Greater resilience of reef fish assemblages in a no-take reserve compared to multi-use areas of the Gulf of California

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Highlights

  • Marine reserve was more effective in maintaining fish functional diversity.

  • Fish density declines were associated to natural and anthropogenic disturbances.

  • Loser and winner species at all MPA indicated that functional structure is dynamic.

  • The marine reserve showed resilience by maintaining species and functional diversity.

  • Analyses of continuous years are necessary to detect accurate patterns in diversity.

Abstract

Conservation strategies, such as the establishment of Marine Protected Areas (MPAs), aim to safeguard biodiversity and to promote resilience of ecosystems by increasing their capacity to maintain key functions and processes following disturbance. However, the extent to which ecosystems in MPAs exhibit resilience remains debated. To address this question, we evaluated changes in reef fish species and functional diversity over time in relation to environmental and anthropogenic disturbances at multiple locations in the Gulf of California, Mexico. From 2005 to 2017, we assessed reef fish species richness and abundance in three MPAs: one no-take marine reserve (Cabo Pulmo) and two multi-use marine protected areas (MUMPAs: Espíritu Santo and Loreto). To examine change in functional diversity and composition, we calculated three functional diversity indices – functional richness, functional dispersion and functional originality – using six biological traits (size, mobility, period of activity, gregariousness, water column position, and diet). Species richness, density and functional diversity were maintained over time (resilience) in the no-take marine reserve. In contrast, MUMPAs showed temporal decline in species richness, which translated into decreases in functional richness and increases in functional dispersion. These differences were also observed at the species level: in Cabo Pulmo, only two ‘loser’ species declined in density, while Espíritu Santo and Loreto showed declines of 12 and 17 species, respectively. The two MUMPAs also shared 9 of the total 22 ‘loser’ species, which are generally abundant and common in the Gulf of California. Density declines were attributed to the combined effect of environmental (sea surface temperature and Chlorophyll-a anomalies) and anthropogenic (fishing, tourism and coastal population density) disturbances. Given the regional decline and the ecological importance of dominant species, long-term decreases in their populations can profoundly modify processes and reef ecosystem services in this region. Thus, local management strategies should be implemented to try to reverse the observed recent decline in fish diversity in MUMPAs.

Introduction

Biodiversity loss in reef ecosystems associated with environmental (El Niño events and marine heat waves) and anthropogenic (overfishing, pollution or increase in tourism activities) drivers can result in loss of ecological functions and services (Miller et al., 2011, Mouillot et al., 2013). To cope with these disturbances, biological systems respond to new conditions at individual (physiological acclimatization), population (changes in distribution ranges and demography), and community (ecological reorganization) organization levels (Webster et al., 2017).

At the community level, overlap in species functions (redundancy) allows communities to preserve ecological processes and therefore present high resilience (Figge, 2004, Hooper et al., 2005), defined as the capacity of a system to maintain structure or function in the presence of disturbance (Walker et al., 2007, O'Leary et al., 2017). This ‘portfolio effect’ is theoretically possible but in practice, it has been difficult to assess resilience in natural communities. To this end, the combination of traditional biodiversity metrics (e.g. species richness) with biological trait analysis (used as a proxy of species functional roles) has become an essential tool to determine the degree of functional redundancy in biotic assemblages, and improve our understanding of the response of ecosystems to disturbance (Hooper et al., 2005, Mouillot et al., 2013).

Conservation strategies involving the establishment of Marine Protected Areas (MPAs) are among the primary means to safeguard biodiversity and to promote resilience of ecosystems by increasing their capacity to maintain key functions and processes following disturbance (Agardy, 1994, Micheli et al., 2014). Different protection schemes involving MPAs have been established around the world, ranging from fishing bans in no-take marine reserves, to the regulation of extractive activities in multi-use marine protected areas (MUMPAs; Agardy et al., 2003, Sala et al., 2018). Previous analyses have shown that well-managed no-take marine reserves lead to increased fish abundances and species richness (Lester et al., 2009), whereas studies in MUMPAs have generally demonstrated positive but non-significant outcomes in these ecological indicators (Lester and Halpern, 2008).

The extent to which reef ecosystems in MPAs exhibit resilience to disturbances remains uncertain as a result of the scarcity of analyses of functional diversity change over time, which in turn is due to the difficulty to maintain long-term monitoring and to the lack of continuous data (Edgar and Stuart-Smith, 2014, Fulton et al.,). Long-term monitoring programs, such as those in place at temperate reefs in Tasmania since 1992, have shown changes in species richness and increases in functional diversity in studies conducted over decadal periods (Bates et al., 2014a, Bates et al., 2014b). These changes include effects of tropicalization (rise in temperature and the associated decrease in the concentration of nutrients) that manifest regardless of the different management schemes (no-take marine reserves or MUMPAs). However, even in the presence of these environmental changes, long-term no-take marine reserves present greater stability (low temporal variability) in biological responses to disturbances in comparison with fished sites in Tasmania (Bates et al., 2014a, Bates et al., 2014b). Interestingly, the biotic response to perturbations can be similar across different level of protection; for example, areas of the Great Barrier Reef showed a general decline in species richness and fish density associated with the impact of tropical cyclone Yasi in 2011, followed by recovery of herbivorous/detritivorous and planktivorous fish. This response was similar everywhere, independent of the protection scheme (Bierwagen et al., 2018).

Long-term biodiversity data have also been analyzed in different MPAs of the Gulf of California, Mexico. In 2006, Alvarez-Filip and Reyes-Bonilla showed declines in fish species richness in the Cabo Pulmo MPA between 1987 and 2003, following a severe coral bleaching event caused by the 1997–1998 El Niño and a series of hurricanes that impacted the reef in 2002–2003. These events significantly modified the habitat (coral cover loss > 50%) and caused a decline of associated invertebrates and fishes. However, at the same time fish assemblages showed maintenance in functional diversity, which was attributed to a high degree of functional redundancy. Aburto-Oropeza and collaborators (2011) also reported that fish biomass was similar between Cabo Pulmo, core zones of MUMPAs (including Espíritu Santo and Loreto), and open access sites immediately after the ENSO event, in 1999, but after ten years of protection, in 2009, Cabo Pulmo presented a dramatic increase of fish biomass (463%) and species richness (166%). This positive effect was attributed to social (support of the protection measures by residents, continuous monitoring and application of environmental regulations) and ecological (creation of a large ∼ 70 km2 MPA, good condition of the coral community, high primary productivity and presence of fish spawning areas) factors. Recently, a trophodynamic ECOPATH model based on survey (2017–2018) and published data found evidence that Cabo Pulmo is a relatively mature ecosystem that exhibits high resilience to disturbances, such as coral bleaching and hurricanes, compared to other ecosystems from the Tropical Eastern Pacific (Calderon-Aguilera et al., 2021). By conducting taxonomic, functional and trophic analyses, these studies have shown that the Cabo Pulmo reefs have been resilient since the establishment of the MPA (1995). However, further analyses are necessary to determine if this capacity is maintained through time.

The effectiveness of protection was also evaluated at the Loreto MPA (central Gulf of California) in a continuous time series (1998 to 2010), which found an increase in herbivorous and planktivorous fish biomass in a small no-take zone within the MPA, while the rest of the MPA -where fishing is allowed- did not show significant temporal changes (Rife et al., 2013a). The authors conclude that the management strategies have contributed to maintain the original conditions of fish assemblages, but that it is necessary to promote enforcement to avoid or reduce legal and illegal fishing inside the MPA.

Finally, evaluation of changes in fish assemblages through time (2005 to 2017) in the Espíritu Santo MPA showed that the conservation aims of this MUMPA have not been accomplished because, despite a long-term increase in biomass (associated to a general increase in fish average size) and maintenance in density and functional originality, species richness, functional richness and some species significantly declined probably due to competitive interactions, habitat loss, and persistence of fishing pressure (Ramírez-Ortiz et al., 2020). Since buffer and no-take zones presented similar results, the authors recommended enforcement of fishing regulations and surveillance in core zones to promote the conservation of fish functional diversity in this MUMPA.

In this paper we evaluated 1) whether fish species richness, density and functional diversity changed through time (2005 to 2017) in one no-take marine reserve (Cabo Pulmo) and two MUMPAs (Espíritu Santo and Loreto) of the Gulf of California, and 2) if changes were associated with environmental or anthropogenic disturbances. This kind of analysis is important considering that the region has been exposed to continuous and intense disturbances, which include high fishing pressure (70% of the fishing activities in Mexico are performed in the Gulf; Cisneros-Mata, 2010, Díaz-Uribe et al., 2013), and accelerated coastal development (Lluch-Cota et al., 2007, Franco-Ochoa et al., 2020), as well as recent increases in sea surface temperature (2013 to 2016: ∼ +2 °C) and declines in primary productivity (∼ -1.5 mg/m3; Gomez-Ocampo et al., 2018). Under these pressures, it is relevant to assess the effects of anthropogenic and environmental disturbances on reef fish functional diversity in MPAs to determine if conservation strategies have been able to mitigate the impacts of these chronic pressures.

To accomplish our goal, we evaluated temporal changes in fish diversity in each MPA. Our premise is that if the area maintained fish species richness, density and functional diversity throughout the study period, it should be considered resilient. If the MPA exhibited changes, we analyzed how variation in the presence and density of common species (those present in > 50% of the surveys) in each MPA contributed to the observed trends in the indices. Finally, we examined the possible role of environmental and anthropogenic variables in explaining temporal population change. We tested the hypotheses that a decrease in fish species richness translates into negative changes in functional diversity independently of the protection scheme, and that the no-take marine reserve Cabo Pulmo and the MUMPAs (Espíritu Santo and Loreto) exhibit similar decline patterns at the assemblage and species level due to a combination of environmental and anthropogenic disturbances that have been observed in the Gulf of California within the last decade.

Section snippets

Study area

The Gulf of California is a dynamic marginal sea (1,600 km long) of the Eastern Pacific Ocean, considered as a transition zone between tropical and subtropical climate regimes, that is exposed to multi-year processes such as the El Niño–Southern Oscillation (ENSO) and the Pacific Decadal Oscillation (PDO; Lluch-Cota et al., 2013). The Gulf of California is an area of high primary productivity with a latitudinal gradient (highest values in the north compared to the south portion), associated

Results

Temporal analyses revealed non-significant changes in the no-take marine reserve Cabo Pulmo for the five ecological indicators (Fig. 2a), while MUMPAs Espíritu Santo (Fig. 3a; Ramírez-Ortiz et al. 2020) and Loreto (Fig. 4a) showed significant decreases in species richness that translated into less functional richness and higher functional dispersion at the end of the study period. Functional originality showed non-significant changes in all MPAs, which suggests that despite the low functional

Discussion

The analysis of fish diversity change over time performed in this study showed that the fully-protected MPA in Cabo Pulmo did not present significant changes in any of the calculated indices, while the partially-protected Loreto and Espíritu Santo showed significant decreases in species and functional richness over the same time period (Fig. 3a; Fig. 4a).

Conclusions

Long-term surveys and diversity analyses show that the fully-protected reefs of Cabo Pulmo appear resilient due to maintenance of fish diversity and limited species-level changes over the years. By contrast, MUMPAs showed biodiversity loss at the community and species level within the study period, associated to environmental anomalies of SST and CHL_a (previously reported for the California Current), as well as anthropogenic disturbances related to increases in visitors, human population and

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This work was funded by Comisión Nacional de Áreas Naturales Protegidas (PROMOBI/IGCBCS/003/2015 and CONANP/PROMANP/MB/DRPBCPN/02/2016), Sociedad de Historia Natural Niparajá, A. C., David & Lucile Packard Foundation, Sandler Family Foundation, The Walton Family Foundation, The Waterloo Foundation, and dataMares. FM acknowledges the US NSF (grant # 2108566), and GRO acknowledges the CONACYT (grant # 266599) and CIBNOR (grant # 1106) scholarship for her Doctorate degree.

We thank the editors

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    Present address: Unidad Académica Mazatlán, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mazatlán, Sinaloa, Mexico.

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