Skip to main content

Advertisement

SpringerLink
Log in

Low-pH Freshwater Discharges Drive Spatial and Temporal Variations in Life History Traits of Neritic Copepod Acartia tonsa

  • Note
  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Land weathering by river runoff makes coastal oceans highly variable ecosystems in terms of seawater pH; however, its effects on biological components and, hence, on the coastal ecosystem functioning has been scarcely addressed. In this study, we determined part of the spatial and seasonal variability of the physical–chemical characteristics of seawater, and life history traits of the neritic copepod Acartia tonsa, along an estuarine-to-coastal zone geographic gradient in the southern Pacific Ocean. There, freshwater influences give rise to sharp gradients in pH, salinity, and temperature, which in turn, may affect the fitness of copepod populations inhabiting along the gradient. In fact, most of the studied copepod traits (egg size, ingestion, and egg production rates) were moderately (r 2 = 0.5, p < 0.05) to robustly (r 2 = 0.9, p < 0.05) explained by physical–chemical and biological (food abundance and composition) factors. Noteworthy was the negative relationship between low-pH waters and copepod reproductive outcomes. This effect was far evident in the estuarine area where small brood sizes and depleted egg production rates were significantly correlated with low seawater pH (r 2 = 0.6, p < 0.05). If short-term episodes of low-pH seawater constitute a significant threshold for reproduction, current findings should stimulate a better description of pH variability in coastal zones, as well as the study of biological consequences derived from the interaction between pH and others drivers on coastal marine populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Aguilera, V.A., K. Donoso, and R. Escribano. 2011. Reproductive performance of small-sized dominant copepods with a highly variable food resource in the coastal upwelling system off the Chilean Humboldt Current. Marine Biology Research 7: 1–15.

    Article  Google Scholar 

  • Attrill, M.J. 2002. A testable linear model for diversity trends in estuaries. Journal of Animal Ecology 71: 262–269.

    Article  Google Scholar 

  • Ban, S. 1994. Effect of temperature and food concentration on postembryonic development, egg production and adult body size of calanoid copepod Eurytemora affinis. Journal of Plankton Research 16: 721–735.

    Article  Google Scholar 

  • Barker, D.E., and D.K. Cone. 2000. Occurrence of Ergasilus celestis (Copepoda) and Pseudodactylogryrus anguillae (Monogenea) among wild eels (Anguilla rostrata) in relation to stream flow, pH and temperature and recommendations for controlling their transmission among captive eels. Aquaculture 187: 261–274.

    Article  Google Scholar 

  • Bell, G., and S. Collins. 2008. Adaptation, extinction and global change. Evolutionary Applications 1: 3–16.

    Article  Google Scholar 

  • Borsheim, K. Y., and G. Bratbak. 1987. Cell volume to cell carbon conversion factors for a bacterivorous Monas sp. enriched from seawater. Marine Ecology Progress Series 36:171–175.

    Article  Google Scholar 

  • Cailleaud, K., G. Maillet, H. Budzinski, S. Souissi, and J. Forget-Leray. 2007. Effects of salinity and temperature on the expression of enzymatic biomarkers in Eurytemora affinis (Calanoida, Copepoda). Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 147: 841–849.

    Article  CAS  Google Scholar 

  • Castro-Longoria, E. 1998. Seasonal and spatial distribution patterns of the congeneric group Acartia in the Solent–Southampton Water estuarine system, with special reference to aspects of their fecundity. Ph.D. thesis, University of Southampton, Southampton

  • Cervetto, G., R. Gaudy, and M. Pagano. 1999. Influence of salinity on the distribution of Acartia tonsa (Copepoda, Calanoida). Journal of Experimental Marine Biology and Ecology 239: 33–45.

    Article  Google Scholar 

  • Chinnery, F.E., and J.A. Williams. 2004. The influence of temperature and salinity on Acartia (Copepoda: Calanoida) nauplii survival. Marine Biology 145: 733–738.

    Google Scholar 

  • Chrzanowski, T.H., and K. Simek. 1990. Prey-size selection by freshwater flagellated protozoa. Limnology and Oceanography 35: 1429–1436.

    Article  Google Scholar 

  • Conover, R.J. 1956. Oceanography of Long Island Sound, 1952–1954. VI. Biology of Acartia clausi and A. tonsa. Bulletin of the Bingham Oceanographic Collection 15: 156–233.

    Google Scholar 

  • Cowell, B.C. 1967. The Copepoda and Cladocera of a Missouri River reservoir: a comparison of sampling in the reservoir and the discharge. Limnology and Oceanography 12: 125–136.

    Article  Google Scholar 

  • Devreker, D., S. Souissi, and L. Seuront. 2004. Development and mortality of the first naupliar stages of Eurytemora affinis (Copepoda, Calanoida) under different conditions of salinity and temperature. Journal of Experimental Marine Biology and Ecology 303: 31–46.

    Article  Google Scholar 

  • Devreker, D., S. Souissi, G. Winkler, J. Forget-Leray, and F. Leboulenger. 2009. Effects of salinity, temperature and individual variability on the reproduction of Eurytemora affinis (Copepoda; Calanoida) from the Seine estuary: A laboratory study. Journal of Experimental Marine Biology and Ecology 368: 113–123.

    Article  Google Scholar 

  • Dickinson, G.G., A.V. Ivanina, O.B. Matoo, H.O. Pörtner, G. Lannig, C. Bock, E. Beniash, and I.M. Sokolova. 2012. Interactive effects of salinity and elevated CO2 levels on juvenile eastern oysters, Crassostrea virginica. Journal of Experimental Biology 215: 29–43.

    Article  CAS  Google Scholar 

  • DOE. 1994. Handbook of methods for analysis of the various parameters of the carbon dioxide system in sea water, ed. A.G. Dickson and C. Goyet. ORNL/CDIAC-74.

  • Dupont. S., and M.C. Thorndyke. 2008. Ocean acidification and its impact on the early life-history stages of marine animals. Commission Internationale pour l'Exploration Scientifique de la Mer Mediterranee-CIESM, Monaco. In CIESM Workshop Monographs (No. 36), ed. F. Briand. CIESM, Monaco.

  • Edler, L. 1979. Recommendations for marine biological studies in the Baltic Sea. The Baltic Marine Biologist Publications 5: 1–38.

    Google Scholar 

  • Escribano, R., P. Hidalgo, M. Fuentes, and K. Donoso. 2012. Zooplankton time series in the coastal zone off Chile: Variation in upwelling and responses of the copepod community. Progress in Oceanography 97–100: 174–186.

    Article  Google Scholar 

  • FIP 2002. Determinación de la capacidad de carga de las zonas estuarinas de los ríos Valdivia y Bueno, X Región. Instituto de Investigación Pesquera Proyecto FIP 2000-29. 191 pp.

  • Fischlin, A., G.F. Midgley, J. Price, R. Leemans, B. Gopal, C. Turley, M. Rounsevell, P. Dube, J. Tarazona, and A. Velichko. 2007. Ecosystems, their properties, goods, and services. Climate Change 2007: Impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, ed. M.L. Parry et al., 211–272. Cambridge: Cambridge University Press UK

  • Forget, J., B. Beliaeff, and G. Bocquene. 2003. Acetylcholinesterase activity in copepods (Tigriopus brevicornis) from the Vilaine River estuary, France, as a biomarker of neurotoxic contaminants. Aquatic Toxicology 62: 195–204.

    Article  CAS  Google Scholar 

  • Frost, B.W. 1972. Effect of size and concentration of food particles on the feeding behaviour of the marine planktonic copepod Calanus pacificus. Limnology and Oceanography 17: 805–815.

    Article  Google Scholar 

  • Gaudy, R., G. Cervetto, and M. Pagano. 2000. Comparison of the metabolism of Acartia clausi and A. tonsa: influence of temperature and salinity. Journal of Experimental Marine Biology and Ecology 247: 51–65.

    Article  CAS  Google Scholar 

  • Gienapp, P., C. Teplitsky, J.S. Alho, J.A. Mills, and J. Merila. 2008. Climate change and evolution: Disentangling environmental and genetic responses. Molecular Ecology 17: 167–178.

    Article  CAS  Google Scholar 

  • Gyllenberg, G., and G. Lundqvist. 1979. The effects of temperature and salinity on the oxygen consumption of Eurytemora hirundoides (Crustacea, Copepoda). Annales Zoologici Fennici 16: 205–208.

    Google Scholar 

  • Haas, L.W. 1982. Improved epifluorescence microscopy for observing planktonic microorganisms. Annales De L Institut Oceanographique 58: 261–266.

    Google Scholar 

  • Hand, S.C. 1991. Metabolic dormancy in aquatic invertebrates. In Advances in comparative and environmental physiology, ed. R. Gilles, 1–50. Heidelberg: Springer.

    Chapter  Google Scholar 

  • Hidalgo, P., R. Escribano, M. Fuentes, E. Jorquera, and O. Vergara. 2011. How coastal upwelling influences spatial patterns of size-structured diversity of copepods off central-southern Chile (summer 2009). Progress in Oceanography 92–95: 134–145.

    Google Scholar 

  • Hochachka, P.W., and G.N. Somero. 2002. Biochemical adaptation: Mechanism and process in physiological evolution. Oxford: Oxford University Press. 446 pp.

    Google Scholar 

  • Hodgkin, E.P., and R.J. Rippingale. 1971. Interspecies conflict in estuarine copepods. Limnology and Oceanography 16: 573–576.

    Article  Google Scholar 

  • Hoffman, G.E., J.E. Smith, K.S. Johnson, U. Send, L.A. Levin, F. Micheli, A. Paytan, N.N. Price, B. Peterson, Y. Takeshita, P.G. Matson, E. Derse Crook, K.J. Kroeker, M.C. Gambi, E.B. Rivest, C.A. Frieder, P.C. Yu, and T.R. Martz. 2011. High-frequency dynamics of ocean pH: A multi-ecosystem comparison. PLoS One 6: e28983. doi:10.1371/journal.pone.0028983.

    Article  Google Scholar 

  • Huntley, M.E., and M.D. Lopez. 1992. Temperature-dependent production of marine copepods: A global synthesis. American Naturalist 140: 201–242.

    Article  CAS  Google Scholar 

  • Invidia, M., S. Sei, and G. Gorbi. 2004. Survival of the copepod Acartia tonsa following egg exposure to near anoxia and to sulfide at different pH values. Marine Ecology Progress Series 276: 187–196.

    Article  Google Scholar 

  • Kaartvedt, S., and D.L. Aksnes. 1992. Does freshwater discharge cause mortality of fjord living zooplankton? Estuarine, Coastal and Shelf Science 34: 305–313.

    Article  CAS  Google Scholar 

  • Kiørboe, T., and T.G. Nielsen. 1994. Regulation of zooplankton biomass and production in a temperate, coastal ecosystem. 1. Copepods. Limnology and Oceanography 39: 493–507.

  • Kiørboe, T. 2011. What makes pelagic copepods so successful? Journal of Plankton Research 33: 677–685.

    Google Scholar 

  • Kimmel, D. G., and B.P. Bradley. 2001. Specific protein responses in the calanoid copepod Eurytemora affinis (Poppe, 1880) to salinity and temperature variation. Journal of Experimental Marine Biology and Ecology 266: 135–149.

    Google Scholar 

  • Kinne, O. 1964. Salinity and temperature combinations. Oceanography and Marine Biology: An Annual Review 2: 281–339.

    Google Scholar 

  • Knutzen, J. 1981. Effects of decreased pH on marine organisms. Marine Pollution Bulletin 12: 25–29.

    Article  CAS  Google Scholar 

  • Kurihara, H., and A. Ishimatsu. 2008. Effects of high CO2 seawater on the copepod (Acartia tsuensis) through all life stages and subsequent generations. Marine Pollution Bulletin 56: 1086–1090.

    Article  CAS  Google Scholar 

  • Kurihara, H., S. Shimode, and Y. Shirayama. 2004a. Sub-lethal effects of elevated concentration of CO2 on planktonic copepods and sea urchins. Journal of Oceanography 60: 743–750.

    Article  CAS  Google Scholar 

  • Kurihara, H., Y. Shirayama, and S. Shimode. 2004b. Effects of raised CO2 concentration on the egg production rate and early development of two species of marine copepods [Acartia steueri and Acartia erythraea]. Marine Pollution Bulletin 49: 721–727.

    Article  CAS  Google Scholar 

  • Lee, H.-W., S. Ban, T. Ikeda, et al. 2003. Effect of temperature on development, growth and reproduction in the marine copepod Pseudocalanus newmani at satiating food condition. Journal of Plankton Research 25: 261–271.

    Article  CAS  Google Scholar 

  • McLaren, I.A. 1966. Predicting development rate of copepod eggs. The Biological Bulletin 131: 457–469.

    Article  Google Scholar 

  • Mauchline, J. 1998. The biology of calanoid copepods. Advances in Marine Biology 33: 1–710.

    Article  Google Scholar 

  • Marín, V., M.E. Huntley, and B. Frost. 1986. Measuring feeding rates of pelagic herbivores: Analysis of experimental design and methods. Marine Biology 93: 49–58.

    Article  Google Scholar 

  • Mayor, D., C. Matthews, K. Cook, A.F. Zuur, and S. Hay. 2007. CO2-induced acidification affects hatching success in Calanus finmarchicus. Marine Ecology Progress Series 350: 91–97.

    Article  Google Scholar 

  • Mayor, D., N.R. Everett, and K.B. Cook. 2012. End of century ocean warming and acidification effects on reproductive success in a temperate marine copepod. Journal of Plankton Research 34: 258–262.

    Article  CAS  Google Scholar 

  • Morales, C.E., M.L. Torreblanca, S. Hormazabal, M. Correa-Ramírez, S. Nuñez, and P. Hidalgo. 2010. Mesoscale structure of copepod assemblages in the coastal transition zone and oceanic waters off central-southern Chile. Progress in Oceanography 84: 158–173.

    Article  Google Scholar 

  • Morgan, I.J., D.G. McDonald, and C.M. Wood. 2001. The cost of living for freshwater fish in a warmer, more polluted world. Global Change Biology 7: 345–355.

    Article  Google Scholar 

  • Orr, J.C., V.J. Fabry, O. Aumont, L. Bopp, S.C. Doney, R.A. Feely, and A. Yool. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681–686.

    Article  CAS  Google Scholar 

  • Pace, M.L., E.G.S. Findlay, and D. Lints. 1992. Zooplankton in advective environments: The Hudson River community and a comparative analysis. Canadian Journal of Fishery and Aquatic Sciences 49: 1060–1069.

    Article  Google Scholar 

  • Pino, M., G.M. Perillo, and P. Santamarina. 1984. Residual fluxes in a cross-section of the Valdivia River Estuary, Chile. Estuarine, Coastal and Shelf Science 38: 491–505.

    Google Scholar 

  • Pörtner, H.O., M. Langenbuch, and A. Reipschläger. 2004. Biological impact of elevated ocean CO2 concentrations: Lessons from animal physiology and earth history. Journal of Oceanography 60: 705–718.

    Article  Google Scholar 

  • Ringwood, A.H., and C.J. Keppler. 2002. Water quality variation and clam growth: Is pH really a non-issue in estuaries? Estuaries and Coasts 25: 901–907.

    Article  Google Scholar 

  • Rivkin, R.B., and L. Legendre. 2001. Biogenic carbon cycling in the upper ocean: Effects of microbial respiration. Science 291: 2398–2400.

    Article  CAS  Google Scholar 

  • Saldías, G., M. Sobarzo, J. Largier, C. Moffat, and R. Letelier. 2012. Seasonal variability of turbid river plumes off central Chile based on high-resolution MODIS imagery. Remote Sensing of Environment 123: 220–233.

    Article  Google Scholar 

  • Seki, H., and J. Fulton. 1969. Infection of marine copepods by Metschnikowia sp. Mycopathologia 38: 61–70.

    CAS  Google Scholar 

  • Smith, C.C., and S.D. Fretwell. 1974. The optimal balance between size and number of offspring. American Naturalist 108: 499–506.

    Article  Google Scholar 

  • Strub, P.T., J.M. Mesias, V. Montecino, J. Rutllant, and S. Salinas. 1998. Coastal ocean circulation off western South America. In In The Global Coastal Ocean—Regional Studies and Synthesis, vol. 11, ed. A.R. Robinson and K.H. Brink, 273–313. New York: Wiley.

    Google Scholar 

  • Tackx, M.D., N. De Pauw, R. Van Mieghem, F. Azémar, A. Hannouti, S. Van Damme, F. Fiers, N. Daro, and P. Meire. 2004. Zooplankton in the Schelde estuary. Belgium and The Netherlands. Spatial and temporal patterns. Journal of Plankton Research 26: 133–141.

    Google Scholar 

  • Tester, P., and T. Turner. 1991. Why is Acartia tonsa restricted to estuarine habitats. In Proc. 4th Int. Conf. on Copepoda, vol. 1 (special issue), Bulletin of Plankton Society of Japan: 603–611.

  • Utermöhl, H. 1958. Zur vervollkommung der quantitativen phyoplankton-methodik. Mitt. Internationale Vereinigung fur Theoretische und Angewandte Limnologie 9: 1–38.

    Google Scholar 

  • Uye, S.-I. 1982. Length–weight relationships of important zooplankton from the Inland Sea of Japan. Journal of the Oceanographical Society of Japan 38: 149–158.

    Article  Google Scholar 

  • Vargas, C.A., S.E. Araneda, and G. Valenzuela. 2003. Influence of tidal phase and circulation on larval fish distribution in a partially mixed estuary, Corral Bay, Chile. Journal of Marine Biology Association U.K. 113: 217–222.

    Google Scholar 

  • Vargas, C.A., and H.E. González. 2004. Plankton community structure and carbon cycling in a coastal upwelling system. I. Diet of copepods and appendicularians. Aquatic Microbiology and Ecology 34: 151–164.

    Article  Google Scholar 

  • Walton, W.E., S.M. Compton, J.D. Allan, and R.E. Daniels. 1982. The effect of acid stress on survivorship and reproduction of Daphnia pulex (Crustacea: Cladocera). Canadian Journal of Zoology 60: 573–579.

    Article  CAS  Google Scholar 

  • Watanabe, Y., A. Yamaguchi, H. Ishida, and T. Harimoto. 2006. Lethality of increasing CO2 levels on deep-sea copepods in the western North Pacific. Journal of Oceanography 62: 185–196.

    Article  Google Scholar 

  • Yamada, Y., and T. Ikeda. 1999. Acute toxicity of lowered pH to some oceanic zooplankton. Plankton Biology and Ecology 46: 62–67.

    Google Scholar 

Download references

Acknowledgments

Authors thank Mauricio Vegas, Elio Quinan, Miguel Barrientos, and Jose Martel for their valuable help during sampling campaigns. Thanks also to Haydee Müller, Karin Acuña, and Loreto Mardones for their logistic support. Special greeting and posthumous thanks to Mr. Leon Matamala (R.I.P.), thanks for your friendship and company. Funding was provided by grants from the Chilean Scientific and Technologic Commission through the postdoctoral FONDECYT Project n° 3110019. Other logistic and financial support for this study was provided by the Proyecto Anillos ACT-132 (http://www.eula.cl/anillos_acidificacion).

Author information

Authors and Affiliations

  1. Aquatic Ecosystem Functioning Lab (LAFE), Environmental Sciences Center EULA-Chile, Universidad de Concepción, PO Box 160-C, Concepción, Chile

    Victor M. Aguilera & Cristian A. Vargas

  2. Instituto de Ciencias Marinas y Limnológicas, Laboratorio Costero de Calfuco, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile

    Patricio H. Manríquez & Jorge M. Navarro

  3. Departamento de Ecología y Biodiversidad, Facultad de Ecología y Recursos Naturales, Universidad Andres Bello, Santiago, Chile

    Cristian Duarte

Authors
  1. Victor M. Aguilera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristian A. Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Patricio H. Manríquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jorge M. Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cristian Duarte
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Victor M. Aguilera.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 382 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aguilera, V.M., Vargas, C.A., Manríquez, P.H. et al. Low-pH Freshwater Discharges Drive Spatial and Temporal Variations in Life History Traits of Neritic Copepod Acartia tonsa . Estuaries and Coasts 36, 1084–1092 (2013). https://doi.org/10.1007/s12237-013-9615-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-013-9615-2

Keywords

Search

Navigation