Food web characterization based on δ15N and δ13C reveals isotopic niche partitioning between fish and jellyfish in a relatively pristine ecosystem

Marine Ecology Progress Series

Volumn 519, Issue , 2015, Pages 13-27

  Nagata, Renato Mitsuo ^a   Moreira, Marcelo Zacharias ^a   Pimentel, Caio Ribeiro ^a   Morini, André Carrara ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Dietary overlap; Forage fish; Gelatinous zooplankton; Stable isotopes; Trophic position

Indexed keywords

ADAPTATION; BENTHOS; ENVIRONMENTAL STRESS; FISH; FOOD WEB; NICHE OVERLAP; NICHE PARTITIONING; PRISTINE ENVIRONMENT; SEASONAL VARIATION;

BRAZIL; CANANEIA ESTUARY; SAO PAULO [BRAZIL];

PISCES; SCYPHOZOA;

EID: 84921909806     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps11071     Document Type: Article

References (74)

1. Ara K (2004) Temporal variability and production of the planktonic copepod community in the Cananéia Lagoon estuarine system, São Paulo, Brazil. Zool Stud 43:179-186
2. Barcellos RL, Camargo PB, Galvão A, Weber RR (2009) Sedimentary organic matter in cores of the Cananéia-Iguape Lagoonal-Estuarine System, São Paulo State, Brazil. J Coast Res 56:1335-1339
3. Bond CE (1996) Biology of fishes. Saunders College Publishing, New York, NY
4. Bouillon S, Koedam N, Raman AV, Dehairs F (2002) Primary producers sustaining macro-invertebrate communities in intertidal mangrove forests. Oecologia 130:441-448
5. Brodeur RD, Sugisaki H, Hunt GL Jr (2002) Increases in jelly fish biomass in the Bering Sea: implications for the ecosystem. Mar Ecol Prog Ser 233:89-103
6. Brodeur RD, Suchman CL, Reese D, Miller T, Daly E (2008) Spatial overlap and trophic interactions between fish and large jellyfish in the Northern California Current. Mar Biol 154:649-659
7. Brotz L, Cheung WWL, Kleisner K, Pakhomov E, Pauly D (2012) Increasing jellyfish populations: trends in large marine ecosystems. Hydrobiologia 690:3-20
8. Condon RH, Graham WM, Duarte CM, Pitt KA and others (2012) Questioning the rise of gelatinous zooplankton in the world's oceans. Bioscience 62:160-189
9. 15N and trophic fractionation in jellyfish: implications for food web ecology. Mar Biol 161:473-480
10. DeNiro MJ, Epstein S (1977) Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197:261-263
11. Din ZB, Gunter G (1986) The food and feeding habits of the common bay anchovy, Anchoa mitchilli (Valenciennes). Pertanika 9:99-108
12. Eiane K, Aksnes DL, Bagøien E, Kaartvedt S (1999) Fish or jellies - a question of visibility? Limnol Oceanogr 44:1352-1357
13. Eskinazi-Sant'Anna EM (2000) Estudo da dieta natural de Parvocalanus crassirostris, Paracalanus quasimodo, Temora stylifera e Temora turbinata (Copepoda, Calanoida), no Canal de São Sebastião (SP, Brasil). PhD dissertation. Universidade de São Paulo
14. Fleming NEC, Houghton JDR, Magill CL, Harrod C (2011) Preservation methods alter stable isotope values in gelatinous zooplankton: implications for interpreting trophic ecology. Mar Biol 158:2141-2146
15. France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307-312
16. Frank KT, Petrie B, Shackell NL (2007) The ups and downs of trophic control in continental shelf ecosystems. Trends Ecol Evol 22:236-242
17. Gibbons MJ, Richardson AJ (2013) Beyond the jellyfish joyride and global oscillations: advancing jellyfish research. J Plankton Res 35:929-938
18. Gonzalez A, Loreau M (2009) The causes and consequences of compensatory dynamics in ecological communities. Annu Rev Ecol Evol Syst 40:393-414
19. Grac¸a-Lopes R, Puzzi A, Severino-Rodrigues E, Bartolotto AS, Guerra DSF, Figueiredo KLB (2002) Comparac¸ão entre a produc¸ão de camarão-sete-barbas e de fauna acompanhante pela frota de pequeno porte sediada na praia de Perequê, estado de São Paulo, Brasil. Bol Inst Pesca 28:189-194
20. Granhag L, Møller LF, Hansson LJ (2011) Size-specific clearance rates of the ctenophore Mnemiopsis leidyi based on in situ gut content analyses. J Plankton Res 33:1043-1052
21. Hagen W, Auel H (2001) Seasonal adaptations and the role of lipids in oceanic zooplankton. Zoology 104:313-326
22. Heileman S, Gasalla MA (2008) South Brazil Shelf LME. In: Sherman K, Hempel G (eds) The UNEP large marine ecosystems report: a perspective on changing conditions in LMEs of the world's regional seas, 2nd edn, United Nations Environmental Program (UNEP), Nairobi, p 723-734
23. Heithaus ER, Heithaus PA, Heithaus MR, Burkholder D, Layman CA (2011) Trophic dynamics in a relatively pristine subtropical fringing mangrove community. Mar Ecol Prog Ser 428:49-61
24. Höfling JC, Ferreira LI, Ribeiro Neto FB, Oliveira MP, Paiva Filho AM, Prado A (2000) Alimentac¸ão de peixes da família Clupeidae do complexo estuarino lagunar de Cananéia, São Paulo, Brasil. Bioikos 14:12-20
25. 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
26. 15N signatures of selected marine organisms. Mar Ecol Prog Ser 219:299-304
27. Knoppers B, Kjerfve B (1999) Coastal lagoons of southeastern Brazil: physical and biogeochemical characteristics. In: Perillo G, Picolo M, Pino-Quivira C (eds) Estuaries of South America. Springer, Berlin, p 57-82
28. Larson RJ (1991) Diet, prey selection and daily ration of Stomo lophus meleagris, a filter-feeding scyphomedusa from the NE Gulf of Mexico. Estuar Coast Shelf Sci 32:511-525
29. Layman CA, Araujo MS, Boucek R, Hammerschlag-Peyer CM and others (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev Camb Philos Soc 87:545-562
30. Lopes RM, Katsuragawa M, Dias JF, Montú MA, Muelbert JH, Gorri C, Brandini FP (2006) Zooplankton and ichthyoplankton distribution in the southern Brazilian shelf: an overview. Sci Mar 70:189-202
31. Lynam CP, Brierley AS (2007) Enhanced survival of 0-group gadoid fish under jellyfish umbrellas. Mar Biol 150:1397-1401
32. Macpherson E (2002) Large-scale species-richness gradients in the Atlantic Ocean. Proc R Soc B 269:1715-1720
33. Mendonc¸a JT, Katsuragawa M (2001) Caracterizac¸ão da pesca artesanal no complexo estuarino-lagunar de Cananéia-Iguape, Estado de São Paulo, Brasil (1995-1996). Acta Sci Bid Sci 23:535-547
34. Mianzan HW, Guerrero RA (2000) Environmental patters and biomass distribution of gelatinous macrozooplankton: three study cases in the South-western Atlantic Ocean. Sci Mar 64(Suppl 1):215-224
35. 15N and animal age. Geochim Cosmochim Acta 48:1135-1140
36. Ministério do Meio Ambiente (MMA) (2007) Áreas prioritárias para a conservac¸ão, uso sustentável e repartic¸ão de benefícios da biodiversidade brasileira: atualizac¸ão - Portaria MMA No. 09, 23/01/2007. Série Biodiversidade (31). MMA/SBF, Bras̈lia
37. Möller H (1980) Scyphomedusae as predators and food competitors of larval fish. Meeresforschung 28:90-100
38. Morandini AC (2003) Estrutura populacional de Chrysaora lactea e Lychnorhiza lucerna (Cnidaria, Scyphozoa) em amostras de plâncton, com a redescric¸ão das espécies. PhD dissertation, Instituto de Biociências da Universidade de São Paulo
39. Morandini AC, Ascher D, Stampar SN, Ferreira JFV (2005) Cubozoa e Scyphozoa (Cnidaria: Medusozoa) de águas costeiras do Brasil. Iheringia. Sér Zool 95:281-294
40. Moreira MGBS (1961) Sôbre Mastigias scintillae sp.nov. (Scyphomedusae, Rhizostomeae) das costas do Brasil. Bolm Inst Oceanogr 11:5-30
41. Nagata RM, Haddad MA, Nogueira M Jr (2009) The nuisance of medusae (Cnidaria, Medusozoa) to shrimp trawls in central part of southern Brazilian Bight, from the perspective of artisanal fishermen. Pan-Am J Aquat Sci 4:312-325
42. Newsome SD, Del Rio CM, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5:429-436
43. Newsome SD, Yeakel JD, Wheatley PV, Tinker T (2012) Tools for quantifying isotopic niche space and dietary variation at the individual and population level. J Mammal 93:329-341
44. Nogueira M Jr, Nagata RM, Haddad MA (2010) Seasonal variation of macromedusae (Cnidaria) at North Bay, Florianópolis, Southern Brazil. Zoologia 27:377-386
45. Ohtsuka S, Koike K, Lindsay D, Nishikawa J and others (2009) Symbionts of marine medusae and ctenophores. Plankton Benthos Res 4:1-13
46. Parnell A, Inger R, Bearhop S, Jackson AL (2008) SIAR: stable isotope analysis in R. (Accessed 01 Nov 2013)
47. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Ecology 18:293-320
48. Pitt KA, Clement AL, Connolly RM, Thibault-Botha D (2008) Predation by jellyfish on large and emergent zooplankton: implications for benthic-pelagic coupling. Estuar Coast Shelf Sci 76:827-833
49. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703-718
50. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrocchi J, Montãa GC (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analysis. Oecologia 152:179-189
51. Potter IC, Bird DJ, Claridge PN, Clarke KR, Hyndes GA, Newton LC (2001) Fish fauna of the Severn Estuary. Are there long-term changes in abundance and species composition and are the recruitment patterns of the main marine species correlated? J Exp Mar Biol Ecol 258:15-37
52. Purcell JE (1997) Pelagic cnidarians and ctenophores as predators: selective predation, feeding rates and effects on prey populations. Ann Inst Oceanogr 73:125-137
53. Purcell JE (2012) Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Annu Rev Mar Sci 4:209-235
54. Purcell JE, Arai MN (2001) Interactions of pelagic cnidarians and ctenophores with fishes: a review. Hydrobiologia 451:27-44
55. Purcell JE, Grover JJ (1990) Predation and food limitation as causes of mortality in larval herring at a spawning ground in British Columbia. Mar Ecol Prog Ser 59:55-61
56. Purcell JE, Sturdevant MV (2001) Prey selection and dietary overlap among zooplanktivorous jellyfish and juvenile fishes in Prince William Sound, Alaska. Mar Ecol Prog Ser 210:67-83
57. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
58. Riascos JM, Villegasa V, Pachecoa AS (2014) Diet composition of the large scyphozoan jellyfish Chrysaora plocamia in a highly productive upwelling centre off northern Chile. Mar Biol Res 10:791-798
59. Richardson AJ, Bakun A, Hays GC, Gibbons MJ (2009) The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends Ecol Evol 24:312-322
60. Schaeffer-Novelli Y, Mesquita HSL, Cintrón-Molero G (1990) The Cananéia lagoon estuarine system, São Paulo, Brazil. Estuaries 13:193-203
61. Sherwood GD, Rose GA (2005) Stable isotope analysis of some representative fish and invertebrates of the Newfoundland and Labrador continental shelf food web. Estuar Coast Shelf Sci 63:537-549
62. Shoji J, Masuda R, Yamashita Y, Tanaka M (2005) Effect of low dissolved oxygen concentrations on behavior and predation rates on fish larvae by moon jellyfish Aurelia aurita and by a juvenile piscivore, Spanish mackerel Scomberomorus niphonius. Mar Biol 147:863-868
63. Shoji J, Mizuno KI, Yamamoto M, Miller TW, Hamaoka H, Omori K (2009) Spatial distribution and dietary overlap between Japanese anchovy Engraulis japonicus and moon jellyfish Aurelia aurita in the Seto Inland Sea, Japan. Sci Mar 73:191-198
64. Silva JTO, Lopes PRD (2002) Notes about the feeding and morphology of digestive system of Chloroscombrus chrysurus (Linnaeus, 1766) (Actinopterygii, Carangidae) in Ponta da Ilha Beach (Itaparica Island, Bahia). Rev Bras Zoociênc 4:179-192
65. Syvöranta J, Harrod C, Kubicek L, Cappanera V, Houghton JDR (2012) Stable isotopes challenge the perception of ocean sunfish Mola mola as obligate jellyfish predators. J Fish Biol 80:225-231
66. Tolley SG (1987) Association of young Chloroscombrus chrysurus (Pisces: Caragidae) with the jellyfish Aurelia aurita. Copeia 1987:216-219
67. Tundisi JG, Matsumura-Tundisi T (2001) The lagoon region and estuary ecosystem of Cananéia, Brazil. In: Seeliger U, Kjerfve B (eds) Coastal marine ecosystems of Latin America. Ecological studies 144. Springer, New York, NY, p 119-130
68. Tundisi J, Matsumura-Tundisi T, Kutner MB (1973) Plankton studies in a mangrove environment. VIII. Further investigations on primary production, standing stock of phyto and zooplankton and some environmental factors. Int Rev Ges Hydrobiol 58:925-940
69. UNESCO (1999) World heritage nomination - IUCN technical evaluation Atlantic forests (southeast) (Brazil). UNESCO, Paris
70. Uye S, Shimauchi H (2005) Population biomass, feeding, respiration and growth rates, and carbon budget of the scyphomedusa Aurelia aurita in the inland Sea of Japan. J Plankton Res 27:237-248
71. 13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061-2066
72. 15N enrichment: a meta-analysis. Oecologia 136:169-182
73. 13C abundances in the Arctic Ocean with emphasis on the biogeochemical structure of the food web. Deep-Sea Res 34:829-841
74. Zamponi M, Mianzan HW (1985) La mecánica de captura y alimentación de Olindias sambaquiensis Müller, 1861 (Limnomedusae) en el medio natural y en condiciones experimentales. Hist Nat (Corrientes) 5:269-278