Abstract
Understanding the fine-scale movements and habitat use patterns of marine predators is critical for identifying important foraging habitat and guiding effective conservation planning. Here, GPS loggers were used to track chick-rearing Cassin’s auklets (Ptychoramphus aleuticus) at their largest breeding colony, located on Triangle Island, British Columbia, Canada (50°51′35″N; 129°4′34″W). Analyses were conducted at both the individual and population level to assess whether inter-annual variation in habitat use (2014, 2015, and 2017) could be explained by dynamic oceanographic features, such as sea surface temperature (SST) and chlorophyll a concentrations, or by static bathymetric features. At both scales of analyses, the foraging behaviour of Cassin’s auklets was most strongly influenced by SST. At the individual level, birds spent more time foraging in areas with lower SST, relative to other areas visited over the course of a foraging trip. At the population level, the at-sea distribution of Cassin’s auklets varied across years, with birds using areas northwest of colony in 2014 and areas west of the colony in 2015 and 2017. Furthermore, the probability of foraging across the study area was higher in areas with lower SST, suggesting that SST influences the broad-scale foraging distribution of Cassin’s auklets. Identification of the environmental drivers of habitat use across multiple years can be used to help in predicting suitable at-sea habitat across time, leading to more effective conservation management.
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References
Adams J, Takekawa JY, Carter HR (2004) Foraging distance and home range of Cassin’s auklets nesting at two colonies in the California Channel Islands. Condor 106:618–637. https://doi.org/10.1650/7428
Adams J, Takekawa JY, Carter HR, Yee J (2010) Factors influencing the at-sea distribution of Cassin’s auklets (Ptychoramphus aleuticus) that breed in the Channel Islands, California. Auk 127:503–513. https://doi.org/10.1525/auk.2010.09273
Ainley DG, Dugger KD, Ford RG, Pierce SD, Reese DC, Brodeur RD, Tynan CT, Barth JA (2009) Association of predators and prey at frontal features in the California Current: competition, facilitation, and co-occurrence. Mar Ecol Prog Ser 389:271–294. https://doi.org/10.3354/meps08153
Ainley DG, Manuwal DA, Adams J, Thoresen AC (2011) Cassin’s auklet (Ptychoramphus aleuticus). In: Poole A (ed) The birds of North America. Cornell Laboratory of Ornithology, Ithaca, NY. https://birdsna.org/Species-Account/bna/species/casauk/
Amélineau F, Grémillet D, Bonnet D, Le Bot T, Fort J (2016) Where to forage in the absence of sea ice?. PLoS One, Bathymetry as a key factor for an Arctic seabird. https://doi.org/10.1371/journal.pone.0157764
Ashmole NP (1963) The regulation of numbers of tropical oceanic birds. Ibis 103:458–473. https://doi.org/10.1111/j.1474-919X.1963.tb06766.x
Avalos MR, Ramos JA, Soares M, Ceia FR, Fagundes AI, Gouveia C, Menezes D, Paiva VH (2017) Comparing the foraging strategies of a seabird predator when recovering from a drastic climatic event. Mar Biol. https://doi.org/10.1007/s00227-017-3082-4
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Boyd WS, McFarlane Tranquilla L, Ryder JL, Shisko SG, Bertram (2008) Variation in marine distributions of Cassin’s auklets (Ptychoramphus aleuticus) breeding at Triangle Island, British Columbia. Auk 125:158–166. https://doi.org/10.1525/auk.2008.125.1.158
Burger AE, Powell DW (1990) Diving depths and diet of Cassin’s Auklet at Reef Island, British Columbia. Can J Zool 68:1572–1577. https://doi.org/10.1139/z90-232
Burnham KP, Anderson DR (2002) Model selection and multimodal inference: a practical information-theoretic approach. Springer, New York
Cai W, Borlace S, Lengaigne M, van Rensch P, Collins M, Vecchi G, Timmermann A, Santoso A, McPhaden MJ, Wu L, England MH, Wang G, Guilyardi E, Jin F-F (2014) Increasing frequency of extreme El Niño events due to greenhouse warming. Nat Clim Chang 4:1–6. https://doi.org/10.1038/nclimate2100
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
Chandler PC, King SA, Perry RI (2015) State of the physical, biological and selected fishery resources of Pacific Canadian marine ecosystems in 2014. Can Tech Rep Fish Aquat Sci 3131
COSEWIC (2014) COSEWIC assessment and status report on the Cassin’s auklet Ptychoramphus aleuticus in Canada. Committee on the Status of Endangered Wildlife in Canada, Ottawa
Crase B, Liedloff AC, Wintle BA (2012) A new method for dealing with residual spatial autocorrelation in species distribution models. Ecography 35:879–888. https://doi.org/10.1111/j.1600-0587.2011.07138.x
Croxall JP, Butchart SHM, Lascelles B, Stattersfield AJ, Sullivan B, Symes A, Taylor P (2012) Seabird conservation status, threats and priority actions: a global assessment. Bird Conserv Int 22:1–34. https://doi.org/10.1017/S0959270912000020
Deppe L, McGregor KF, Tomasetto F, Briskie JV, Scofield RP (2014) Distribution and predictability of foraging areas in breeding Chatham albatrosses Thalassarche eremita in relation to environmental characteristics. Mar Ecol Prog Ser 498:287–301. https://doi.org/10.3354/meps10624
Edelhoff H, Signer J, Balkenhol N (2016) Path segmentation for beginners: an overview of current methods for detecting changes in animal movement patterns. Mov Ecol. https://doi.org/10.1186/s40462-016-0086-5
Freeman R, Dennis T, Landers T, Thompson D, Bell E, Walker M, Guilford T (2010) Black petrels (Procellaria parkinsoni) patrol the ocean shelf-break: GPS tracking of a vulnerable Procellariiform seabird. PLOS One. https://doi.org/10.1371/journal.pone.0009236
Genin A (2004) Bio-physical coupling in the formation of zooplankton and fish aggregations over abrupt topographies. J Mar Syst 50:3–20. https://doi.org/10.1016/j.jmarsys.2003.10.008
Grecian WJ, Witt MJ, Attrill MJ, Bearhop S, Becker PH, Egevang C, Furness RW, Godley BJ, Gonzalez-Solis J, Grémillet D, Kopp M, Lescroel A, Matthiopoulos J, Patrick SC, Peter H-U, Phillips RA, Stenhouse IJ, Votier SC (2016) Seabird diversity hotspot linked to ocean productivity in the Canary Current Large Marine Ecosystem. Biol Lett 12:20160024. https://doi.org/10.1098/rsbl.2016.0024
Green DB, Coetzee JC, Rishworth GM, Pistorius PA (2015) Foraging distribution of Cape gannets in relation to oceanographic features, prey availability and marine protected areas. Mar Ecol Prog Ser 537:277–288. https://doi.org/10.3354/meps11428
Gregg WW, Casey NW (2007) Sampling biases in MODIS and SeaWiFS ocean chlorophyll data. Remote Sens Environ 111:25–35. https://doi.org/10.1016/j.rse.2007.03.008
Grémillet D, Dell’Omo G, Ryan PG, Peters G, Ropert-Coudert Y, Weeks SJ (2004) Offshore diplomacy, or how seabirds mitigate intra-specific competition: a case study based on GPS tracking of Cape gannets from neighbouring colonies. Mar Ecol Prog Ser 268:265–279
Grémillet D, Péron C, Pons J-B, Ouni R, Authier M, Thévenet M, Fort J (2014) Irreplaceable area extends marine conservation hotspot of Tunisia: insights from GPS-tracking Scopoli’s shearwaters from the largest seabird colony in the Mediterranean. Mar Biol 161:2669–2680. https://doi.org/10.1007/s00227-014-2538-z
Hazen EL, Suryan RM, Santora JA, Bograd SJ, Watanuki Y, Wilson RP (2013) Scales and mechanisms of marine hotspot formation. Mar Ecol Prog Ser 487:177–183. https://doi.org/10.3354/meps10477
Hedd A, Ryder JL, Cowen LL, Bertram DF (2002) Inter-annual variation in the diet, provisioning and growth of Cassin’s auklet at Triangle Island, British Columbia: responses to variation in ocean climate. Mar Ecol Prog Ser 229:221–232
Hipfner JM (2008) Matches and mismatches: ocean climate, prey phenology and breeding success in a zooplanktivorous seabird. Mar Ecol Prog Ser 368:295–304. https://doi.org/10.3354/meps07603
Hipfner JM (2009) Euphausiids in the diet of a North Pacific seabird: annual and seasonal variation and the role of ocean climate. Mar Ecol Prog Ser 390:277–289. https://doi.org/10.3354/meps08209
Hooker SK, Cañadas A, Hyrenbach KD, Corrigan C, Polovina JJ, Reeves RR (2011) Making protected area networks effective for marine top predators. Endanger Species Res 13:203–218. https://doi.org/10.3354/esr00322
Irons DB (1998) Foraging area fidelity of individual seabirds in relation to tidal cycles and flock feeding. Ecology 79:647–655. https://doi.org/10.1890/0012-9658(1998)079[0647:FAFOIS]2.0.CO;2
Jones T, Parrish JK, Peterson WT, Bjorkstedt EP, Bond NA, Ballance LT, Bowes V, Hipfner JM, Burgess HK, Dolliver JE, Lindquist K, Lindsey J, Nevins HM, Robertson RR, Roletto J, Wilson L, Joyce T, Harvey J (2018) Massive mortality of a planktivorous seabird in response to a marine heatwave. Geophys Res Lett. https://doi.org/10.1002/2017gl076164
Keister JE, Di Lorenzo E, Morgan CA, Combes V, Peterson WT (2011) Zooplankton species composition is linked to ocean transport in the Northern California Current. Glob Chan Biol 17:2498–2511. https://doi.org/10.1111/j.1365-2486.2010.02383.x
Knechtel HA (1998) Effects of age, gender, and condition on the reproductive effort of Cassin’s Auklets (Ptychoramphus aleuticus) on Triangle Island, British Columbia. MSc thesis, Simon Fraser University, Burnaby
Lee DE, Nur N, Sydeman WJ (2007) Climate and demography of the planktivorous Cassin’s auklet Ptychoramphus aleuticus off northern California: implications for population change. J Anim Ecol 76:337–347. https://doi.org/10.1111/j.1365-2656.2007.01198.x
Lewis S, Sherratt TN, Hamer KC, Wanless S (2001) Evidence of intra-specific competition for food in a pelagic seabird. Nature 412:816–819. https://doi.org/10.1038/35090566
Louzao M, Delord K, García D, Boué A, Weimerskirch H (2012) Protecting persistent dynamic oceanographic features: transboundary conservation efforts are needed for the critically endangered balearic shearwater. PLOS One. https://doi.org/10.1371/journal.pone.0035728
Ludynia K, Kemper J, Roux J-P (2012) The Namibian Islands’ marine protected area: using seabird tracking data to define boundaries and assess their adequacy. Biol Conserv 156:136–145. https://doi.org/10.1016/j.biocon.2011.11.014
Mackas DL, Coyle KO (2005) Shelf-offshore exchange processes, and their effects on mesozooplankton biomass and community composition patterns in the northeast Pacific. Deep Res Part II 52:707–725. https://doi.org/10.1016/j.dsr2.2004.12.020
Mackas DL, Kieser R, Saunders M, Yelland DR, Brown RM, Moore DF (1997) Aggregation of euphausiids and Pacific hake (Merluccius productus) along the outer continental shelf off Vancouver Island. Can J Fish Aquat Sci 54:2080–2096. https://doi.org/10.1139/f97-113
Mackas DL, Thomson RE, Galbraith M (2001) Changes in the zooplankton community of the British Columbia continental margin, 1985–1999, and their covariation with oceanographic conditions. Can J Fish Aquat Sci 58:685–702. https://doi.org/10.1139/cjfas-58-4-685
Mann KH, Lazier JRN (2006) Dynamics of marine ecosystems: biological–physical interactions in the oceans. Blackwell Publishing, Malden
Manugian S, Elliott ML, Bradley R, Howar J, Karnovsky N, Saenz B, Studwell A, Warzybok P, Nur N, Jahncke J (2015) Spatial distribution and temporal patterns of Cassin’s auklet foraging and their euphausiid prey in a variable ocean environment. PLOS One. https://doi.org/10.1371/journal.pone.0144232
Manuwal DA (1974a) The natural history of Cassin’s auklet (Ptychoramphus aleuticus). Condor 76:421–431. https://doi.org/10.2307/1365815
Manuwal DA (1974b) Effects of territoriality on breeding in a population of Cassin’s auklet. Ecology 55:1399–1406. https://doi.org/10.2307/1935468
Marinovic BB, Croll DA, Gong N, Benson SR, Chavez FP (2002) Effects of the 1997–1999 El Niño and La Niña events on zooplankton abundance and euphausiid community composition within the Monterey Bay coastal upwelling system. Prog Oceanogr 54:265–277. https://doi.org/10.1016/S0079-6611(02)00053-8
McGowan J, Hines E, Elliot M, Howar J, Dransfield A, Nur N, Jahncke J (2013) Using seabird habitat modeling to inform marine spatial planning in central California’s National Marine Sanctuaries. PLOS One. https://doi.org/10.1371/journal.pone.0071406
McLeay LJ, Page B, Goldsworthy SD, Paton DC, Teixeira C, Burch P, Ward T (2010) Foraging behaviour and habitat use of a short-ranging seabird, the crested tern. Mar Ecol Prog Ser 411:271–283. https://doi.org/10.3354/meps08606
Morrison KW, Hipfner JM, Blackburn GS, Green DJ (2011) Effects of extreme climate events on adult survival of three Pacific auks. Auk 128:707–715. https://doi.org/10.1525/auk.2011.10198
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. https://doi.org/10.1111/j.2041-210x.2012.00261.x
Nur N, Jahncke J, Herzog MP, Howar J, Hyrenbach KD, Zamon JE, Ainley DG, Wiens JA, Morgan K, Ballance LT, Stralberg D (2011) Where the wild things are: predicting hotspots of seabird aggregations in the California Current System. Ecol Appl 21:2241–2257. https://doi.org/10.1890/10-1460.1
Oppel S, Meirinho A, Ramírez I, Gardner B, O’Connell AF, Miller PI, Louzao M (2012) Comparison of five modelling techniques to predict the spatial distribution and abundance of seabirds. Biol Conserv 156:94–104. https://doi.org/10.1016/j.biocon.2011.11.013
Paiva VH, Geraldes P, Ramírez I, Meirinho A, Garthe S, Ramos JA (2010) Oceanographic characteristics of areas used by Cory’s shearwaters during short and long foraging trips in the North Atlantic. Mar Biol 157:1385–1399. https://doi.org/10.1007/s00227-010-1417-5
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. https://doi.org/10.1371/journal.pone.0139390
Paleczny M, Hammill E, Karpouzi V, Pauly D (2015) Population trend of the world’s monitored seabirds, 1950–2010. PLOS One. https://doi.org/10.1371/journal.pone.0129342
Pichegru L, Grémillet D, Crawford RJM, Ryan PG (2010) Marine no-take zone rapidly benefits endangered penguin. Biol Lett 6:498–501. https://doi.org/10.1098/rsbl.2009.0913
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018) nlme: linear and nonlinear mixed effects models. R package version 3.1-131.1. https://CRAN.R-project.org/package=nlme
Ponchon A, Aulert C, Le Guillou G, Gallien F, Péron C, Grémillet D (2017) Spatial overlaps of foraging and resting areas of black-legged kittiwakes breeding in the English Channel with existing marine protected areas. Mar Biol 164:119. https://doi.org/10.1007/s00227-017-3151-8
Regular PM, Hedd A, Montevecchi WA (2013) Must marine predators always follow scaling laws? Memory guides the foraging decisions of a pursuit-diving seabird. Anim Behav 86(545):552. https://doi.org/10.1016/j.anbehav.2013.06.008
Roberts JJ, Best BD, Dunn DC, Treml EA, Halpin PN (2010) Marine Geospatial Ecology Tools: an integrated framework for ecological geoprocessing with ArcGIS, Python, R, MATLAB, and C++. Environ Model Softw 25:1197–1207
Robertson GS, Bolton M, Grecian WJ, Monaghan P (2014) Inter- and intra-year variation in foraging areas of breeding kittiwakes (Rissa tridactyla). Mar Biol 161:1973–1986. https://doi.org/10.1007/s00227-014-2477-8
Rodway MS (1991) Status and conservation of breeding seabirds in British Columbia. In: Croxall JP (ed) Supplement to the status and conservation of the world’s seabirds. International Council for Bird Preservation, Cambridge, pp 43–102
Rodway MS, Lemon MJF (2011) Use of permanent plots to monitor trends in burrow-nesting seabird populations in British Columbia. Mar Ornithol 39:243–253
Sabarros PS, Grémillet D, Demarcq H, Moseley C, Pichegru L, Mullers RHE, Stenseth NC, Machu E (2014) Fine-scale recognition and use of mesoscale fronts by foraging Cape gannets in the Benguela upwelling region. Deep Res Part II 107:77–84. https://doi.org/10.1016/j.dsr2.2013.06.023
Santora JA, Sydeman WJ, Schroeder ID, Wells BK, Field JC (2011) Mesoscale structure and oceanographic determinants of krill hotspots in the California Current: implications for trophic transfer and conservation. Prog Oceanogr 91:397–409. https://doi.org/10.1016/j.pocean.2011.04.002
Scales KL, Miller PI, Embling CB, Ingram SN, Pirotta E, Votier SC (2014) Mesoscale fronts as foraging habitats: composite front mapping reveals oceanographic drivers of habitat use for a pelagic seabird. J R Soc Interface 11:20140679. https://doi.org/10.1098/rsif.2014.0679
Scales KL, Miller PI, Ingram SN, Hazen EL, Bograd SJ, Phillips RA (2016) Identifying predictable foraging habitats for a wide-ranging marine predator using ensemble ecological niche models. Divers Distrib 22:212–224. https://doi.org/10.1111/ddi.12389
Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113. https://doi.org/10.1111/j.2041-210X.2010.00012.x
Speich S, Manuwal DA (1974) Gular pouch development and population structure of Cassin’s auklet. Auk 91:291–306
Suryan RM, Sato F, Balogh GR, Hyrenbach KD, Sievert PR, Ozaki K (2006) Foraging destinations and marine habitat use of short-tailed albatrosses: a multi-scale approach using first-passage time analysis. Deep Res Part II 53:370–386. https://doi.org/10.1016/j.dsr2.2006.01.012
Suryan RM, Santora JA, Sydeman WJ (2012) New approach for using remotely sensed chlorophyll a to identify seabird hotspots. Mar Ecol Prog Ser 451:213–225. https://doi.org/10.3354/meps09597
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. www.r-project.org
Thomson RE (1981) Oceanography of the British Columbia coast. Canada Department of Fisheries and Oceans, Ottawa, Canada
Thoresen AC (1964) The breeding behavior of the Cassin Auklet. Condor 66:456–476. https://doi.org/10.2307/1365223
Trathan PN, García-Borboroglu P, Boersma D, Bost CA, Crawford RJM, Crossin GT, Cuthbert RJ, Dann P, Davis LS, De La Puente S, Ellenberg U, Lynch HJ, Mattern T, Pütz K, Seddon PJ, Trivelpiece W, Wienecke B (2014) Pollution, habitat loss, fishing, and climate change as critical threats to penguins. Conserv Biol 29:31–41. https://doi.org/10.1111/cobi.12349
Warwick-Evans V, Atkinson PW, Gauvain RD, Robinson LA, Arnould JPY, Green JA (2015) Time-in-area represents foraging activity in a wide-ranging pelagic forager. Mar Ecol Prog Ser 527:233–246. https://doi.org/10.3354/meps11262
Warwick-Evans V, Ratcliffe N, Lowther AD, Manco F, Ireland L, Clewlow HL, Trathan PN (2018) Using habitat models for chinstrap penguins Pygoscelis antarctica to advise krill fisheries management during the penguin breeding season. Biodivers Res https://doi.org/10.1111/ddi.12817
Watanuki Y, Daunt F, Takahashi A, Newell M, Wanless S, Sato K, Miyazaki N (2008) Microhabitat use and prey capture of a bottom-feeding top predator, the European shag, shown by camera loggers. Mar Ecol Prog Ser 356:283–293. https://doi.org/10.3354/meps07266
Wolf SG, Sydeman WJ, Hipfner JM, Abraham CL, Tershy BR, Croll DA (2009) Range-wide reproductive consequences of ocean climate variability for the seabird Cassin’s Auklet. Ecology 90:742–753. https://doi.org/10.1890/07-1267.1
Wolf SG, Snyder MA, Sydeman WJ, Doak DF, Croll DA (2010) Predicting population consequences of ocean climate change for an ecosystem sentinel, the seabird Cassin’s auklet. Glob Chang Biol 16:1923–1935. https://doi.org/10.1111/j.1365-2486.2010.02194.x
Zuur A, Ieno EN, Smith GM (2007) Analyzing ecological data. Springer, New York
Acknowledgements
This research would not have been possible without the help of many dedicated volunteers and field technicians. We owe special thanks to Connie Smith (Centre for Wildlife Ecology) for logistical support, and to West Coast Helicopters and the Canadian Coast Guard for safe transport to field sites. Access to field sites was granted by British Columbia Parks.
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Funding was provided by Environment and Climate Change Canada (JMH), Natural Sciences and Engineering Research Council (NSERC) Discovery Grant (DJG), and NSERC Canada Graduate Scholarship (ADD).
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Research was conducted under permits from Environment Canada (banding permit #10667; scientific permits BC-14-0026#1, BC-15-0005, BC-17-0028). Wildlife protocols were approved by Simon Fraser University Animal Care Services in 2017 (1229B-94), and Environment Canada’s Western and Northern Animal Care Committee in 2014, 2015, and 2017 (14MH01, 15MH01, 17MH01).
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Domalik, A.D., Hipfner, J.M., Studholme, K.R. et al. At-sea distribution and fine-scale habitat use patterns of zooplanktivorous Cassin’s auklets during the chick-rearing period. Mar Biol 165, 177 (2018). https://doi.org/10.1007/s00227-018-3434-8
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DOI: https://doi.org/10.1007/s00227-018-3434-8