An holistic ecological analysis of the diet of Cory's shearwaters using prey morphological characters and DNA barcoding

Molecular Ecology

Volumn 23, Issue 15, 2014, Pages 3719-3733

  Alonso, Hany ^a,b,d   Granadeiro, José P ^c   Waap, Silke ^a,e   Xavier, José ^b   Symondson, William O C ^e   Ramos, Jaime A ^b   Catry, Paulo ^a  

^a INSTITUTO SUPERIOR DE PSICOLOGIA APLICADA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF LISBON   (Portugal)

^d Museu Nacional de Historia Natural Universidade de Lisboa   (Portugal)

^e CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Calonectris diomedea; nonbreeders; prebreeding; prey identification; Selvagens; sexual segregation

Indexed keywords

ANIMALIA; AVES; CALONECTRIS DIOMEDEA; CEPHALOPODA; PROCELLARIIDAE;

RNA 16S;

AFRICA; ANIMAL; BIRD; CALONECTRIS DIOMEDEA; CEPHALOPOD; CLASSIFICATION; CONFERENCE PAPER; DIET; DNA BARCODING; ECOSYSTEM; FEMALE; FISH; FOOD CHAIN; GENETICS; ISLAND (GEOLOGICAL); MALE; MOLECULAR GENETICS; NONBREEDERS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PREBREEDING; PREDATION; PREY IDENTIFICATION; SEASON; SELVAGENS; SEXUAL SEGREGATION; STOMACH JUICE;

CALONECTRIS DIOMEDEA; NONBREEDERS; PREBREEDING; PREY IDENTIFICATION; SELVAGENS; SEXUAL SEGREGATION;

AFRICA; ANIMALS; BIRDS; CEPHALOPODA; DIET; DNA BARCODING, TAXONOMIC; ECOSYSTEM; FEMALE; FISHES; FOOD CHAIN; GASTROINTESTINAL CONTENTS; ISLANDS; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; PREDATORY BEHAVIOR; RNA, RIBOSOMAL, 16S; SEASONS;

EID: 84904730746     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12785     Document Type: Conference Paper

References (64)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.
2. Barnett A, Redd KS, Frusher SD, Stevens JD, Semmens JM, (2010) Non-lethal method to obtain stomach samples from a large marine predator and the use of DNA analysis to improve dietary information. Journal of Experimental Marine Biology and Ecology, 393, 188-192.
3. Barrett RT, Camphuysen KCJ, Anker-Nilssen T, et al,. (2007) Diet studies of seabirds: a review and recommendations. ICES Journal of Marine Science, 64, 1675-1691.
4. Belda EJ, Sanchez A, (2001) Seabird mortality on longline fisheries in the western Mediterranean: factors affecting bycatch and proposed mitigating measures. Biological Conservation, 98, 357-363.
5. Bowen WD, Iverson SJ, (2013) Methods of estimating marine mammal diets: a review of validation experiments and sources of bias and uncertainty. Marine Mammal Science, 29, 719-754.
6. Bowser AK, Diamond AW, Addison JA, (2013) From puffins to plankton: a DNA-based analysis of a Seabird Food Chain in the Northern Gulf of Maine. PLoS ONE, 8, e83152.
7. Castillo-Guerrero JA, Mellink E, (2011) Occasional inter-sex differences in diet and foraging behavior of the Blue-footed Booby: maximizing chick rearing in a variable environment? Journal of Ornithology, 152, 269-277.
8. Dai L, Zheng X, Kong L, Li Q, (2012) DNA barcoding analysis of Coleoidea (Mollusca: Cephalopoda) from Chinese waters. Molecular Ecology Resources, 12, 437-447.
9. Daunt F, Wanless S, Harris MP, Money L, Monaghan P, (2007) Older and wiser: improvements in breeding success are linked to better foraging performance in European shags. Functional Ecology, 21, 561-567.
10. De Laet (2010) Letter to the editor. A problem in POY tree searches (and its work-around) when some sequences are observed to be absent in some terminals. Cladistics, 26, 453-455.
11. Deagle BE, Gales NJ, Evans K, et al,. (2007) Studying seabird diet through genetic analysis of faeces: a case study on macaroni penguins (Eudyptes chrysolophus). PLoS ONE, 2, e831.
12. Deagle BE, Chiaradia A, McInnes J, Jarman SN, (2010) Pyrosequencing faecal DNA to determine diet of little penguins: is what goes in what comes out? Conservation Genetics, 11, 2039-2048.
13. Dunn MR, Szabo A, McVeagh MS, Smith PJ, (2010) The diet of deepwater sharks and the benefits of using DNA identification of prey. Deep Sea Research Part I, 57, 923-930.
14. Forero MG, Hobson KA, Bortolotti GR, Donázar JA, Bertellotti M, Blanco G, (2002) Food resource utilisation by the Magellanic penguin evaluated through stable-isotope analysis: segregation by sex and age and influence on offspring quality. Marine Ecology Progress Series, 234, 289-299.
15. Goss-Custard JD, Durell SLVD, McGrorty S, Reading CJ, (1982) Use of mussel Mytilus edulis beds by oystercatchers Haematopus ostralegus according to age and population size. Journal of Animal Ecology, 51, 543-554.
16. Granadeiro JP, (1993) Variation in measurements of Cory's Shearwater between populations and sexing by discriminant analysis. Ringing and Migration, 14, 103-112.
17. Granadeiro JP, Monteiro LR, Furness RW, (1998) Diet and feeding ecology of Cory's shearwater Calonectris diomedea in the Azores, north-east Atlantic. Marine Ecology Progress Series, 166, 267-276.
18. Granadeiro JP, Dias MP, Rebelo R, Santos CD, Catry P, (2006) Numbers and population trends of Cory's Shearwater Calonectris diomedea at Selvagem Grande, northeast Atlantic. Waterbirds, 29, 56-60.
19. Granadeiro JP, Alonso H, Almada V, Menezes D, Phillips RA, Catry P, (2009) Mysterious attendance cycles in Cory's shearwater Calonectris diomedea: an exploration of patterns and hypotheses. Animal Behaviour, 78, 1455-1462.
20. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
21. den Hartog JC, Clarke MR, (1996) A study of stomach contents of Cory's Shearwater, Calonectris diomedea borealis (Cory, 1881) (Aves: Procellariidae), from the Macaronesian Islands. Zoologische Mededeelingen, 70, 117-133.
22. Hebert PDN, Cywinska A, Ball SL, deWaard JR, (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London-Biological Sciences, 270, 313-321.
23. Jarman SN, Gales NJ, Tierney M, Gill PC, Elliott NG, (2002) A DNA-based method for identification of krill species and its application to analysing the diet of marine vertebrate predators. Molecular Ecology, 11, 2679-2690.
24. Jarman SN, McInnes JC, Faux C, et al,. (2013) Adélie penguin population diet monitoring by analysis of food DNA in scats. PLoS ONE, 8, e82227.
25. Jedlicka JA, Sharma AM, Almeida RP, (2013) Molecular tools reveal diets of insectivorous birds from predator fecal matter. Conservation Genetics Resources, 5, 879-885.
26. Kimura M, (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111-120.
27. Kitowski I, (2003) Age-related differences in foraging behavior of Montagu's harrier Circus pygargus males in south-east Poland. Acta Ethologica, 6, 35-38.
28. Kochzius M, Seidel C, Antoniou A, et al,. (2010) Identifying fishes through DNA barcodes and microarrays. PLoS ONE, 5, e12620.
29. Lewallen EA, Pitman RL, Kjartanson SL, Lovejoy NR, (2011) Molecular systematics of flyingfishes (Teleostei: Exocoetidae): evolution in the epipelagic zone. Biological Journal of the Linnean Society, 102, 161-174.
30. Lucifora LO, García VB, Menni RC, Escalante AH, Hozbor NM, (2009) Effects of body size, age and maturity stage on diet in a large shark: ecological and applied implications. Ecological Research, 24, 109-118.
31. Mougin J-L, Jouanin C, Roux F, (1997) Intermittent breeding in Cory's Shearwater Calonectris diomedea of Selvagem Grande, North Atlantic. Ibis, 139, 40-44.
32. Naito Y, Costa DP, Adachi T, Robinson PW, Fowler M, Takahashi A, (2013) Unravelling the mysteries of a mesopelagic diet: a large apex predator specializes on small prey. Functional Ecology, 27, 710-717.
33. Navarro J, González-Solís J, Viscor G, (2007) Nutritional and feeding ecology in Cory's shearwater Calonectris diomedea during breeding. Marine Ecology Progress Series, 351, 261-271.
34. Navarro J, Kaliontzopoulou A, Gonzalez-Solis J, (2009) Sexual dimorphism in bill morphology and feeding ecology in Cory's shearwater (Calonectris diomedea). Zoology, 112, 128-138.
35. Neves VC, Nolf D, Clarke M, (2012) Spatio-temporal variation in the diet of Cory's shearwater Calonectris diomedea in the Azores archipelago, north-east Atlantic. Deep Sea Research Part I, 70, 1-13.
36. Oksanen J, Blanchet FG, Kindt R, et al,. (2011) vegan: Community Ecology Package. R Package Version 2.0-2. http://CRAN.R-project.org/package=vegan
37. Oro D, Torres R, Rodríguez C, Drummond H, (2010) Climatic influence on demographic parameters of a tropical seabird varies with age and sex. Ecology, 91, 1205-1214.
38. Paiva VH, Xavier JC, Geraldes P, Ramírez I, Garthe S, Ramos JA, (2010) Foraging ecology of Cory's shearwaters in different oceanic environments of the North Atlantic. Marine Ecology Progress Series, 410, 257-268.
39. Paiva VH, Geraldes P, Marques V, Rodríguez R, Garthe S, Ramos JA, (2013) Effects of environmental variability on different trophic levels of the North Atlantic food web. Marine Ecology Progress Series, 477, 15-28.
40. Palumbi SR, (1996) Nucleic acids II: the polymerase chain reaction. In: Molecular Systematics (eds, Hillis DM, Mable BK, &, Moritz C,), pp. 205-247. Sinauer, Sunderland, MA.
41. Phillips RA, Silk JRD, Phalan B, Catry P, Croxall JP, (2004) Seasonal sexual segregation in two Thalassarche albatross species: competitive exclusion, reproductive role specialization or foraging niche divergence? Proceedings of the Royal Society of London-Biological Sciences, 271, 1283-1291.
42. Phillips RA, McGill RAR, Dawson DA, Bearhop S, (2011) Sexual segregation in distribution, diet and trophic level of seabirds: insights from stable isotope analysis. Marine Biology, 158, 2199-2208.
43. Polis GA, (1984) Age structure component of niche width and intraspecific resource partitioning: can age groups function as ecological species? American Naturalist, 123, 541-564.
44. Pompanon F, Deagle BE, Symondson WOC, Brown DS, Jarman SD, Taberlet P, (2012) Who is eating what: diet assessment using next generation sequencing. Molecular Ecology, 21, 1931-1950.
45. Quéro J-C, Porché P, Vayne JJ, (2003) Guide des Poissons de l'Atlantique Européen. Delachaux & Niestlé, Paris.
46. R Development Core Team (2010) R: A Language and Environment for Statistical Computing (2.10.1). R Foundation for Statistical Computing, Vienna.
47. Ramos JA, Granadeiro JP, Phillips RA, Catry P, (2009) Flight morphology and foraging behaviour of male and female Cory's Shearwaters. Condor, 111, 424-432.
48. Ramos R, Granadeiro JP, Rodríguez B, et al,. (2013) Meta-population feeding grounds of Cory's shearwater in the subtropical Atlantic Ocean: implications for the definition of Marine Protected Areas based on tracking studies. Diversity and Distributions, 19, 1284-1298.
49. Symondson WOC, (2002) Molecular identification of prey in predator diets. Molecular Ecology, 11, 627-641.
50. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, (2013) MEGA 6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725-2729.
51. Thibault J-C, Bretagnolle V, Rabouam C, (1997) Calonectris diomedea Cory's Shearwater. Birds of the Western Palearctic Update, 1, 75-98.
52. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighing, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673-4680.
53. Tuset VM, Lombarte A, Assis CA, (2008) Otolith atlas for the western Mediterranean, north and central eastern Atlantic. Scientia Marina, 72, 7-198.
54. Valdez-Moreno M, Quintal-Lizama C, Gõmez-Lozano R, García-Rivas MdC, (2012) Monitoring an alien invasion: DNA barcoding and the identification of lionfish and their prey on coral reefs of the Mexican caribbean. PLoS ONE, 7, e36636.
55. Varõn A, Vinh LS, Wheeler WC, (2010) POY version 4: phylogenetic analysis using dynamic homologies. Cladistics, 26, 72-85.
56. Votier SC, Grecian WJ, Patrick S, Newton J, (2011) Inter-colony movements, at sea behaviour and foraging in an immature seabird: results from GPS-PTT tracking, radiotracking and stable isotope analysis. Marine Biology, 158, 355-362.
57. Weimerskirch H, Le Corre M, Ropert-Coudert Y, Kato A, Marsac F, (2006) Sex-specific foraging behaviour in a seabird with reversal sexual dimorphism: the red-footed booby. Oecologia, 146, 681-691.
58. Wilson RP, (1984) An improved stomach pump for penguins and other seabirds. Journal of Field Ornithology, 55, 109-112.
59. Wilson LJ, Daunt F, Wanless S, (2004) Self-feeding and chick-provisioning diet differ in the common guillemot Uria aalge. Ardea, 92, 197-208.
60. Wilson JJ, Rougerie R, Schonfeld J, et al,. (2011) When species matches are unavailable are DNA barcodes correctly assigned to higher taxa? An assessment using sphingid moths. BMC Ecology, 11, 1-14.
61. Xavier JC, Croxall JP, (2005) Sexual differences in foraging behaviour and diets: a case study of wandering albatrosses. In: Sexual Segregation in Vertebrates: Ecology of the Two Sexes (eds, Ruckstuhl KE, &, Neuhaus P,), pp. 74-91. Cambridge University Press, Cambridge.
62. Xavier JC, Magalhães MC, Mendonça AS, et al,. (2011) Changes in diet of Cory's Shearwaters Calonectris diomedea breeding in the Azores. Marine Ornithology, 39, 129-134.
63. Zavalaga CB, Benvenuti S, Dall'Antonia L, Emslie SD, (2007) Diving behavior of blue-footed boobies Sula nebouxii in northern Peru in relation to sex, body size and prey type. Marine Ecology Progress Series, 336, 291-303.
64. Zhang J, Hanner R, (2012) Molecular approach to the identification of fish in the South China Sea. PLoS ONE, 7, e30621.