Combinations of biological attributes predict temporal dynamics of fish species in response to environmental changes
Introduction
Human activities have strongly and sometimes irreversibly impacted all ecosystems on Earth, either directly or through global change (Vitousek, 1997). These disturbances induce deep modifications of ecological communities and a loss of the biodiversity upon which ecosystem goods and services depend. Because the magnitude and the frequency of human-mediated disturbances are likely to intensify over the coming decades (Millennium Ecosystem Assessment, 2005), there is an urgent need to understand their effects on communities, in order to improve our ability to predict potential impacts of environmental modifications.
Changes in biodiversity can be complex because species of the same community can exhibit markedly different responses to disturbances (Hughes, 2000). Contrary to expectations from the neutral theory, species demographic response to disturbances (e.g. changes in occurrence, abundance or biomass) is not a random process (Kadmon and Benjamini, 2006). Disturbances tend to affect some species more than others, as a probable result of differences in their biology and physiology (Mouillot et al., 2013b). Disentangling the intrinsic drivers of the species decline are therefore some of the major challenges in predicting community responses to disturbance, and thus closely linked to conservation objectives.
Among the multiple causes of interspecific variation in species responses to environmental disturbances (e.g. historical abundance or geographical range), species biological attributes (i.e. phylogeny, ecology and physiology) probably play a central role (Purvis et al., 2000). Ecological and life-history traits (ELHT) in particular have often been shown to drive species sensitivity to disturbance and thus seemed be good indicators of the endangered status (McKinney, 1997, Olden et al., 2006). This influence of ELHT on species vulnerability is now well documented for mammals (Purvis et al., 2000, Cardillo and Bromham, 2001, Cardillo and Bromham, 2003, Dulvy et al., 2003, Cardillo et al., 2005, Davidson et al., 2009), birds (Bennett and Owens, 1997, Norris and Harper, 2004, Jiguet et al., 2007, Kruger and Radford, 2008), insects (Williams et al., 2010) and fishes (Olden et al., 2007, Field et al., 2009), where one of the most striking examples is perhaps the relationship between asymptotic body size of fish and sensitivity to fishing effort, with large-bodied species being depleted first (Olden et al., 2008). The link between ELHT of species and their responses to disturbance has resulted in an increasing number of authors investigating the use of biological attributes, alone or combined, for evaluating species vulnerability to environmental changes (Davies et al., 2000, Cardillo et al., 2008, Dalgleish et al., 2010, Angert et al., 2011). This has confirmed the value of multiple combinations of biological attributes to predict species occurrence and relative abundance within communities or habitats (Newbold et al., 2013), or their endangered status (Murray et al., 2011, Cardillo et al., 2008, Anderson et al., 2011, Allen et al., 2012). However, studies investigating the links between combinations of biological attributes and inter-specific variations in temporal demographic response to perturbations are still sparse (Olden et al., 2006, Pocock, 2010).
In the present work, we build on the data gathered through three decades of extensive and standardized annual sampling of fish communities and abiotic parameters in a vast tropical ecosystem (the Terminos lagoon, Mexico) to investigate whether some combinations of biological attributes can be indicators of temporal changes in species demography caused by environmental disturbances. After testing for abiotic environmental modifications in the lagoon over the last thirty years, we developed a methodology to characterize temporal responses of fish species (i.e. “demographic trajectories”) and tested how accurately these responses can be predicted by combinations of biological attributes (mixing ELHT and taxonomy). This information is particularly relevant for fish species, since few evaluations of their sensitivity to environmental changes have been based on multiple combinations of traits (e.g. Olden et al., 2006, Villéger et al., 2010). Assessing and disentangling the drivers of community responses to perturbations in tropical estuarine environments is also particularly relevant because these fragile ecosystems provide many critical goods and services for human populations (Costanza et al., 1997, Rochette et al., 2010Layman et al., 2011). The multiple disturbances linked to human activities in the littoral zone have already strongly impacted their biological communities (Lotze et al., 2006, Halpern et al., 2008). Therefore, in the absence of appropriate conservation measures, the predicted > 60% increase in human populations living within 100 km of the coastline by 2050 (Lefebvre, 2011, Vitousek, 1997) might result in irreversible alterations of their biodiversity and functions.
Section snippets
Study area
The Terminos Lagoon (90°00′–90°20′W18°25′–19°00′N) is the largest estuarine system along the coast of Mexico and the third largest lagoon in the world. Located in the southwest part of the Gulf of Mexico (Fig. 1), it communicates with the sea through only two outlets, located at both ends of Carmen island (30 km long and 2.5 km wide): the Puerto Real outlet to the east and the Carmen outlet to the west. Depths in the lagoon are low (2.5 ± 1.0 m) and water temperatures are high throughout the year
Environmental constraints: Description of abiotic shifts
Abiotic parameters showed very different temporal evolutions over the three decades studied (Fig. 2). Both surface and bottom salinities increased significantly, from 22.8 ± 0.6 (mean ± SE) to 26.8 ± 0.5 and from 24.6 ± 0.5 to 27.9 ± 0.5, respectively, between 1980 and 2011. The water pH increased from 7.7 ± 0.1 in 1980 to 8.9 ± 0.4 in 1997, then decreased back to 7.94 ± 0.47 in 2011. Meanwhile, depth and water clarity both significantly decreased between 1980 and 1997, from 2.84 ± 0.81 to 2.03 ± 1.10 m for depth
Discussion
Our results demonstrate that even the complex and diverse demographic responses of the fish species can be accurately predicted when combining appropriate biological attributes. This validates the used of biological attributes, especially ELHT, as indicators of species vulnerability to local perturbations and stresses their potential value for predicting future temporal changes in the composition of local fish communities.
Conclusions
Our study validates the feasibility of accurately predicting temporal trajectories of fish species in a context of changing environment directly from combinations of appropriate biological attributes. This paves the ways to more complex models to predict future demographic changes in fish communities. The list of discriminant traits might be different in environments undergoing other environmental changes. Therefore, the next step would be to investigate whether the set of traits obtained here
Acknowledgments
This study was funded by the French ANR (Agence nationale de la recherche, C004-2009-01-111465) and the Mexican CONACYT (Consejo Nacional de Ciencia y Tecnologia) through the “BIODIVNEK” project (C004, 2009-01, 111465; coordinators: Pr. David Mouillot and Dr. Julia Ramos-Miranda). We are grateful to all the members of the EPOMEX laboratory and the local fishermen involved in sampling Terminos since 1980 to collect the precious data used in this work. We would also especially like to thank Dr.
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