Population dynamics of resident fish in a coastal lagoon under eutrophication-mediated habitat changes

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Published: Oct 9, 2024
DOI: https://doi.org/10.12681/mms.38054
Keywords:
anthropogenic impacts ecological indicators transitional waters shallow areas Mar Menor
ADRIÁN GUERRERO-GÓMEZ
Department of Zoology and Physical Anthropology¸ Faculty of Biology, University of Murcia, Spain
ANTONIO ZAMORA-LÓPEZ
Department of Zoology and Physical Anthropology¸ Faculty of Biology, University of Murcia, Spain
MAR TORRALVA
Department of Zoology and Physical Anthropology¸ Faculty of Biology, University of Murcia, Spain
JOSÉ MANUEL ZAMORA-MARÍN
Department of Zoology and Physical Anthropology¸, Faculty of Biology, University of Murcia, Spain & Department of Applied Biology, Centro de Investigación e Innovación Agroalimentaria (CIAGRO-UMH), Miguel Hernández University of Elche, Elche, Spain
ANTONIO GUILLÉN-BELTRÁN
Department of Zoology and Physical Anthropology¸ Faculty of Biology, University of Murcia, Spain
FRANCISCO OLIVA-PATERNA J.
Department of Zoology and Physical Anthropology¸ Faculty of Biology, University of Murcia, Spain
Abstract

Coastal lagoons, as transitional ecosystems, are crucial for providing ecosystem services and preserving fish communities, yet they face increasing pressures from anthropogenic activities. The Mar Menor coastal lagoon in the western Mediterranean exemplifies this challenge, as it suffers from severe eutrophication driven by agricultural and urban influences. In this study, we assess changes in the population dynamics of three resident fish species (Apricaphanius iberus, Pomatoschistus marmoratus, and Syngnathus abaster) in the context of human-induced impacts in the Mar Menor. Using long-term monitoring data (the reference period of 2002-2004 vs. the eutrophication period of 2015-2019), we analyze temporal variations in their population dynamics and their relationships with eutrophication-mediated structural changes in shallow waters. Our results suggest that these resident species, which are closely associated with shallow areas, show population dynamics that reflect habitat alterations, underscoring their potential as indicators of eutrophication impacts. This study enhances our understanding of the dynamics within transitional ecosystems and provides a basis for integrated management strategies aimed at promoting effective fish conservation.

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References
Alcaraz, C., Pou-Rovira, Q., García-Berthou, E., 2008. Use of a flooded salt marsh habitat by an endangered cyprinodontid fish (Aphanius iberus). Hydrobiologia, 600, 177-185.
Almeida, D., Cruz, A., Llinares, C., Torralva, M., Lantero, E. et al., 2023. Fish morphological and parasitological traits as ecological indicators of habitat quality in a Mediterranean coastal lagoon. Aquatic Conservation: Marine and Freshwater Ecosystems, 1-16.
Álvarez-Rogel, J., Barberá, G. G., Maxwell, B., Guerrero-Brotons, M., Díaz-García, C. et al., 2020. The case of Mar Menor eutrophication: State of the art and description of tested Nature-Based Solutions. Ecological Engineering, 158, 106086.
Araújo, F.G., Williams, W.P., Bailey, R.G., 2000. Fish assemblages as indicators of water quality in the middle Thames estuary, England (1980-1989). Estuaries, 23, 305-317.
Badosa, A., Boix, D., Brucet, S., López-Flores, R., Quintana, X.D., 2007. Short-term effects of changes in water management on the limnological characteristics and zooplankton of a eutrophic Mediterranean coastal lagoon (NE Iberian Peninsula). Marine Pollution Bulletin, 54, 1273 -1284.
Barton, K., 2015. MuMIn - Model Selection and Model Averaging Based on Information Criteria (AICc and Alike). R package version 1.15.1.
Bates, D., Mächler, M., Bolker, B., Walker, S., 2015. Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software, 67.
Becheker, A., Chaoui, L., Kara, M.H., 2022. The profiles of occupancy by fish fauna of four shallow coastal habitats at a limited regional scale in the south-western Mediterranean. Regional Studies in Marine Science, 51, 102195.
Bernardeau-Esteller, J., Sandoval-Gil, J.M., Belando, M.D., Ramos-Segura, A., García-Muñoz, R. et al., 2023. The Role of Cymodocea nodosa and Caulerpa prolifera Meadows as Nitrogen Sinks in Temperate Coastal Lagoons. Diversity, 15, 1-17.
Branco, P., Costa, J.L., Raposo de Almeida, P., 2008. Conservation Priority Index for Estuarine Fish (COPIEF). Estuarine, Coastal and Shelf Science, 80, 581-588.
Brauko, K.M., Cerveira, A.F., Freitas, R.F., Hadlich, H.L., Beras, T. et al., 2020. Comparing structural and functional approaches to distinguish benthic communities from eutrophic and non-eutrophic estuaries. Marine Pollution Bulletin, 157, 111290.
Burnham, K.P., Anderson, D.R., 2002. Model selection and multimodel inference: A practical information‐theoretic approach. Springer‐Verlag., (Ed.), Berlin.
Caldwell, I.R., Vincent, A.C.J., 2012. A sedentary fish on the move: Effects of displacement on long-snouted seahorse (Hippocampus guttulatus Cuvier) movement and habitat use. Environmental Biology of Fishes, 96, 67-75.
Caro, T.M., O’Doherty, G., 1999. On the use of surrogate species in conservation biology. Conservation Biology, 13, 805-814.
Castro-Fernández, J., Castejón-Silvo, I., Arechavala-López, P., Terrados, J., Morales-Nin, B., 2020. Feeding ecology of pipefish species inhabiting Mediterranean seagrasses. Mediterranean Marine Science, 22, 705-718.
Dauvin, J.C., Ruellet, T., 2009. The estuarine quality paradox. Is it possible to define an ecological quality status for specific modified and naturally stressed estuarine ecosystems? Marine Pollution Bulletin, 59, 38-47.
El Mahrad, B., Abalansa, S., Newton, A., Icely, J.D., Snoussi, M. et al., 2020. Social-Environmental Analysis for the Management of Coastal Lagoons in North Africa. Frontiers in Environmental Science, 8.
Elliott, M., Whitfield, A.K., Potter, I.C., Blaber, S.J.M.M., Cyrus, D.P. et al., 2007. The guild approach to categorizing estuarine fish assemblages: A global review. Fish and Fisheries, 8, 241-268.
Facca, C., Cavraro, F., Franzoi, P., Malavasi, S., 2020. Lagoon Resident Fish Species of Conservation Interest According to the Habitat Directive (92/43/CEE): A Review on Their Potential Use as Ecological Indicator Species. Water, 12, 2059.
Fonseca, V.F., Vasconcelos, R.P., Gamito, R., Pasquaud, S., Gonçalves, C.I. et al., 2013. Fish community-based measures of estuarine ecological quality and pressure-impact relationships. Estuarine, Coastal and Shelf Science, 134, 128-137.
Fox, J., Weisberg, S., 2011. An R Companion to Applied Regression, Second Edition. Franco, A., Torricelli, P., Franzoi, P., 2009. A habitat-specific fish-based approach to assess the ecological status of Mediterranean coastal lagoons. Marine Pollution Bulletin, 58, 1704-1717.
Franco, A., Franzoi, P., Malavasi, S., Riccato, F., Torricelli, P., 2006. Fish assemblages in different shallow water habitats of the Venice Lagoon. Hydrobiologia., 555, 159-174.
Franco, A., Elliott, M., Franzoil, P., Torricellil, P., 2008. Life strategies of fishes in European estuaries: the functional guild approach. Marine Ecology-Progress Series, 354 %W
Franco, A., Pérez-Ruzafa, A., Drouineau, H., Franzoi, P., Koutrakis, E. T. et al., 2012. Assessment of fish assemblages in coastal lagoon habitats: Effect of sampling method. Estuarine, Coastal and Shelf Science, 112, 115-125.
García-Oliva, M., Pérez-Ruzafa, Á., Umgiesser, G., McKiver, W., Ghezzo, M. et al., 2018. Assessing the hydrodynamic response of the Mar Menor lagoon to dredging inlets interventions through numerical modelling. Water, 10, 1-33.
García-Sánchez, M., Korbee, N., Pérez-Ruzafa, I.M., Marcos, C., Domínguez, B. et al., 2012. Physiological response and photoacclimation capacity of Caulerpa prolifera (Forsskål) JV Lamouroux and Cymodocea nodosa (Ucria) Ascherson meadows in the Mar Menor lagoon (SE Spain). Marine Environmental Research, 79, 37-47.
Gonzalez, E.G., Cunha, C., Ghanavi, H.R., Oliva-Paterna, F.J., Torralva, M. et al., 2018. Phylogeography and Population Genetic Analyses in the Iberian Toothcarp (Aphanius iberus Valenciennes, 1846) at Different Time Scales. Journal of Heredity, 109, 253-263.
Guerrero-Gómez, A., Zamora-López, A., Guillén-Beltrán, A., Zamora-Marín, J. M., Sánchez-Pérez, A. et al., 2022. An updated checklist of YOY fish occurrence in the shallow perimetral areas of the Mar Menor (Western Mediterranean Sea). Limnetica, 41, 101-106.
Hallett, C.S., Trayler, K.M., Valesini, F.J., 2019. The Fish Community Index: A Practical Management Tool for Monitoring and Reporting Estuarine Ecological Condition. Integrated Environmental Assessment and Management, 15, 726-738.
Hughes, B.B., Lummis, S.C., Anderson, S.C., Kroeker, K.J., 2018. Unexpected resilience of a seagrass system exposed to global stressors. Global Change Biology, 24, 224-234.
Hughes, J.E., Deegan, L.A., Wyda, J.C., Weaver, M.J., Wright, A., 2002. The effects of eelgrass habitat loss on estuarine fish communities of southern New England. Estuaries, 25, 235-249.
Jacobson, P.C., Hansen, G.J.A., Bethke, B.J., Cross, T.K., 2017. Disentangling the effects of a century of eutrophication and climate warming on freshwater lake fish assemblages. PLoS one, 12, 1-17.
Jiang, Z., Du, P., Liu, J., Chen, Y., Zhu, Y. et al., 2019. Phytoplankton biomass and size structure in Xiangshan Bay, China: Current state and historical comparison under accelerated eutrophication and warming. Marine Pollution Bulletin, 142, 119-128.
Jones, J.C., Reynolds, J.D., 1999. The influence of oxygen stress on female choice for male nest structure in the common goby. Animal Behaviour, 57, 189-196. Jones, S., 2022. Endangered Mar Menor lagoon in Spain granted legal status as a person. The Guardian.
Koutrakis, E.T., Tskliras, A.C., 2009. Reproductive biology of the marbled goby, Pomatoschistus marmoratus (Pisces, Gobiidae), in a northern Aegean estuarine system (Greece). Folia Zoologica, 58, 447-456.
Koyama, A., Inui, R., Akamatsu, Y., Onikura, N., 2019. Physicochemical factors affecting goby fauna in the intertidal zones of temperate riverine estuaries of the Seto Inland Sea. Estuarine, Coastal and Shelf Science, 219, 24-32.
Lenth, R., 2020. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.4.5. Mazzoldi, C., Rasotto, M.B., 2001. Extended breeding season in the marbled goby, Pomatoschistus marmoratus (Teleostei: Gobiidae), in the Venetian Lagoon. Environmental Biology of Fishes, 61, 175-183.
Mercado, J.M., Cortés, D., Gómez-Jakobsen, F., García- Gómez, C., Ouaissa, S. et al., 2021. Role of small-sized phytoplankton in triggering an ecosystem disruptive algal bloom in a Mediterranean hypersaline coastal lagoon. Marine Pollution Bulletin, 164, 111989.
Müller, C., Erzini, K., 2016. Description of burrowing behaviour of the pipefish Syngnathus abaster Risso, 1827 in the Ria Formosa lagoon, Portugal. Journal of Applied Ichthyology, 32, 973-975.
Oliva-Paterna, F.J., Torralva, M., Fernández-Delgado, C., 2006. Threatened fishes of the world: Aphanius iberus (Cuvier & Valenciennes, 1846) (Cyprinodontidae). Environmental Biology of Fishes, 75, 307-309.
Oliva-Paterna, F.J., Ruiz-Navarro, A., Torralva, M., Fernández- Delgado, C., 2009. Biology of the endangered cyprinodontid Aphanius iberus in a saline wetland (SE Iberian Peninsula). Italian Journal of Zoology, 76, 316-329.
Olsson, J., Andersson, M.L., Bergström, U., Arlinghaus, R., Audzijonyte, A. et al., 2023. A pan-Baltic assessment of temporal trends in coastal pike populations. Fisheries Research, 260, 106594.
Parmanne, R., Lindström, K., 2003. Annual variation in gobiid larval density in the northern Baltic Sea. Journal of Fish Biology, 62, 413-426.
Pérez-Ruzafa, A., Marcos, C., 2012. Fisheries in coastal lagoons: An assumed but poorly researched aspect of the ecology and functioning of coastal lagoons. Estuarine, Coastal and Shelf Science, 110, 15-31.
Pérez-Ruzafa, A., Marcos, C., Gilabert, J., 2005. The ecology of the Mar Menor coastal lagoon: A fast changing ecosystem under human pressure. p. 392-422. In: Coastal lagoons. Ecosystem processes and modeling for sustainable use and development. Gönenç, I. E., J. P. Wolflin (Eds.), CRC Press, Boca Raton.
Pérez-Ruzafa, A., García-Charton, J.A., Barcala, E., Marcos, C., 2006. Changes in benthic fish assemblages as a consequence of coastal works in a coastal lagoon: The Mar Menor (Spain, Western Mediterranean). Marine Pollution Bulletin, 53, 107-120.
Pérez-Ruzafa, A., Mompeán, M.C., Marcos, C., 2007. Hydrographic, geomorphologic and fish assemblage relationships in coastal lagoons. Hydrobiologia, 577, 107-125.
Pérez-Ruzafa, A., Marcos, C., Pérez-Ruzafa, I. M., 2011. Mediterranean coastal lagoons in an ecosystem and aquatic resources management context. Physics and Chemistry of the Earth, 36, 160-166.
Pérez-Ruzafa, A., Marcos, C., Bernal, C.M., Quintino, V., Freitas. et al,. 2012. Cymodocea nodosa vs. Caulerpa prolifera: Causes and consequences of a long term history of interaction in macrophyte meadows in the Mar Menor coastal lagoon (Spain, southwestern Mediterranean). Estuarine, Coastal and Shelf Science, 110, 101-115.
Pérez-Ruzafa, A., Marcos, C., Pérez-Ruzafa, I.M., 2018. When maintaining ecological integrity and complexity is the best restoring tool: The case of the Mar Menor lagoon. p. 67-95. In:, Management and restoration of Mediterranean coastal lagoons in Europe. Quintana, X., Boix, D., Gascón, S., Sala J. (Eds.) Càtedra d’Ecosistemes mediterranis litorals i LIFE Pletera, Girona.
Pérez-Ruzafa, A., Campillo, S., Fernández-Palacios, J.M., García-Lacunza, A., García-Oliva, M. et al., 2019. Longterm dynamic in nutrients, chlorophyll a, and water quality parameters in a coastal lagoon during a process of eutrophication for decades, a sudden break and a relatively rapid recovery. Frontiers in Marine Science, 6, 1-23.
Pérez-Ruzafa, A., Pérez-Marcos, M., Marcos, C., 2020a. Coastal lagoons in focus: Their environmental and socioeconomic importance. Journal for Nature Conservation, 57, 125886.
Pérez-Ruzafa, A., Morkune, R., Marcos, C., Pérez-Ruzafa, I.M., Razinkovas-Baziukas, A., 2020b. Can an oligotrophic coastal lagoon support high biological productivity? Sources and pathways of primary production. Marine Environmental Research, 153 (October), 104824.
Pombo, L., Rebelo, J. E., 2002. Spatial and temporal organization of a coastal lagoon fish community - Ria de Aveiro, Portugal. Cybium, 26, 185-196.
R Core Team, 2020. R: A language and environment for statistical computing.
Ram, A., Jaiswar, J.R. M., Rokade, M.A., Bharti, S., Vishwasrao, C. et al., 2014. Nutrients, hypoxia and Mass Fish kill events in Tapi Estuary, India. Estuarine, Coastal and Shelf Science, 148, 48-58.
Reis-Filho, J.A., Giarrizzo, T., 2016. Microgobius meeki as a potential bio-indicator of habitat disturbance in shallow estuarine areas: a useful tool for the assessment of estuarine quality. Journal of fish biology, 89, 713-734.
Ribeiro, J., Carvalho, G.M., Gonçalves, J.M.S., Erzini, K., 2012. Fish assemblages of shallow intertidal habitats of the Ria Formosa lagoon (South Portugal): Influence of habitat and season. Marine Ecology Progress Series, 446, 259-273.
Robledano, F., Calvo-Sendín, J.F., Hernández-Gil, V. (Eds.), 2006. Libro rojo de los vertebrados de la Región de Murcia. Comunidad Autónoma de la Región de Murcia, Murcia, 358 pp.
Rose, T.H., Tweedley, J.R., Warwick, R.M., Potter, I.C., 2019. Zooplankton dynamics in a highly eutrophic microtidal estuary. Marine Pollution Bulletin, 142, 433-451.
Ruiz-Fernández, J.M., León, V., Marín-Guirao, L., Giménez- Casaduero, F., Rogel, J. et al., 2019. Synthesis report of the current state of Mar Menor lagoon and its causes in relation to the nutrient contents. Instituto Español de Oceanografía (IEO), IEO Technical report, 7 pp.
Ruiz-Fernández, J.M., Albentosa, M., Aldeguer, B., Álvarez- Rogel, J., Antón, J. et al., 2020. Informe de evolución y estado actual del Mar Menor en relación al proceso de eutrofización y sus causas. Informe de asesoramiento técnico. Instituto Español de Oceanografía (IEO), IEO Technical report, 165pp.
Sayer, C.D., Davidson, T.A., Rawcliffe, R., Langdon, P.G., Leavitt, P.R. et al., 2016. Consequences of Fish Kills for Long-Term Trophic Structure in Shallow Lakes: Implications for Theory and Restoration. Ecosystems, 19, 1289-1309.
Scapin, L., Zucchetta, M., Facca, C., Sfriso, A., Franzoi, P., 2016. Using fish assemblage to identify success criteria for seagrass habitat restoration. Web Ecology, 16, 33-36.
Scapin, L., Cavraro, F., Malavasi, S., Riccato, F., Zucchetta, M. et al., 2018a. Linking pipefishes and seahorses to seagrass meadows in the Venice lagoon: Implications for conservation. Aquatic Conservation: Marine and Freshwater Ecosystems, 28, 282-295.
Scapin, L., Zucchetta, M., Sfriso, A., Franzoi, P., 2018b. Local Habitat and Seascape Structure Influence Seagrass Fish Assemblages in the Venice Lagoon: The Importance of Conservation at Multiple Spatial Scales. Estuaries and Coasts, 41, 2410-2425.
Schneider, C.A., Rasband, W.S., Eliceiri, K.W., 2012. NIH Image to ImageJ: 25 years of image analysis. Nature methods, 9, 671-675.
Souza, G.B.G., Vianna, M., 2020. Fish-based indices for assessing ecological quality and biotic integrity in transitional waters: A systematic review. Ecological Indicators, 109, 105665.
Tallmark, B., Evans, S., 1986. Substrate-related differences in anti-predator behaviour of two gobiid fish species and the brown shrimp, and their adaptive value. Marine Ecology Progress Series, 29, 217-222.
Tomasini, J.A., Quignard, J.P., Capape, C., Bouchereau, J.L., 1991. Facteurs du succes reproductif de Syngnathus abaster Risso, 1826 (Pisces, Teleostei, Syngnathidae) en milieu lagunaire mediterraneen (lagune de Mauguio, France). Acta oecolologica, 12, 331-355.
Verdiell-Cubedo, D., Oliva-Paterna, F. J., Torralva, M., 2007. The effects of competitors on fitness of marbled goby Pomatoschistus marmoratus (Pisces, Gobiidae) in the Mar Menor coastal lagoon (SE Iberian Peninsula). Italian Journal of Zoology, 74 (2), 169-177.
Verdiell-Cubedo, D., Oliva-Paterna, F.J., Egea-Serrano, A.E., Torralva, M., 2008. Population biology and habitat associations of benthic fish species in the shallow areas of a Mediterranean coastal lagoon (SE Iberian Peninsula). Scientia Marina, 72 (2), 319-328.
Verdiell-Cubedo, D., Torralva, M., Andreu-Soler, A., Oliva-Paterna, F.J., 2012. Effects of Shoreline Urban Modification on Habitat Structure and Fish Community in Littoral Areas of a Mediterranean Coastal Lagoon (Mar Menor, Spain). Wetlands, 32 (4), 631-641.
Verdiell-Cubedo, D., Torralva, M., Ruiz-Navarro, A., Oliva-Paterna, F.J., 2013. Fish assemblages in different littoral habitat types of a hypersaline coastal lagoon (Mar Menor, Mediterranean Sea). Italian Journal of Zoology, 80, 104-116.
Verdiell-Cubedo, D., Ruiz-Navarro, A., Torralva, M., Moreno- Valcárcel, R., Oliva-Paterna, F.J., 2014. Habitat use of an endangered cyprinodontid fish in a saline wetland of the Iberian Peninsula (SW Mediterranean Sea). Mediterranean Marine Science, 15, 27-36.
Viaroli, P., Nizzoli, D., Pinardi, M., Soana, E., Bartoli, M., 2015. Eutrophication of the Mediterranean Sea: a watershed- cascading aquatic filter approach. Rendiconti Lincei, 26, 13-23.
Vivas, M., Peñalver, J., Oliver, J.A., López Giraldo, J.D., Mena, C., 2023. Population dynamics of the long‐snouted seahorse (Hippocampus guttulatus Cuvier, 1829) in the Mar Menor coastal lagoon. Journal of Fish Biology, 104, 163-170.
Whitfield, A.K., Elliott, M., 2002. Fishes as indicators of environmental and ecological changes within estuaries: A review of progress and some suggestions for the future. Journal of Fish Biology, 61, 229-250.
Zamora-López, A., Guerrero-Gómez, A., Torralva, M., Zamora- Marín, J.M., Guillén-Beltrán, A. et al., 2023. Shallow waters as critical habitats for fish assemblages under eutrophication- mediated events in a coastal lagoon. Estuarine, Coastal and Shelf Science, 291, 108447.