Appraisal of Warm-Temperate South African Mangrove Estuaries as Habitats to Enhance Larval Nutritional Condition and Growth of Gilchristella aestuaria (Family Clupeidae) Using RNA:DNA Ratios
Estuaries are highly dynamic systems that serve as nursery areas to fishes and are likely to vary in nursery function, mostly due to habitat quality and food availability. Mangroves are thought to be good nurseries as they enhance food availability and protection, improving growth and survival of juvenile fishes. Food quantity and quality may be reflected in nutritional condition, which may in turn be a useful proxy for growth and survival of larval fishes. This study compared the nutritional condition and growth rate of 793 late stage larvae of estuarine roundherring, Gilchristella aestuaria, by using RNA:DNA indices to indirectly compare the feeding environment among similar warm-temperate mangrove and non-mangrove estuaries in South Africa during January 2015 and 2016. Results indicated that G. aestuaria larvae had differing nutritional conditions within the sampling years and within the estuaries. The standardised RNA:DNA (sRD) as well as the RNA residual index values were higher within mangrove estuaries only in 2016. The instantaneous growth rates (Gi) of larvae in mangrove and non-mangrove estuaries were similar; however, post-flexion larvae were found to have a higher Gi and sRD in mangrove estuaries. Turbidity was the major factor influencing the nutritional condition of G. aestuaria larvae. Mangroves have been found to act as sediment sinks and thus may provide advantages that increase feeding success for post-flexion larvae; however, more is yet to be understood in terms of feeding environment dynamics and how habitat quality influences the survival of larval fishes.
KeywordsNursery habitats Mangroves Fish feeding environments RNA:DNA Nutritional condition Estuarine roundherring Fish larvae
We thank Helmholtz Centre for Ocean Research (GEOMAR) for laboratory assistance supported by the EU project BIOC3. We also thank the South African Weather Service for providing rainfall data.
Funding was provided by the National Research Foundation of South Africa under grant number 93570.
Compliance with Ethical Standards
Conflict of Interest
The co-author, Nadine A. Strydom, is the M.Sc. supervisor of the first author and is an associate editor of Estuaries and Coasts. The authors declare that there are no other conflicts of interest.
Fishes were treated in accordance with Nelson Mandela University ethics, under ethics clearance number A15-SCI-ZOO-002.
- Beck, Michael W., Kenneth L. Heck, Kenneth W. Able, Daniel L. Childers, David B. Eggleston, Bronwyn M. Gillanders, Benjamin Halpern, et al. 2001. The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bioscience 51 (8): 633. https://doi.org/10.1641/0006-3568(2001)051[0633:TICAMO]2.0.CO;2.Google Scholar
- Blaber, Stephen J.M. 2007. Mangroves and fishes: Issues of diversity, dependence, and dogma. Bulletin of Marine Science 80: 457–472.Google Scholar
- Blaber, Stephen J.M., Digby P. Cyrus, and Alan K. Whitfield. 1981. The influence of zooplankton food resources on the morphology of the estuarine clupeid Gilchristella aestuarius (Gilchrist, 1914). Environmental Biology of Fishes 6 (3-4): 351–355. https://doi.org/10.1007/BF00005764.CrossRefGoogle Scholar
- Buckley, Lawrence J., Elaine M. Caldarone, and Catriona Clemmesen. 2008. Multi-species larval fish growth model based on temperature and fluorometrically derived RNA/DNA ratios: Results from a meta-analysis. Marine Ecology Progress Series 371: 221–232. https://doi.org/10.3354/meps07648.CrossRefGoogle Scholar
- Caldarone, Elaine M., Melissa Wagner, Jeanne St Onge-Burns, and Lawrence J. Buckley. 2001. Protocol and guide for estimating nucleic acids in larval fish using a fluorescence microplate reader. Northeast Fisheries Science Center Reference Document 01–11: 22.Google Scholar
- Caldarone, Elaine M., Catriona Clemmesen, Elisa Berdalet, Thomas J. Miller, Arild Folkvord, Gloria J. Holt, Pilar M. Olivar, and Iain M. Suthers. 2006. Intercalibration of four spectrofluorometric protocols for measuring RNA/DNA ratios in larval and juvenile fish. Limnology and Oceanography: Methods 4 (5): 153–163. https://doi.org/10.4319/lom.2006.4.153.CrossRefGoogle Scholar
- Chícharo, Maria A., Luis Chícharo, Luis Valdés, Eduardo Lópes-Jamar, and Pedro Ré. 1998. Estimation of starvation and diel variation of the RNA/DNA ratios in field-caught Sardina pilchardus larvae off the north of Spain. Marine Ecology Progress Series 164: 273–283. https://doi.org/10.3354/meps164273.CrossRefGoogle Scholar
- Chícharo, Maria A., Ana Amaral, Ana Faria, Pedro Morais, Carlos Mendes, David Piló, Radhouan Ben-Hamadou, and Luis Chícharo. 2012. Are tidal lagoons ecologically relevant to larval recruitment of small pelagic fish? An approach using nutritional condition and growth rate. Estuarine, Coastal and Shelf Science 112: 265–279. https://doi.org/10.1016/j.ecss.2012.07.033.CrossRefGoogle Scholar
- Clemmesen, Catriona. 1996. Importance and limits of RNA/DNA ratios as a measure of nutritional condition in fish larvae. In Survival strategies in early life stages of marine resources, ed. Y. Watanabe, 67–82. Rotterdam: A.A. Balkema.Google Scholar
- Costalago, David, Nadine A. Strydom, Carminita Frost, and Catriona Clemmesen. 2015. Preliminary insight into the relationship between environmental factors and the nutritional condition and growth of Gilchristella aestuaria larvae in the upper reaches of South African estuaries. Environmental Biology of Fishes 98 (12): 2367–2378. https://doi.org/10.1007/s10641-015-0447-8.CrossRefGoogle Scholar
- Dahlgren, Craig P., G. Todd Kellison, Aaron J. Adams, Bronwyn M. Gillanders, Matthew S. Kendall, Craig A. Layman, Janet A. Ley, Ivan Nagelkerken, and Joseph E. Serafy. 2006. Marine nurseries and effective juvenile habitats: Concepts and applications. Marine Ecology Progress Series 312: 291–295. https://doi.org/10.3354/meps312291.CrossRefGoogle Scholar
- Emmerson, Winston David. 1992. Feeding and assimilation of mangrove leaves by the crab Sesarma meinerti de Man in relation to leaf-litter production in Mgazana, a warm-temperate southern African mangrove swamp. Journal of Experimental Marine Biology and Ecology 157 (1): 41–53. https://doi.org/10.1016/0022-0981(92)90073-J.CrossRefGoogle Scholar
- MacArthur, Robert H. 1965. Patterns of species diversity. Biological Reviews 40 (4): 510–533. https://doi.org/10.1111/j.1469-185X.1965.tb00815.x.CrossRefGoogle Scholar
- Mazumder, Debashish, Neil Saintilan, Robert J. Williams, and Ron Szymczak. 2011. Trophic importance of a temperate intertidal wetland to resident and itinerant taxa: Evidence from multiple stable isotope analyses. Marine and Freshwater Research 62 (1): 11–19. https://doi.org/10.1071/MF10076.CrossRefGoogle Scholar
- Mbande, Sekiwe M., Alan K. Whitfield, and Paul D. Cowley. 2005. The ichthyofaunal composition of the Mngazi and Mngazana estuaries: A comparative study. Smithiana: 1–56.Google Scholar
- Nagelkerken, Ivan, A.M. De Schryver, Marieke C. Verweij, Farid Dahdouh-Guebas, Gerard van der Velde, and Nico Koedam. 2010. Differences in root architecture influence attraction of fishes to mangroves: A field experiment mimicking roots of different length, orientation, and complexity. Journal of Experimental Marine Biology and Ecology 396 (1): 27–34. https://doi.org/10.1016/j.jembe.2010.10.002.CrossRefGoogle Scholar
- Newman, Brent K., and R. John Watling. 2007. Definition of baseline metal concentrations for assessing metal enrichment of sediment from the south-eastern Cape coastline of South Africa. Water SA 33: 675–691.Google Scholar
- O’Brien, W. John. 1979. The predator-prey interactions of planktivorous fish and zooplankton. American Scientist 67: 572–581.Google Scholar
- Paterson, Angus W., and Alan K. Whitfield. 1997. A stable carbon isotope study of the food-web in a freshwater-deprived South African estuary, with particular emphasis on the ichthyofauna. Estuarine, Coastal and Shelf Science 45 (6): 705–715. https://doi.org/10.1006/ecss.1997.0243.CrossRefGoogle Scholar
- Pepin, Pierre, and Randy W. Penney. 1997. Patterns of prey size and taxonomic composition in larval fish: Are there general size-dependent models? Journal of Fish Biology 51 (sa): 84–100. https://doi.org/10.1111/j.1095-8649.1997.tb06094.x.CrossRefGoogle Scholar
- Reddering, Johan S.V., and Kevin Esterhuysen. 1987. The effects of river floods on sediment dispersal in small estuaries; a case study from East London. South African Journal of Geology 90: 458–470.Google Scholar
- Rönnbäck, Patrik, Max Troell, Nils Kautsky, and Jurgenne H. Primavera. 1999. Distribution pattern of shrimps and fish among Avicennia and Rhizophora microhabitats in the Pagbilao Mangroves, Philippines. Estuarine, Coastal and Shelf Science 48 (2): 223–234. https://doi.org/10.1006/ecss.1998.0415.CrossRefGoogle Scholar
- Silva, Ivan A.L., Ana Faria, Maria A. Teodósio, and Susana Garrido. 2014. Ontogeny of swimming behaviour in sardine Sardina pilchardus larvae and effect of larval nutritional condition on critical speed. Marine Ecology Progress Series 504: 287–300. https://doi.org/10.3354/meps10758.CrossRefGoogle Scholar
- Steinke, Trevor D. 1972. Further observations on the distribution of mangroves in the Eastern Cape Province. Journal of South African Botany 38: 165–178.Google Scholar
- Steinke, Trevor D. 1986. Mangroves of the East London area. The Naturalist 30: 50–53.Google Scholar
- Strydom, Nadine A., and Alan K. Whitfield. 2000. The effects of a single freshwater release into the Kromme Estuary. 4: Larval fish response. Water SA 26: 319–328.Google Scholar
- Strydom, Nadine A., Alan K. Whitfield, and Angus W. Paterson. 2002. Influence of altered freshwater flow regimes on abundance of larval and juvenile Gilchristella aestuaria (Pisces: Clupeidae) in the upper reaches of two South African estuaries. Marine and Freshwater Research 53 (2): 431–438. https://doi.org/10.1071/MF01077.CrossRefGoogle Scholar
- Talbot, Mark, Eugene B. Branch, Stephen A. Marsland, and R. John Watling. 1985. Metal surveys in South African estuaries X. Blind, Ihlanza, Nahoon and Quinera Rivers. Water SA 11: 65–68.Google Scholar
- Teodósio, Maria A., Claire B. Paris, Eric Wolanski, and Pedro Morais. 2016. Biophysical processes leading to the ingress of temperate fish larvae into estuarine nursery areas: A review. Estuarine, Coastal and Shelf Science 183: 187–202. https://doi.org/10.1016/j.ecss.2016.10.022.CrossRefGoogle Scholar
- Teodósio, Maria A., Susana Garrido, Janna Peters, Francisco Leitão, Ré Pedro, Álvaro J. Peliz, and A. Miguel P. Santos. 2017. Assessing the impact of environmental forcing on the condition of anchovy larvae in the Cadiz Gulf using nucleic acid and fatty acid-derived indices. Estuarine, Coastal and Shelf Science 185: 94–106. https://doi.org/10.1016/j.ecss.2016.10.023.CrossRefGoogle Scholar
- van Niekerk, Lara, and Jane Turpie. 2012. Technical report, volume 3: estuary component. South African National Biodiversity Assessment 2011. Vol. 3. Stellenbosch.Google Scholar
- Vasconcelos, Rita P., Patrick Reis-Santos, Maria J. Costa, and Henrique N. Cabral. 2011. Connectivity between estuaries and marine environment: Integrating metrics to assess estuarine nursery function. Ecological Indicators 11 (5): 1123–1133. https://doi.org/10.1016/j.ecolind.2010.12.012.CrossRefGoogle Scholar