Emigration patterns of motile cryptofauna and their implications for trophic functioning in coral reefs

Abstract

Patterns of movement of marine species can reflect strategies of reproduction and dispersal, species' interactions, trophodynamics, and susceptibility to change, and thus critically inform how we manage populations and ecosystems. On coral reefs, the density and diversity of metazoan taxa are greatest in dead coral and rubble, which are suggested to fuel food webs from the bottom up. Yet, biomass and secondary productivity in rubble is predominantly available in some of the smallest individuals, limiting how accessible this energy is to higher trophic levels. We address the bioavailability of motile coral reef cryptofauna based on small-scale patterns of emigration in rubble. We deployed modified RUbble Biodiversity Samplers (RUBS) and emergence traps in a shallow rubble patch at Heron Island, Great Barrier Reef, to detect community-level differences in the directional influx of motile cryptofauna under five habitat accessibility regimes. The mean density (0.13-4.5 ind cm −3 ) and biomass (0.14-5.2 mg cm −3 ) of cryptofauna were high and varied depending on microhabitat accessibility. Emergent zooplankton represented a distinct community (dominated by the Appendicularia and Calanoida) with the lowest density and biomass, indicating constraints on nocturnal resource availability. Mean cryptofauna density and biomass were greatest when interstitial access within rubble was blocked, driven by the rapid proliferation of small harpacticoid copepods from the rubble surface, leading to trophic simplification. Individuals with high biomass (e.g., decapods, gobies, and echinoderms) were greatest when interstitial access within rubble was unrestricted.Treatments with a closed rubble surface did not differ from those completely open, suggesting that top-down predation does not diminish rubble-derived resources. Our results show that conspecific cues and species' interactions (e.g., competition and predation) within rubble are most critical in shaping ecological outcomes within the cryptobiome. These findings have implications for prey accessibility through trophic and community size structuring in rubble, which may become increasingly relevant as benthic reef complexity shifts in the Anthropocene.

Hierarchical drivers of cryptic biodiversity on coral reefs

“…This pattern reflects outcomes anticipated under the intermediate disturbance hypothesis (Connell, 1978), which suggests that species abundance and/or diversity are maximized when the ecological disturbance is neither too low nor high (Dial & Roughgarden, 1998). We speculate that the mid‐exposure site harbors ecological conditions best suited for sessile growth and productivity, including water flow (Gischler, 1997), habitat accessibility (Wolfe, Desbiens, & Mumby, 2023), sedimentation rates (Adam et al, 2015; Logan et al, 2008; Tebbett & Bellwood, 2020), light attenuation (Choi & Ginsburg, 1983) and nutrient profiles (Corredor et al, 1988; Holmes, 1997; Holmes et al, 2000; Nava et al, 2014; Thomas & Atkinson, 1997; Ward‐Paige et al, 2005). However, determining these environmental drivers was beyond the scope of this study and a plethora of alternative hypotheses could be debated, including interactions with other organisms (competition, predation) (Charpy et al, 2012; Cheroske et al, 2000; Gischler, 1997; Meesters et al, 1991) and the age of rubble pieces shaping typical patterns of community succession in rubble (Choi, 1984; Jackson, 1977; Kenyon, 2021; Wulff, 1984).…”

“…Steep spectral slopes ( b ≤ −1.2), as found across all sites here (groove site excluded), indicate small predator–prey ratios within the rubble interstices (Jennings & Mackinson, 2003; Jennings & Warr, 2003) and high predation risk of larger bodied cryptofauna to predators beyond the measured community (Rassoulzadegan & Sheldon, 1986). Coral rubble biomes are certainly dominated by small‐bodied taxa with low biomass (Wolfe, Desbiens, et al, 2020) and these steep slopes reflect high rubble‐derived productivity of the smallest members of the cryptofauna (Wolfe, Desbiens, & Mumby, 2023). Our data demonstrate that rubble is indeed a lower trophic level haven facilitated by high microhabitat complexity that enhances fine‐scale prey refugia (Heather et al, 2021), as found for epifauna in association with turf and macroalgae (Ape et al, 2018; Fraser et al, 2021b; Fraser, Lefcheck, et al, 2020; Kramer et al, 2017).…”

“…This supports key concepts in the hierarchical structuring theory of global ecosystems (O'Neill et al, 1989; Wu & Loucks, 1995). Indeed, fine‐scale patterns in microhabitat complexity influence coral reef biodiversity with the potential to shape ecological outcomes, but exactly how the proliferation of life in rubble scales up to influence reef food webs and functioning requires attention (Wolfe, Desbiens, & Mumby, 2023). Quantification of direct biomass and energy transfers from the rubble to higher order fishes are needed to predict how bottom‐up processes within rubble may alter trophic and fisheries productivity as reefs degrade. Size spectra analysis of the motile cryptofauna revealed the steepest slopes in shallow sites, coinciding with an increase in rubble branchiness and higher cover of macroalgae, turf and sessile invertebrates.…”

“…Sessile taxa and motile cryptofauna communities are associated with a range of environmental parameters including flow, wave energy, light attenuation, and sedimentation in rubble biomes (Wolfe et al, 2021), but these factors were not measured along the disturbance gradient at Heron Reef. We predict that increased rubble branchiness would facilitate greater accessibility and interstitial flow within rubble beds (Wolfe, Desbiens, & Mumby, 2023), which may provide optimal conditions with regard to the penetration of oxygen, the influx of nutrients, and deposition of sediment in the rubble framework. How differences in rubble branchiness and patch depth (i.e., crypts and interstitial space) influence reef biogeochemistry, including oxygen profiles and carbonate chemistry, are yet to be quantified.…”

“…As lower biological entities, cryptofauna can have disproportionate contributions to coral reef food webs and functioning relative to their size (Brandl et al, 2019; Glynn & Enochs, 2011; Goatley & Brandl, 2017; Opitz, 1993). Higher trophic levels are dependent on these lower‐level entities within the cryptobenthos (Glynn & Enochs, 2011; Mihalitsis et al, 2022), but little is known about the response of cryptofauna to microhabitat structure and exactly how lower‐level outcomes scale up to influence reef communities at seascape scales and vice versa (Wolfe, Desbiens, & Mumby, 2023). It is therefore critical to ask to what extent changes in microhabitat complexity influence the cryptofauna given the observed and predicted macro‐scale outcomes for reef fishes and coral reefs in the Anthropocene (Strona et al, 2021).…”