Abstract
The seasonal variability of stable isotope values (δ15N and δ13C), ∆15N values, and niche width of calanoid copepod species, three zooplankton size fractions and seston were assessed from samples obtained monthly between January and December 2012 at a coastal sampling site in the Eastern Tropical Pacific off Mexico (19°09′03″ N, 104°44′50″ W). Twenty calanoid copepod species were analyzed, 15 of which were sampled in both the cool, productive ‘mixed’ period and the warm, oligotrophic ‘stratified’ period. While copepod δ15N and ∆15N values were higher during the mixed period, seston δ15N values did not differ between periods. The δ13C values indicated a seasonal difference between a priori-defined groups of oceanic and coastal copepod species. The seasonal variations of both the isotopic niche (Bayesian ellipses) values and Layman metrics in tropical copepods and zooplankton fractions suggested an opportunistic feeding strategy responding to the local coupled physical–biological seasonal processes. During the productive mixed period, the trophic web was more robust and stable, and a wider niche was observed. Contrary to commonly reported responses to environmental conditions, we found a more complex mesozooplankton food web during the productive period and a shorter web during the oligotrophic period, highlighting the importance of researching trophic dynamics in coastal tropical ecosystems.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All stable isotope data analyzed during the current study are available in the PANGAEA repository, https://doi.org/10.1594/PANGAEA.902824
References
Abrantes KG, Barnett A, Bouillon S (2014) Stable isotope-based community metrics as a tool to identify patterns in food web structure in east African estuaries. Funct Ecol 28:270–282. https://doi.org/10.1111/1365-2435.12155
Ambriz-Arreola I, Gómez-Gutiérrez J, Franco-Gordo MC, Lavaniegos BE, Godínez-Domínguez E (2012) Influence of coastal upwelling–downwelling variability on tropical euphausiid abundance and community structure in the inshore Mexican central Pacific. Mar Ecol Prog Ser 451(119):136. https://doi.org/10.3354/meps09607
Ambriz-Arreola I, Gómez-Gutiérrez J, Franco-Gordo MC, Plascencia-Palomera V, Gasca R, Kozak ER, Lavaniegos BE (2018) Seasonal succession of tropical community structure, abundance, and biomass of five zooplankton taxa in the central Mexican Pacific. Cont Shelf Res 168:54–67. https://doi.org/10.1016/j.csr.2018.08.007
Armengol L, Calbet A, Franchy G, Rodríguez-Santos A, Hernández-León S (2019) Planktonic food web structure and trophic transfer efficiency along a productivity gradient in the tropical and subtropical Atlantic Ocean. Sci Rep 9:2044. https://doi.org/10.1038/s41598-019-38507-9
Azam F, Fenchel T, Field JG, Grey JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263
Barton MB, Litvin SY, Vollenweider JJ, Heintz RA, Norcross BL, Boswell KM (2019) Implications of trophic discrimination factor selection for stable isotope food web models of low trophic levels in the Arctic nearshore. Mar Ecol Prog Ser 613:211–216. https://doi.org/10.3354/meps12893
Bearhop S, Adams CE, Waldron S (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012. https://doi.org/10.1111/j.0021-8790.2004.00861.x
Beers JR (1976) Volumetric methods. Zooplankton fixation and preservation. Monogr Oceanogr Methodol 4:56–60
Bode A, Alvarez-Ossorio MT (2004) Taxonomic versus trophic structure of mesozooplankton: a seasonal study of species succession and stable carbon and nitrogen isotopes in a coastal upwelling ecosystem. ICES J Mar Sci 61:563–571. https://doi.org/10.1016/j.icesjms.2004.03.004
Brun P, Vogt M, Payne MR, Gruber N, O'brien CJ, Buitenhuis ET, Le Quéré C, Leblanc K, Luo YW (2015) Ecological niches of open ocean phytoplankton taxa. Limnol Oceanogr 60(3):1020–1038. https://doi.org/10.1002/lno.10074
Brun PG, Payne MR, Kiørboe T (2017) A trait database for marine copepods. Earth Syst Sci Dat 9:1–33. https://doi.org/10.5194/essd-9-99-2017
Calbet A, Landry MR (2004) Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol Oceanogr 49(1):51–57. https://doi.org/10.4319/lo.2004.49.1.0051
Chen M, Kim D, Liu H, Kang CK (2018) Variability in copepod trophic levels and feeding selectivity based on stable isotope analysis in Gwangyang Bay of the southern coast of the Korean Peninsula. Biogeosciences 15:2055–2073. https://doi.org/10.5194/bg-15-2055-2018
Driscoll ZG, Bootsma HA, Christiansen E (2015) Zooplankton trophic structure in Lake Michigan as revealed by stable carbon and nitrogen isotopes. J Great Lakes Res 41(3):104–114. https://doi.org/10.1016/j.jglr.2015.04.012
Fileman E, Smith T, Harris R (2007) Grazing by Calanus helgolandicus and Para-Pseudocalanus spp. on phytoplankton and protozooplankton during the spring bloom in the Celtic Sea. J Exp Mar Biol Ecol 348:70–84. https://doi.org/10.1016/j.jembe.2007.04.003
Franco-Gordo C, Ambriz-Arreola I, Kozak ER, Gómez-Gutiérrez J, Plascencia-Palomera V, Godínez-Domínguez E, Hinojosa-Larios A (2015) Seasonal succession of zooplankton taxonomic group assemblages in surface waters of Bahía de Navidad, Mexico (November 2010–December 2011). Hidrobiologica 25(3):335–345
Gasca R, Franco-Gordo C, Godínez-Domínguez E, Suárez-Morales E (2012) Hyperiid amphipod community in the Eastern Tropical Pacific before, during, and after El Niño 1997–1998. Mar Ecol Prog Ser 455:123–139. https://doi.org/10.3354/meps09571
Giering SLC, Wells SR, Mayers KMJ, Schuster H, Cornwell L, Fileman ES, Atkinson A, Cook KB, Preece C, Mayor DJ (2018) Seasonal variation of zooplankton community structure and trophic position in the Celtic Sea: a stable isotope and biovolume spectrum approach. Prog Oceanogr. https://doi.org/10.1016/j.pocean.2018.03.012(in press)
Godínez VM, Beier E, Lavín MF, Kurczyn JA (2010) Circulation at the entrance of the Gulf of California from satellite altimeter and hydrographic observations. J Geophys Res Oceans. https://doi.org/10.1029/2009JC005705
Gómez-Valdivia F, Parés-Sierra A, Flores-Morales AL (2015) The Mexican Coastal Current: a subsurface seasonal bridge that connects the tropical and subtropical Northeastern Pacific. Cont Shelf Res 110:100–107. https://doi.org/10.1016/j.csr.2015.10.010
Irigoien X, Head RN, Harris RP, Cummings D, Harbour D, Meyer-Harms B (2000) Feeding selectivity and egg production of Calanus helgolandicus in the English Channel. Limnol Oceanogr 45:44–54. https://doi.org/10.4319/lo.2000.45.1.0044
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 Animal Ecol 80:595–602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
Keister JE, Peterson WT, Pierce SD (2009) Zooplankton distribution and cross-shelf transfer of carbon in an area of complex mesoscale circulation in the northern California Current. Deep Sea Res Part 1 Oceanogr Res Pap 56(2):212–231. https://doi.org/10.1016/j.dsr.2008.09.004
Kleppel GS (1993) On the diets of calanoid copepods. Mar Ecol Prog Ser 99:183–195. https://doi.org/10.3354/meps099183
Kozak ER, Franco-Gordo C, Suárez-Morales E, Palomares-García R (2014) Seasonal and interannual variability of the calanoid copepod community structure in shelf waters of the Eastern Tropical Pacific. Mar Ecol Prog Ser 507:95–110. https://doi.org/10.3354/meps10811
Kozak ER, Franco-Gordo C, Palomares-García R, Gómez-Gutiérrez J, Suárez-Morales E (2017) Annual egg production rates of calanoid copepod species on the continental shelf of the Eastern Tropical Pacific off Mexico. Estuar Coast Shelf Sci 184:138–150. https://doi.org/10.1016/j.ecss.2016.11.012
Kurczyn JA, Beier E, Lavín MF, Chaigneau A (2012) Mesoscale eddies in the northeastern Pacific tropical-subtropical transition zone: Statistical characterization from satellite altimetry. J Geophys Res Oceans. https://doi.org/10.1029/2012JC007970
Kürten B, Painting SJ, Struck U, Polunin NV, Middelburg JJ (2013) Tracking seasonal changes in North Sea zooplankton trophic dynamics using stable isotopes. Biogeochemistry 113(1–3):167–187. https://doi.org/10.1007/s10533-011-9630-y
Landry MR (1981) Switching between herbivory and carnivory by the planktonic marine copepod Calanus pacificus. Mar Biol 65(1):77–82. https://doi.org/10.1007/BF00397070
Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88(1):42–48. https://doi.org/10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2
López-Ibarra GA, Bode A, Hernández-Trujillo S, Zetina-Rejón MJ, Arreguín-Sánchez F (2018) Trophic position of twelve dominant pelagic copepods in the eastern tropical Pacific Ocean. J Mar Syst 187:13–22. https://doi.org/10.1016/j.jmarsys.2018.06.009
Meunier CL, Boersma M, Wiltshire KH, Malzahn AM (2016) Zooplankton eat what they need: copepod selective feeding and potential consequences for marine systems. Oikos 125(1):50–58. https://doi.org/10.1111/oik.02072
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140. https://doi.org/10.1016/0016-7037(84)90204-7
Nielsen JM, Winder M (2015) Seasonal dynamics of zooplankton resource use revealed by carbon amino acid stable isotope values. Mar Ecol Prog Ser 1:143–154. https://doi.org/10.3354/meps11319
Paffenhöfer GA (1988) Feeding rates and behavior of zooplankton. Bull Mar Sci 43(3):430–445
Pelayo-Martínez G, Olivos-Ortiz A, Franco-Gordo C, Quijano-Scheggia S, Gaviño-Rodríguez J, Kono-Martínez T, Castro-Ochoa F (2017) Physical, chemical and zooplankton biomass variability (inshore-offshore) of Mexican Central Pacific during El Niño-La Niña 2010. Lat Am J Aquat Res 45(1):67–78. https://doi.org/10.3856/vol45-issue1-fulltext-7
Portela E, Beier E, Barton ED, Castro R, Godínez V, Palacios-Hernández E, Fiedler PC, Sánchez-Velasco L, Trasviña A (2016) Water masses and circulation in the tropical Pacific off central Mexico and surrounding areas. J Phys Oceanogr 46(10):3069–3081. https://doi.org/10.1175/JPO-D-16-0068.1
Protopapa M, Koppelmann R, Zervoudaki S, Wunsch C, Peters J, Parinos C, Paraschos F, Gogou A, Möllmann C (2019) Trophic positioning of prominent copepods in the epi- and mesopelagic zone of the ultra-oligotrophic eastern Mediterranean Sea. Deep Sea Res Part II Top Stud Oceanogr 164:144–155. https://doi.org/10.1016/j.dsr2.2019.04.011
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Rosende-Pereiro A, Flores-Ortega JR, González-Sansón G, Corgos A (2019) Stomach content and stable isotopes reveal an ontogenetic dietary shift of young-of-the-year scalloped hammerhead sharks (Sphyrna lewini) inhabiting coastal nursery areas. Environ Biol Fishes. https://doi.org/10.1007/s10641-019-00932-0
Schoo KL, Boersma M, Malzahn AM, Löder M, Wiltshire KH, Aberle N (2018) Dietary and seasonal variability in trophic relations at the base of the North Sea pelagic food web revealed by stable isotope and fatty acid analysis. J Sea Res 141:61–70. https://doi.org/10.1016/j.seares.2018.08.004
Shinada A, Ban S, Yamada Y, Ikeda T (2005) Seasonal variations of plankton food web structure in the coastal water off Usujiri southwestern Hokkaido Japan. J Oceanogr 61(4):645–654. https://doi.org/10.1007/s10872-005-0072-9
Sprules WG, Bowerman JE (1988) Omnivory and food chain length in zooplankton food webs. Ecology 69(2):418–426. https://doi.org/10.2307/1940440
St John MA, Clemmesen C, Lund T, Köster T (2001) Diatom production in the marine environment: implications for larval fish growth and condition. ICES J Mar Sci 58(5):1106–1113. https://doi.org/10.1006/jmsc.2001.1089
Stoecker D, Pierson J (2019) Predation on protozoa: its importance to zooplankton revisited. J Plankton Res 41(4):367–373. https://doi.org/10.1093/plankt/fbz027
Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis, Bulletin 167, 2nd edn. Fisheries Research Board of Canada, Ottawa
Suárez-Morales E, Franco-Gordo C, Saucedo-Lozano M (2000) On the pelagic copepod community of the central Mexican tropical Pacific (Autumn, 1990). Crustaceana 73(6):751–762. https://doi.org/10.1163/156854000504778
Torres-Orozco E, Trasviña A, Muhlia-Melo A, Ortega-García S (2005) Mesoscale dynamics and yellowfin tuna catches in the Mexican Pacific. Cienc Mar 31(4):671–683. https://doi.org/10.7773/cm.v31i4.33
Trochine C, Villanueva VD, Balseiro E, Modenutti B (2019) Nutritional stress by means of high C:N ratios in the diet and starvation affects nitrogen isotope ratios and trophic fractionation of omnivorous copepods. Oecologia 190(3):547–557. https://doi.org/10.1007/s00442-019-04438-5
Turner JT (2004) The importance of small planktonic copepods and their roles in pelagic marine food webs. Zool stud 43(2):255–266
Verity PG, Smetacek V (1996) Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar Ecol Prog Ser 130:277–293. https://doi.org/10.3354/meps130277
Zamudio L, Hurlburt HE, Metzger EJ, Tilburg CE (2007) Tropical wave-induced oceanic eddies at Cabo Corrientes and the Maria Islands Mexico. J Geophys Res Oceans 1:112. https://doi.org/10.1029/2006JC004018(C5)
Zhou L, Huang L, Tan Y, Lian X, Li K (2015) Size-based analysis of a zooplankton community under the influence of the Pearl River plume and coastal upwelling in the northeastern South China Sea. Mar Biol Res 11:168–179. https://doi.org/10.1080/17451000.2014.904882
Zhou M, Tande KS, Zhu Y, Basedow S (2009) Productivity, trophic levels and size spectra of zooplankton in northern Norwegian shelf regions. Deep Sea Res Part II Top Stud Oceanogr 56:1934–1944. https://doi.org/10.1016/j.dsr2.2008.11.018
Acknowledgements
We thank crewmember A. Alvizar-Martínez for navigating the panga “Leon Marino” and his assistance with zooplankton sampling. Thanks to the reviewers who improved an earlier version of this manuscript. This project was funded by research grants from the Universidad de Guadalajara. The first author was granted a PhD scholarship (CONACyT 33487/229202). All authors are SNI fellows.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors declare that they have no conflict of interest.
Human and animal rights statement
This article does not contain any studies with human participants; sampling, care and experimental use of animals followed national guidelines.
Additional information
Responsible Editor: N. Aberle-Malzahn.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by Undisclosed experts.
Rights and permissions
About this article
Cite this article
Kozak, E.R., Franco-Gordo, C., Godínez-Domínguez, E. et al. Seasonal variability of stable isotope values and niche size in tropical calanoid copepods and zooplankton size fractions. Mar Biol 167, 37 (2020). https://doi.org/10.1007/s00227-020-3653-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-020-3653-7