Agent-based model of Eastern Pacific damselfish and sea urchin interactions shows increased coral reef erosion under post-ENSO conditions
Introduction
Trophic and non-trophic interactions can have significant influences on ecosystems (Schmitz, 2009). For example, aggression or predation can lead to shifts in habitat use in many organisms, marine as well as terrestrial (Pringle et al., 2019). On eastern Pacific coral reefs, population and movement dynamics of a sea urchin (Diadema mexicanum) can be positively or negatively influenced by damselfish (Stegastes acapulcoensis) aggression (Glynn, 1990; Hixon, 1997, 2015; Jones, 1991; Karlson, 1999; Kaufman, 1977; Pennings, 1997; Potts, 1977; Vine, 1974). In defending their algal lawn territories, damselfishes aid (Sammarco, 1980; Wellington, 1982) or interfere (Lobel, 1980; Potts, 1977) with sea urchins, by providing trophic resources or in limiting grazing time respectively. But damselfish also influence coral recruitment, competitive outcomes among corals (Kaufman, 1977), reduce coral mortality from predators and competitors (Glynn and Colgan, 1988; Sammarco and Carleton, 1982; Sammarco and Williams, 1982), and affect bioerosive processes (Risk and Sammarco, 1982; Sammarco et al., 1987; Strömberg and Kvarnemo, 2005). Thus, a tight coupling of movement and population dynamics of sea urchins and damselfish behaviors and abundance can be expected that in turn will influence corals and reef-building accretion. But the net influence of this multi-faceted interaction on the ecosystem and on reef-building are still poorly understood. It furthermore remains unquantified whether the spatial distribution of damselfish on a Panamanian coral reef (Uva Island) might exacerbate the erosion and degradation of the reef framework, especially following severe El Niño Southern Oscillation (ENSO) events, such as in 1982–1983.
The fundamental ecological interactions between damselfish, which cultivate and protect algal lawn territories, and sea urchins that graze on algae and in the process erode coral substrates, are herein explored in a modeling study based on empirical observations. ENSO events (Cortés et al., 1984; Glynn, 1983, 1984; Robinson, 1985; Von Prahl, 1983) trigger these interactions by precipitating increases in sea urchin population abundances (Eakin, 1996; Glynn, 1988). Sea urchins attempting to invade and graze on algal lawns are aggressively ejected by damselfish and tend to form aggregations outside of defended lawn territories. The sea urchin aggregations persist and result in severe coral erosion (bioerosion) (Eakin, 1996, 2001; Glynn, 1988). Later sea urchin declines coincided with loss of topographic complexity, suggesting echinoid population collapse was precipitated by their increased bioerosional activity and loss of sheltering habitat (Eakin, 2001). After their population collapse, Uva reef experienced robust recovery and its present-day morphology consists of patches with high live coral cover interspersed with areas of little to no coral cover strewn with dead coral rubble (Fong et al., 2017).
From this sequence of events we derive the testable null-hypothesis that damselfish ejection of sea urchins from their territories has no effect on coral bioerosion. Our empirical observations support an alternative hypothesis, namely that the defense of algal lawns by damselfish can indeed promote sea urchin aggregations that exacerbate coral bioerosion. Thus, a spatially heterogeneous pattern of high and low densities of sea-urchins will lead to areas of increased erosion versus areas of favored coral growth. By protecting their algal lawns from sea-urchins, the damselfish at the same time may create a refuge for corals. High densities of damselfish territories could therefore protect corals, which is in contrast to the Caribbean where some damselfish species kill corals to establish their territories and can therefore negatively impact coral health (Precht et al., 2010; Vermeij et al, 2015).
To evaluate the suspected role of damselfish-sea urchin interaction, we developed a spatially explicit model of a study site located on Uva reef (Gulf of Chiriquí, Panama) following an El Niño-Southern Oscillation (ENSO) event that resulted in high echinoid abundances and low coral cover using agent-based modeling techniques to simulate the daily interactions between damselfish and sea urchins across both space and time to explore whether this alternative hypothesis could indeed be supported.
Section snippets
Study site
Studies were conducted at the Uva Island coral reef (7°48′46″N, 81°45′35″W) in the Gulf of Chiriquí, Pacific Panama (Fig. 1A and B). This reef is ~2.5 ha in planar area, shallow (1–6 m depth) and is situated in a sheltered, NW-facing embayment. The principal framework- building corals are ramose, pocilloporid species, mainly Pocillopora damicornis and Pocillopora elegans.
A bathymetric map (Fig. 1 C) was produced in May 2010, using a downward-directed ADCP (Acoustic Doppler Current Profiler)
Results
Mean sea urchin ejection event count frequencies within the MP for the n1 = 250 test cases where damselfish are present was 0.886 ± 0.036 ejections m−2 day−1 (mean ± SD) (Fig. 8 A). Sea urchin ejection event count frequencies were binned in intervals of 0.01 ejections m−2 day−1. The mean sea urchin ejection event count frequency included ejection events resulting from damselfish aggression and from ejection events caused when a sea urchin aggregation attempted to move to another cell in the MP
Discussion
Our modeling study confirms a strong interaction between damselfish and sea urchins and that damselfish agonistic behavior towards invading echinoids contributes to a complex indirect effect on the overall CaCO3 budget of a coral reef. The bioerosion score frequencies where damselfish were present was 2.0842 ± 0.8398 g m−2 day−1, which are significantly different than the bioerosion score frequencies of 1.526 ± 0.847 g m−2 day−1 where damselfish are not present (two sample t-test, t = 45.177,
Credit author statement
Peter J. Glynn: Conceptualization, Methodology, Software, Validation, Formal Analysis, Writing – Original Draft, Formal Analysis. Peter W. Glynn: Investigation, Writing – Original Draft, Writing – Review & Editing. Juan Mate: Resources, Project Administration. Bernhard Riegl: Investigation, Writing – Original Draft, Writing – Review & Editing, Resources.
Declaration of Competing Interests
None.
Acknowledgments
P.W. Glynn acknowledges U. S. National Science Foundation support, Biological Oceanography Program grants OCE-1447306, OCE-9314798 and earlier awards. We thank Kevan Mantell (Dive Base Coiba, Pixvae, Panama), Ernesto Santos, and Alfredo de León (Mistolín) for field support. The Ministry of Environment (MiAmbiente), Republic of Panama, granted permits to work in the Coiba National Park. Juan Maté was supported by the Smithsonian Tropical Research Institute.
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