differences in the foraging movements, spatial distribution, and trophic ecology of Boyd’s shearwaters Puffinus lherminieri boydi in Raso Islet (16°36’ N, 24°35’ W), Cabo Verde, during the chick-rearing periods of 2018–2019. The existence of sexual foraging segregation was tested in short (< 1 day) and in long trips (≥ 1 day). Females engaged in slightly longer and more distant foraging trips, reaching northerly regions when compared to males, although sex differences were more pronounced during short trips. Spatial overlap within and between sexes was low, indicating a sex-specific pattern, albeit slight, in the foraging behaviour and spatial distribution of adult breeders. Habitat suitability models revealed a higher contribution of sea surface temperature and height for short and long trips, respectively, and regardless of sex. Stable isotope analysis revealed that both sexes occupied similar isotopic niches and the mixing model revealed no diet differences. In the absence of sexual size dimorphism, these findings may indicate that differential energetic demands may not manifest in strong differences in foraging behaviour or prey preferences, however, may be perceptible in differences in provisioning behaviour. Thus, it is possible that other factors involving distinct parental investment in chick-provisioning, such as the sensitivity to chick begging, could help explain the occurrence of sexual segregation in Boyd’s shearwater.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data will be available upon reasonable request to the authors.
References
Almeida N, Ramos JA, Rodrigues I, dos Santos I, Pereira JM, Matos DM, Araújo PM, Geraldes P, Melo T, Paiva VH (2021) Year-round at-sea distribution and trophic resources partitioning between two sympatric Sulids in the tropical Atlantic. PLoS ONE 16:1–27. https://doi.org/10.1371/journal.pone.0253095
Araujo M, Pearson R, Thuiller W, Erhard M (2005) Validation of species-climate impact models under climate change. Glob Chang Biol 11:1504–1513. https://doi.org/10.1111/j.1365-2486.2005.001000.x
Austin RE, De Pascalis F, Arnould JP, Haakonsson J, Votier SC, Ebanks-Petrie G, Austin T, Morgan G, Bennett G, Green J (2019) A sex-influenced flexible foraging strategy in the magnificent frigatebird Fregata magnificens. Mar Ecol Prog Ser 611:203–214
Barbet-Massin M, Jiguet F, Albert CH, Thuiller W (2012) Selecting pseudo-absences for species distribution models: How, where and how many? Methods Ecol Evol 3:327–338. https://doi.org/10.1111/j.2041-210X.2011.00172.x
Barrett RT, Camphuysen KCJ, Anker-Nilssen T, Chardine JW, Furness RW, Garthe S, Hüppop O, Leopold MF, Montevecchi WA, Veit RR (2007) Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64:1675–1691. https://doi.org/10.1093/icesjms/fsm152
Barron DG, Brawn JD, Weatherhead PJ (2010) Meta-analysis of transmitter effects on avian behaviour and ecology. Methods Ecol Evol 1:180–187. https://doi.org/10.1111/j.2041-210x.2010.00013.x
Bates D, Martin Maechler, Bolker B, Walker S, Christensen RHB, Singmann H, Dai B, Grothendieck G (2015) lme4: linear mixed-effects models using “Eigen” and S4. R package version 1.1-10, pp 1–98
Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458. https://doi.org/10.1086/342800
Becker BH, Peery MZ, Beissinger SR (2007) Ocean climate and prey availability affect the trophic level and reproductive success of the marbled murrelet, an endangered seabird. Mar Ecol Prog Ser 329:267–279. https://doi.org/10.3354/meps329267
Bennison A, Giménez J, Quinn JL, Green JA, Jessopp M (2022) A bioenergetics approach to understanding sex differences in the foraging behaviour of a sexually monomorphic species. R Soc Open Sci 9:15. https://doi.org/10.1098/rsos.210520
BirdLife International (2020) Species factsheet: Puffinus lherminieri. http//www.birdlife.org. Accessed 20 Aug 2020
Bodey TW, Cleasby IR, Bell F, Parr N, Schultz A, Votier SC, Bearhop S (2018) A phylogenetically controlled meta-analysis of biologging device effects on birds: deleterious effects and a call for more standardized reporting of study data. Methods Ecol Evol 9:946–955. https://doi.org/10.1111/2041-210X.12934
Bolton M (2021) GPS tracking reveals highly consistent use of restricted foraging areas by European Storm-petrels Hydrobates pelagicus breeding at the largest UK colony: implications for conservation management. Bird Conserv Int 31:1–18. https://doi.org/10.1017/s0959270920000374
Bond AL, Jones Ian L (2009) A practical introduction to stable-isotope analysis for seabird biologists: approaches, cautions and caveats. Mar Ornithol 37:183–188
Braun CD, Gaube P, Sinclair-Taylor TH, Skomal GB, Thorrold SR (2019) Mesoscale eddies release pelagic sharks from thermal constraints to foraging in the ocean twilight zone. Proc Natl Acad Sci U S A 116:17187–17192. https://doi.org/10.1073/pnas.1903067116
Burke CM, Montevecchi WA, Regular PM (2015) Seasonal variation in parental care drives sex-specific foraging by a monomorphic seabird. PLoS ONE 10:1–22. https://doi.org/10.1371/journal.pone.0141190
Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecol Modell 197:516–519. https://doi.org/10.1016/j.ecolmodel.2006.03.017
Cardoso C (2017) Eddies of the Cape Verde Archipelago. Dissertation, Universidade do Algarve
Carreiro AR, Paiva VH, Medeiros R, Franklin KA, Oliveira N, Fagundes AI, Ramos JA (2020) Metabarcoding, stables isotopes, and tracking: unraveling the trophic ecology of a winter-breeding storm petrel (Hydrobates castro) with a multimethod approach. Mar Biol 167:1–13. https://doi.org/10.1007/s00227-019-3626-x
Catry T, Ramos JA, Jaquemet S, Faulquier L, Berlincourt M, Hauselmann A, Pinet P, Le CM (2009) Comparative foraging ecology of a tropical seabird community of the Seychelles, western Indian Ocean. Mar Ecol Prog Ser 374:259–272. https://doi.org/10.3354/meps07713
Catry T, Ramos JA, Catry I, Monticelli D, Granadeiro JP (2013) Inter-annual variability in the breeding performance of six tropical seabird species: influence of life-history traits and relationship with oceanographic parameters. Mar Biol 160:1189–1201. https://doi.org/10.1007/s00227-013-2171-2
Cecere JG, De Pascalis F, Imperio S, Ménard D, Catoni C, Griggio M, Rubolini D (2020) Inter-individual differences in foraging tactics of a colonial raptor: consistency, weather effects, and fitness correlates. Mov Ecol 8:1–13. https://doi.org/10.1186/s40462-020-00206-w
Cerveira LR, Ramos JA, Rodrigues I, Almeida N, Araújo PM, dos Santos I, Vieira C, Pereira JM, Ceia FR, Geraldes P, Melo T, Paiva VH (2020) Inter-annual changes in oceanic conditions drives spatial and trophic consistency of a tropical marine predator. Mar Environ Res 162:105165. https://doi.org/10.1016/j.marenvres.2020.105165
Cherel Y, Hobson KA, Bailleul F, Groscolas R (2005a) Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881–2888
Cherel Y, Hobson KA, Weimerskirch H (2005b) Using stable isotopes to study resource acquisition and allocation in procellariiform seabirds. Oecologia 145:533–540. https://doi.org/10.1007/s00442-005-0156-7
Chimienti M, Cornulier T, Owen E, Bolton M, Davies IM, Travis JMJ, Scott BE (2017) Taking movement data to new depths: Inferring prey availability and patch profitability from seabird foraging behavior. Ecol Evol 7:10252–10265. https://doi.org/10.1002/ece3.3551
Clark B, Cox S, Atkins K, Bearhop S, Bicknell A, Bodey T, Cleasby I, Grecian W, Hamer K, Loveday B, Miller P, Morgan G, Morgan L, Newton J, Patrick S, Scales K, Sherley R, Vigfúsdóttir F, Wakefield E, Votier S (2021) Sexual segregation of gannet foraging over 11 years: movements vary but isotopic differences remain stable. Mar Ecol Prog Ser 661:1–16. https://doi.org/10.3354/meps13636
Clay TA, Joo R, Weimerskirch H, Phillips RA, den Ouden O, Basille M, Clusella-Trullas S, Assink JD, Patrick SC (2020) Sex-specific effects of wind on the flight decisions of a sexually dimorphic soaring bird. J Anim Ecol 89:1811–1823. https://doi.org/10.1111/1365-2656.13267
Cleasby IR, Wakefield ED, Bodey TW, Davies RD, Patrick SC, Newton J, Votier SC, Bearhop S, Hamer KC (2015) Sexual segregation in a wide-ranging marine predator is a consequence of habitat selection. Mar Ecol Prog Ser 518:1–12. https://doi.org/10.3354/meps11112
Congdon BC, Krockenberger AK, Smithers BV (2005) Dual-foraging and co-ordinated provisioning in a tropical Procellariiform, the wedge-tailed shearwater. Mar Ecol Prog Ser 301:293–301. https://doi.org/10.3354/meps301293
Davoren GK, Garthe S, Montevecchi WA, Benvenuti S (2010) Influence of prey behaviour and other predators on the foraging activities of a marine avian predator in a low arctic ecosystem. Mar Ecol Prog Ser 404:275–287. https://doi.org/10.3354/meps08370
Elliott KH, Gaston AJ, Crump D (2010) Sex-specific behavior by a monomorphic seabird represents risk partitioning. Behav Ecol 21:1024–1032. https://doi.org/10.1093/beheco/arq076
Falkowski PG, Ziemann D, Kolber Z, Bienfang PK (1991) Role of eddy pum** in enhancing primary production in the ocean. Nature 352:55–58
Flood R, van der Vliet R (2019) Variation and identification of Barolo Shearwater and Boyd’s Shearwater. Dutch Bird 41:215–237
Furness RW, Camphuysen CJ (1997) Seabirds as monitors of the marine environment. ICES J Mar Sci 54:726–737. https://doi.org/10.1006/jmsc.1997.0243
Garriga J, Palmer JRB, Oltra A, Bartumeus F (2016) Expectation-maximization binary clustering for behavioural annotation. PLoS ONE 11:1–26. https://doi.org/10.1371/journal.pone.0151984
Garthe S, Montevecchi WA, Davoren GK (2007) Flight destinations and foraging behaviour of northern gannets (Sula bassana) preying on a small forage fish in a low-Arctic ecosystem. Deep Res Part II Top Stud Oceanogr 54:311–320. https://doi.org/10.1016/j.dsr2.2006.11.008
Gillies N, Fayet AL, Padget O, Syposz M, Wynn J, Bond S, Evry J, Kirk H, Shoji A, Dean B, Freeman R, Guilford T (2020) Short-term behavioural impact contrasts with long-term fitness consequences of biologging in a long-lived seabird. Sci Rep 10:1–10. https://doi.org/10.1038/s41598-020-72199-w
Giménez J, Arneill GE, Bennison A, Pirotta E, Gerritsen HD, Bodey TW, Bearhop S, Hamer KC, Votier S, Jessopp M (2021) Sexual mismatch between vessel-associated foraging and discard consumption in a marine top predator. Front Mar Sci 8:1–13. https://doi.org/10.3389/fmars.2021.636468
Gladbach A, Braun C, Nordt A, Peter HU, Quillfeldt P (2009) Chick provisioning and nest attendance of male and female Wilson’s storm petrels Oceanites oceanicus. Polar Biol 32:1315–1321. https://doi.org/10.1007/s00300-009-0628-z
González-Solís J, Croxall JP, Wood AG (2000) Sexual dimorphism and sexual segregation in foraging strategies of northern giant petrels, Macronectes halli, during incubation. Oikos 90:390–398. https://doi.org/10.1034/j.1600-0706.2000.900220.x
Granadeiro JP, Bolton M, Silva MC, Nunes M, Furness RW (2000) Responses of breeding Cory’s shearwater Calonectris diomedea to experimental manipulation of chick condition. Behav Ecol 11:274–281. https://doi.org/10.1093/beheco/11.3.274
Gray CM, Hamer KC (2001) Food-provisioning behaviour of male and female Manx shearwaters, Puffinus puffinus. Anim Behav 62:117–121. https://doi.org/10.1006/anbe.2001.1717
Hamer KC, Quillfeldt P, Masello JF, Fletcher KL (2006) Sex differences in provisioning rules: responses of Manx shearwaters to supplementary chick feeding. Behav Ecol 17:132–137. https://doi.org/10.1093/beheco/arj008
Healy K, Guillerme T, Kelly SBA, Inger R, Bearhop S, Jackson AL (2018) SIDER: an R package for predicting trophic discrimination factors of consumers based on their ecology and phylogenetic relatedness. Ecography 41:1393–1400. https://doi.org/10.1111/ecog.03371
Hijmans RJ, Etten J van, Sumner M, Cheng J, Bevan A, Bevan R, Busetto L, Canty M, Forrest D, Ghosh A, Golicher D, Gray J, Greenberg JA (2020) “raster” R package version 3.3-13, pp 1–249
Hsieh CH, Kim HJ, Watson W, Di Lorenzo E, Sugihara G (2009) Climate-driven changes in abundance and distribution of larvae of oceanic fishes in the southern California region. Glob Chang Biol 15:2137–2152. https://doi.org/10.1111/j.1365-2486.2009.01875.x
Ichii T, Mahapatra K, Sakai M, Inagake D, Okada Y (2004) Differing body size between the autumn and the winter-spring cohorts of neon flying squid (Ommastrephes bartramii) related to the oceanographic regime in the North Pacific: a hypothesis. Fish Oceanogr 13:295–309. https://doi.org/10.1111/j.1365-2419.2004.00293.x
Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150:447–461. https://doi.org/10.1111/j.1474-919X.2008.00839.x
Ismar SMH, Raubenheimer D, Bury SJ, Millar CD, Hauber ME (2017) Sex-specific foraging during parental care in a size-monomorphic seabird, the Australasian Gannet (Morus serrator). Wilson J Ornithol 129:139–147. https://doi.org/10.1676/1559-4491-129.1.139
Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
Jaquemet S, Le Corre M, Marsac F, Potier M, Weimerskirch H (2005) Foraging habitats of the seabird community of Europa Island (Mozambique Channel). Mar Biol 147:573–582. https://doi.org/10.1007/s00227-005-1610-0
Johnson DL, Henderson MT, Anderson DL, Booms TL, Williams CT (2020) Bayesian stable isotope mixing models effectively characterize the diet of an Arctic raptor. J Anim Ecol 89:2972–2985. https://doi.org/10.1111/1365-2656.13361
Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27. https://doi.org/10.1139/z99-165
Klein P, Lapeyre G (2009) The oceanic vertical pump induced by mesoscale and submesoscale turbulence. Ann Rev Mar Sci 1:351–375. https://doi.org/10.1146/annurev.marine.010908.163704
Lascelles BG, Taylor PR, Miller MGR, Dias MP, Oppel S, Torres L, Hedd A, Le Corre M, Phillips RA, Shaffer SA, Weimerskirch H, Small C (2016) Applying global criteria to tracking data to define important areas for marine conservation. Divers Distrib 22:422–431. https://doi.org/10.1111/ddi.12411
Lewis S, Benvenuti S, DallAntonia L, Griffiths R, Money L, Sherratt TN, Wanless S, Hamer KC (2002) Sex-specific foraging behaviour in a monomorphic seabird. Proc R Soc B Biol Sci 269:1687–1693. https://doi.org/10.1098/rspb.2002.2083
López-Pérez C, Olivar MP, Hulley PA, Tuset VM (2020) Length–weight relationships of mesopelagic fishes from the equatorial and tropical Atlantic waters: influence of environment and body shape. J Fish Biol 96:1388–1398. https://doi.org/10.1111/jfb.14307
Louzao M, Bécares J, Rodríguez B, Hyrenbach KD, Ruiz A, Arcos JM (2009) Combining vessel-based surveys and tracking data to identify key marine areas for seabirds. Mar Ecol Prog Ser 391:183–197. https://doi.org/10.3354/meps08124
Louzao M, Wiegand T, Bartumeus F, Weimerskirch H (2014) Coupling instantaneous energy-budget models and behavioural mode analysis to estimate optimal foraging strategy: an example with wandering albatrosses. Mov Ecol. https://doi.org/10.1186/2051-3933-2-8
Magalhães MC, Santos RS, Hamer KC (2008) Dual-foraging of Cory’s shearwaters in the Azores: feeding locations, behaviour at sea and implications for food provisioning of chicks. Mar Ecol Prog Ser 359:283–293. https://doi.org/10.3354/meps07340
Mann KH, Lazier JR (2013) Dynamics of marine ecosystems: biological-physical interactions in the oceans. Blackwell Publishing, Oxford
Marmion M, Parviainen M, Luoto M, Heikkinen RK, Thuiller W (2009) Evaluation of consensus methods in predictive species distribution modelling. Divers Distrib 15:59–69. https://doi.org/10.1111/j.1472-4642.2008.00491.x
McDuie F, Weeks SJ, Congdon BC (2018) Oceanographic drivers of near-colony seabird foraging site use in tropical marine systems. Mar Ecol Prog Ser 589:209–225. https://doi.org/10.3354/meps12475
Meunier T, Barton ED, Barreiro B, Torres R (2012) Upwelling filaments off cap blanc: Interaction of the NW african upwelling current and the cape verde frontal zone eddy field? J Geophys Res Ocean 117:1–18. https://doi.org/10.1029/2012JC007905
Minagawa M, Wada E (1986) Nitrogen isotope ratios of red tide organisms in the East China Sea: a characterization of biological nitrogen fixation. Mar Chem 19:245–259. https://doi.org/10.1016/0304-4203(86)90026-5
Monaghan P, Nager RG, Houston DC (1998) The price of eggs: Increased investment in egg production reduces the offspring rearing capacity of parents. Proc R Soc B Biol Sci 265:1731–1735. https://doi.org/10.1098/rspb.1998.0495
Monteiro C (2019) Ecología trófica de la comunidad de aves marinas de Cabo Verde. Dissertation, University of Barcelona
Morato T, Varkey DA, Damaso C, Machete M, Santos M, Prieto R, Santos RS, Pitcher TJ (2008) Evidence of a seamount effect on aggregating visitors. Mar Ecol Prog Ser 357:23–32. https://doi.org/10.3354/meps07269
Morgenthaler A, Millones A, Gandini P, Frere E (2021) Which trophic discrimination factors fit the best? A combined dietary study of a coastal seabird. J Ornithol 162:179–190. https://doi.org/10.1007/s10336-020-01813-5
Naimi B (2017) usdm: uncertainty analysis for species distribution models. R package version 1.1-18
Navarro AB, Magioli M, Bogoni JA, Silveira LF, Moreira MZ, Alexandrino ER, da Luz DTA, Silva WR, Pizo MA, de Oliveira VC, de Ferraz KMPMB (2021) Isotopic niches of tropical birds reduced by anthropogenic impacts: a 100-year perspective. Oikos 130:1892–1904. https://doi.org/10.1111/oik.08386
Nelson JB (1965) The behaviour of the gannet. Br Birds 58:231–336
Neves VC, Bried J, González-Solís J, Roscales JL, Clarke MR (2012) Feeding ecology and movements of the Barolo shearwater Puffinus baroli baroli in the Azores, NE Atlantic. Mar Ecol Prog Ser 452:269–285. https://doi.org/10.3354/meps09670
Newsome SD, Martinez del Rio C, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436
Nisbet ICT, Montoya JP, Burger J, Hatch JJ (2002) Use of stable isotopes to investigate individual differences in diets and mercury exposures among common terns Sterna hirundo in breeding and wintering grounds. Mar Ecol Prog Ser 242:267–274. https://doi.org/10.3354/meps242267
Paiva VH, Geraldes P, Rodrigues I, Melo T, Melo J, Ramos JA (2015) The foraging ecology of the endangered cape verde shearwater, a sentinel species for marine conservation off West Africa. PLoS ONE 10:e0139390. https://doi.org/10.1371/journal.pone.0139390
Paiva VH, Pereira J, Ceia FR, Ramos JA (2017) Environmentally driven sexual segregation in a marine top predator. Sci Rep 7:1–11. https://doi.org/10.1038/s41598-017-02854-2
Paiva VH, Ramos JA, Nava C, Neves V, Bried J, Magalhães M (2018) Inter-sexual habitat and isotopic niche segregation of the endangered Monteiro’s storm-petrel during breeding. Zoology 126:29–35. https://doi.org/10.1016/j.zool.2017.12.006
Paredes R, Jones IL, Boness DJ (2006) Parental roles of male and female thick-billed murres and razorbills at the Gannet Islands, Labrador. Behaviour 143:451–481. https://doi.org/10.1163/156853906776240641
Parnell A, Inger R (2016) simmr: a stable isotope mixing model. R Package version 0.3
Peck DR, Congdon BC (2006) Sex-specific chick provisioning and diving behaviour in the wedge-tailed shearwater Puffinus pacificus. J Avian Biol 37:245–251. https://doi.org/10.1111/j.2006.0908-8857.03558.x
Peña-Izquierdo J, Pelegrí JL, Pastor MV, Castellanos P, Emelianov M, Gasser M, Salvador J, Vázquez-Domínguez E (2012) The continental slope current system between Cape Verde and the Canary Islands. Sci Mar 76S1:65–78. https://doi.org/10.3989/scimar.03607.18C
Pereira JM, Paiva VH, Phillips RA, Xavier JC (2018) The devil is in the detail : small—scale sexual segregation despite large—scale spatial overlap in the wandering albatross. Mar Biol 165:1–16. https://doi.org/10.1007/s00227-018-3316-0
Pereira JM, Paiva VH, Ceia FR, Ramos JA (2020) Facing extremes: Cory’s shearwaters adjust their foraging behaviour differently in response to contrasting phases of North Atlantic Oscillation. Reg Environ Chang 20:1–13. https://doi.org/10.1007/s10113-020-01662-1
Pereira JM, Ramos JA, Marques AM, Ceia FR, Krüger L, Votier SC, Paiva VH (2021) Low spatial overlap between foraging shearwaters during the breeding season and industrial fisheries off the west coast of Portugal. Mar Ecol Prog Ser 657:209–221. https://doi.org/10.3354/meps13549
Pereira JM, Ramos JA, Almeida N, Araújo PM, Ceia FR, Geraldes P, Marques AM, Matos DM, Rodrigues I, dos Santos I, Paiva VH (2022) Foraging costs drive within-colony spatial segregation in shearwaters from two contrasting environments in the North Atlantic. Oecologia. https://doi.org/10.1007/s00442-022-05109-8
Phillips RA, Silk JRD, Phalan B, Catry P, Croxall JP (2004) Seasonal sexual segregation in two Thalassarche albatross species: competitive exclusion, reproductive role specializaion or foraging niche divergence? Proc R Soc B Biol Sci 271:1283–1291. https://doi.org/10.1098/rspb.2004.2718
Phillips RA, McGill RAR, Dawson DA, Bearhop S (2011) Sexual segregation in distribution, diet and trophic level of seabirds: Insights from stable isotope analysis. Mar Biol 158:2199–2208. https://doi.org/10.1007/s00227-011-1725-4
Phillips DL, Inger R, Bearhop S, Jackson AL, Moore JW, Parnell AC, Semmens BX, Ward EJ (2014) Best practices for use of stable isotope mixing models in food-web studies. Can J Zool 92:823–835. https://doi.org/10.1139/cjz-2014-0127
Pinet P, Jaquemet S, Phillips RA, Le Corre M (2012) Sex-specific foraging strategies throughout the breeding season in a tropical, sexually monomorphic small petrel. Anim Behav 83:979–989. https://doi.org/10.1016/J.ANBEHAV.2012.01.019
Plummer M, Stukalov A, Denwood M (2019) rjags: Bayesian graphical models using MCMC
Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189. https://doi.org/10.1007/s00442-006-0630-x
Quillfeldt P, Masello JF, Hamer KC (2004) Sex differences in provisioning rules and honest signalling of need in Manx shearwaters, Puffinus puffinus. Anim Behav 68:613–620. https://doi.org/10.1016/j.anbehav.2003.12.002
Quillfeldt P, McGill RAR, Masello JF, Weiss F, Strange IJ, Brickle P, Furness RW (2008) Stable isotope analysis reveals sexual and environmental variability and individual consistency in foraging of thin-billed prions. Mar Ecol Prog Ser 373:137–148. https://doi.org/10.3354/meps07751
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.r-project.org/
Ramos JA, Isabel Fagundes A, Xavier JC, Fidalgo V, Ceia FR, Medeiros R, Paiva VH (2015) A switch in the Atlantic Oscillation correlates with inter-annual changes in foraging location and food habits of Macaronesian shearwaters (Puffinus baroli) nesting on two islands of the sub-tropical Atlantic Ocean. Deep Sea Res Part I Oceanogr Res Pap 104:60–71. https://doi.org/10.1016/j.dsr.2015.07.001
Ramos R, Paiva VH, Zajková Z, Precheur C, Fagundes AI, Jodice PGRR, Mackin W, Zino F, Bretagnolle V, González-Solís J (2020) Spatial ecology of closely related taxa: the case of the little shearwater complex in the North Atlantic Ocean. Zool J Linn Soc 191:1–21. https://doi.org/10.1093/zoolinnean/zlaa045
Ravache A, Bourgeois K, Weimerskirch H, Pagenaud A, de Grissac S, Miller M, Dromzée S, Lorrain A, Allain V, Bustamante P, Bylemans J, Gleeson D, Letourneur Y, Vidal É (2020) Behavioral and trophic segregations help the Tahiti petrel to cope with the abundance of wedge-tailed shearwater when foraging in oligotrophic tropical waters. Sci Rep 10:1–18. https://doi.org/10.1038/s41598-020-72206-0
Reyes-González JM, De Felipe F, Morera-Pujol V, Soriano-Redondo A, Navarro-Herrero L, Zango L, García-Barcelona S, Ramos R, González-Solís J (2021) Sexual segregation in the foraging behaviour of a slightly dimorphic seabird: Influence of the environment and fishery activity. J Anim Ecol 90:1109–1121. https://doi.org/10.1111/1365-2656.13437
Rotger A, Sola A, Tavecchia G, Sanz-Aguilar A (2021) Foraging far from home: gps-tracking of mediterranean Storm-Petrels Hydrobates pelagicus melitensis reveals long-distance foraging movements. Ardeola 68:3–16. https://doi.org/10.13157/arla.68.1.2021.ra1
Schmitt S, Pouteau R, Justeau D, de Boissieu F, Birnbaum P (2017) ssdm: an r package to predict distribution of species richness and composition based on stacked species distribution models. Methods Ecol Evol 8:1795–1803. https://doi.org/10.1111/2041-210X.12841
Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39. https://doi.org/10.1126/science.185.4145.27
Scopel LC, Diamond AW, Kress SW, Hards AR, Shannon P (2017) Seabird diets as bioindicators of Atlantic herring recruitment and stock size: a new tool for ecosystem-based fisheries management. Can J Fish Aquat Sci 15:1–15. https://doi.org/10.1139/cjfas-2017-0140
Semedo G, Paiva VH, Militão T, Rodrigues I, Dinis HA, Pereira J, Matos D, Ceia FR, Almeida NM, Geraldes P, Saldanha S, Barbosa N, Hernández-Montero M, Fernandes C, González-Sólis J, Ramos JA (2021) Distribution, abundance, and on-land threats to Cabo Verde seabirds. Bird Conserv Int 31:53–76. https://doi.org/10.1017/S0959270920000428
Shaffer SA, Weimerskirch H, Costa DP (2001) Functional significance of sexual dimorphism in Wandering Albatrosses, Diomedea exulans. Funct Ecol 15:203–210. https://doi.org/10.1046/j.1365-2435.2001.00514.x
Shoji A, Aris-Brosou S, Fayet A, Padget O, Perrins C, Guilford T (2015) Dual foraging and pair coordination during chick provisioning by Manx shearwaters: empirical evidence supported by a simple model. J Exp Biol 218:2116–2123. https://doi.org/10.1242/jeb.120626
Smith JA, Mazumder D, Suthers IM, Taylor MD (2013) To fit or not to fit: evaluating stable isotope mixing models using simulated mixing polygons. Methods Ecol Evol 4:612–618. https://doi.org/10.1111/2041-210X.12048
Soanes LM, Bright JA, Brodin G, Mukhida F, Green JA (2015) Tracking a small seabird: first records of foragign movements in the sooty tern Onychoprion fuscatus. Mar Ornithol 43:235–239
Stauss C, Bearhop S, Bodey TW, Garthe S, Gunn C, Grecian WJ, Inger R, Knight ME, Newton J, Patrick SC, Phillips RA, Waggitt JJ, Votier SC (2012) Sex-specific foraging behaviour in northern gannets Morus bassanus: Incidence and implications. Mar Ecol Prog Ser 457:151–162. https://doi.org/10.3354/meps09734
Stramma L, Bange HW, Czeschel R, Lorenzo A, Frank M (2013) On the role of mesoscale eddies for the biological productivity and biogeochemistry in the eastern tropical Pacific Ocean off Peru. Biogeosciences 10:7293–7306. https://doi.org/10.5194/bg-10-7293-2013
Sumner MD, Luque S, Fischbach A, Hengl T (2020) trip: tools for the analysis of animal track data. R package version 1.8.0. pp 1–37
Sun A, Whelan S, Hatch SA, Elliott KH (2020) Tags below three percent of body mass increase nest abandonment by rhinoceros auklets, but handling impacts decline as breeding progresses. Mar Ecol Prog Ser 643:173–181. https://doi.org/10.3354/meps13341
Surman CA, Nicholson LW, Ayling S (2017) Foraging behavior of the Lesser Noddy Anous tenuirostris from the eastern Indian Ocean: insights from micro-geologging. Mar Ornithol 45:123–128
Swan GJF, Bearhop S, Redpath SM, Silk MJ, Goodwin CED, Inger R, McDonald RA (2020) Evaluating Bayesian stable isotope mixing models of wild animal diet and the effects of trophic discrimination factors and informative priors. Methods Ecol Evol 11:139–149. https://doi.org/10.1111/2041-210X.13311
Sztukowski LA, Cotton PA, Weimerskirch H, Thompson DR, Torres LG, Sagar PM, Knights AM, Fayet AL, Votier SC (2018) Sex differences in individual foraging site fidelity of Campbell albatross. Mar Ecol Prog Ser 601:227–238. https://doi.org/10.3354/meps12684
Thaxter CB, Daunt F, Hamer KC, Watanuki Y, Harris MP, Grémillet D, Peters G, Wanless S (2009) Sex-specific food provisioning in a monomorphic seabird, the common guillemot Uria aalge: Nest defence, foraging efficiency or parental effort? J Avian Biol 40:75–84. https://doi.org/10.1111/j.1600-048X.2008.04507.x
Tyson C, Kirk H, Fayet A, Van Loon EE, Shoji A, Dean B, Perrins C, Freeman R, Guilford T (2017) Coordinated provisioning in a dual-foraging pelagic seabird. Anim Behav 132:73–79. https://doi.org/10.1016/j.anbehav.2017.07.022
Vasconcelos R, Freitas R, Hazevoet CJ (2015) Cabo verde—história natural das ilhas desertas/the natural history of the Desertas islands. Santa Luzia Branco e Raso, Porto
Votier SC, Fayet AL, Bearhop S, Bodey TW, Clark BL, Grecian J, Guilford T, Hamer KC, Jeglinski JWE, Morgan G, Wakefield E, Patrick SC (2017) Effects of age and reproductive status on individual foraging site fidelity in a long-lived marine predator. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2017.1068
Weimerskirch H (2007) Are seabirds foraging for unpredictable resources? Deep Res Part II: Top Stud Oceanogr 54:211–223. https://doi.org/10.1016/j.dsr2.2006.11.013
Weimerskirch H, Chastel O, Ackermann L, Chaurand T, Cuenot-Chaillet F, Hindermeyer X, Judas J (1994) Alternate long and short foraging trips in pelagic seabird parents. Anim Behav 47:472–476
Weimerskirch H, Le CM, Ropert-Coudert Y, Kato A, Marsac F (2006) Sex-specific foraging behaviour in a seabird with reversed sexual dimorphism: the red-footed booby. Oecologia 146:681–691. https://doi.org/10.1007/s00442-005-0226-x
Welcker J, Steen H, Harding AMA, Gabrielsen GW (2009) Sex-specific provisioning behaviour in a monomorphic seabird with a bimodal foraging strategy. Ibis 151:502–513. https://doi.org/10.1111/j.1474-919X.2009.00931.x
Wilson RP, White CR, Quintana F, Halsey LG, Liebsch N, Martin GR, Butler PJ (2006) Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant. J Anim Ecol 75:1081–1090. https://doi.org/10.1111/j.1365-2656.2006.01127.x
Wilson RP, Pütz K, Peters G, Culik B, Scolaro JA, Charrassin J-B, Ropert-Coudert Y (1997) Long-term attachment of transmitting and recording devices to penguins and other seabirds. Wildl Soc Bull 25:101–106
Wilson RP, Gómez-Laich A, Sala JE, Dell’Omo G, Holton MD, Quintana F (2017) Long necks enhance and constrain foraging capacity in aquatic vertebrates. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2017.2072
Wojczulanis-Jakubas K, Araya-Salas M, Jakubas D (2018) Seabird parents provision their chick in a coordinated manner. PLoS ONE 13:1–13. https://doi.org/10.1371/journal.pone.0189969
Xavier JC, Cherel Y (2009) Cephalopod beak guide for the Southern Ocean. British Antarctic Survey, Cambridge
Xavier JC, Cherel Y, Medeiros R, Velez N, Dewar M, Ratcliffe N, Carreiro AR, Trathan PN (2018) Conventional and molecular analysis of the diet of gentoo penguins: contributions to assess scats for non-invasive penguin diet monitoring. Polar Biol 41:2275–2287. https://doi.org/10.1007/s00300-018-2364-8
Young HS, McCauley DJ, Dirzo R, Dunbar RB, Shaffer SA (2010) Niche partitioning among and within sympatric tropical seabirds revealed by stable isotope analysis. Mar Ecol Prog Ser 416:285–294. https://doi.org/10.3354/meps08756
Zajková Z, Militão T, González-Solís J (2017) Year-round movements of a small seabird and oceanic isotopic gradient in the tropical Atlantic. Mar Ecol Prog Ser 579:169–183. https://doi.org/10.3354/meps12269
Zango L, Navarro-Herrero L, García-Vendrell M, Safi K, González-Solís J (2020) Niche partitioning and individual specialization among age, breeding status and sex classes in a long-lived seabird. Anim Behav 170:1–14. https://doi.org/10.1016/j.anbehav.2020.10.001
Zhang J, Rayner M, Vickers S, Landers T, Sagar R, Stewart J, Dunphy B (2019) GPS telemetry for small seabirds: using hidden Markov models to infer foraging behaviour of common diving petrels (Pelecanoides urinatrix urinatrix). Emu 119:126–137. https://doi.org/10.1080/01584197.2018.1558997
Zurell D, Franklin J, König C, Bouchet PJ, Dormann CF, Elith J, Fandos G, Feng X, Guillera-Arroita G, Guisan A, Lahoz-Monfort JJ, Leitão PJ, Park DS, Peterson AT, Rapacciuolo G, Schmatz DR, Schröder B, Serra-Diaz JM, Thuiller W, Yates KL, Zimmermann NE, Merow C (2020) A standard protocol for reporting species distribution models. Ecography 43:1261–1277. https://doi.org/10.1111/ecog.04960
Acknowledgements
We are grateful to Biosfera I and its staff for the logistics, namely transport to the colony and all the provided conditions, supplies and companionship during fieldwork. We are thankful for the comments and suggestion of changes provided by two anonymous referees and the editor, which improved the overall quality of the manuscript.
Funding
This work received financial and logistic support (for fieldwork campaigns, GPS tracking devices and laboratory analysis) from the project Alcyon—Conservation of seabirds from Cabo Verde, coordinated by BirdLife International and funded by the MAVA foundation (MAVA17022; https://mava-foundation.org/oaps/promoting-the-conservation-of-sea-birds/), through its strategic plan for West Africa (2017–2022). IR and NA received PhD and MSc grants, respectively, from MAVA through the Alcyon project. AC were funded by PhD grants from the Portuguese Foundation for Science and Technology (FCT) (SFRH/BD/139019/2018). This study benefitted from national funds through FCT, I.P., within the scope of the project UIDB/04292/2020 granted to MARE - Marine and Environmental Sciences Centre and project LA/P/0069/2020 granted to the Associate Laboratory ARNET.
Author information
Authors and Affiliations
Contributions
IS, JAR, and VHP: conceptualisation and methodology. IS, FRC, IR, NA, and SA carried out the fieldwork and collected the samples. ARC and RJL undertook the molecular sexing of birds and prey identification. IS and DM carried out the stable isotope analysis. PG provided logistical and fieldwork support. IS, JAR, and VHP: investigation, writing, and visualisation. All the authors have read, reviewed, and edited the manuscript and approved its submission.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
All applicable institutional and/or national guidelines for the care and use of animals were followed. All animals were handled in strict accordance with good animal practice as defined by the current European legislation. All animal work was approved by the “National Directorate of the Environment” of Cabo Verde (DNA) through licences issued annually, authorising the work carried out at Raso Islet, Desertas Islands Natural Reserve. All sampling procedures and/or experimental manipulations have been reviewed and specifically approved as part of obtaining the field license.
Additional information
Responsible Editor: T. Clay.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
dos Santos, I., Ramos, J.A., Ceia, F.R. et al. Sexual segregation in the foraging distribution, behaviour, and trophic niche of the endemic Boyd’s shearwater (Puffinus lherminieri boydi). Mar Biol 169, 144 (2022). https://doi.org/10.1007/s00227-022-04127-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-022-04127-7