Cryptic predation on coral spawn: Hidden trophic links in the dead of night

Abstract

Broadcast-spawning, where gametes are released into the water for external fertilization, is a widespread reproductive strategy in marine environments, particularly among invertebrates. Coral broadcast-spawning events rank among nature's most synchronized reproductive phenomena (Harrison et al., 1984). Typically occurring annually, these well-timed events enhance fertilization success by mitigating gamete dilution and satiating predators (Babcock et al., 1986; Harrison et al., 1984; Shlesinger & Loya, 1985). Most corals and reef organisms spawn at night, presumably to reduce gamete predation by visually oriented predators. Consequently, most research and hypotheses regarding gamete predation have focused on conspicuous fish predation (Alino & Coll, 1989; Baird et al., 2001; Chamberland et al., 2017; Ip et al., 2023; Muller & Vermeij, 2011; Pratchett et al., 2001; Westneat & Resing, 1988), leaving the role of cryptic invertebrate consumers underexplored. Based on extensive nocturnal observations in Eilat, Gulf of Aqaba, northern Red Sea, I document previously underappreciated coral spawn predation by diverse invertebrates. These findings reveal previously overlooked trophic interactions and suggest that invertebrate predation may constitute a substantial source of gamete loss, potentially altering fertilization rates or simply reducing overall reproductive output—an increasing concern as coral populations continue to decline globally (Chamberland et al., 2017; Hartmann et al., 2018; Johnston et al., 2020; Levitan et al., 2014; Mumby et al., 2024; Nozawa et al., 2015; Shlesinger & Loya, 2019b; Williamson et al., 2023). Understanding such ecological interactions and their impact on coral-reef resilience is crucial as coral reefs face increasing environmental pressures (Donovan et al., 2021; Hoegh-Guldberg et al., 2017; Hughes et al., 2017; van Woesik et al., 2022).

Most reef-building corals are simultaneous hermaphrodites, functioning as both male and female and releasing eggs and sperm into the water for external fertilization (Harrison, 2011). These gametes, however, remain viable for only a few hours, making precise timing crucial (Levitan et al., 2011; Nozawa et al., 2015; Oliver & Babcock, 1992). The ocean's vast dilution effect coupled with the high palatability of coral eggs exerts pressure for highly synchronized spawning—typically occurring once per species per year, at a specific month, night, and hour. Since 2015, I have conducted an extensive nocturnal survey in the northern Red Sea, documenting the reproduction, behavior, and interactions of coral-reef dwellers. Over five reproductive seasons (June–August 2015–2019), I spent ~300 nights snorkeling and freediving, often for 5–6 h per night, recording spawning events and nocturnal behaviors (Shlesinger et al., 2016, 2017, 2021; Shlesinger & Loya, 2019a, 2019b). Observations continued at a reduced frequency from 2022 to 2024. While the goal was to construct a reproductive calendar for corals and other reef inhabitants, I encountered unexpected trophic interactions, highlighting the substantial but underappreciated role of cryptic invertebrate predation on coral spawn.

To date, invertebrate predation on coral gametes has been documented only recently in the ruby brittle star (Williamson et al., 2023), while most research attributes coral gamete consumption to fish (Figure 1A,B; Appendix S1: Figure S1A). However, my observations reveal numerous invertebrates—spanning multiple phyla—actively preying on coral spawn (Table 1, Video S1). I documented clear predation by the phyla Arthropoda (e.g., crabs; Figure 1C), Echinodermata (e.g., basket stars and brittle stars; Figure 1D, Video S1), Mollusca (e.g., worm-snails; Figure 1E; Appendix S1: Figure S1B), and Cnidaria (e.g., hydrozoans; Figure 1F) feeding on gametes from at least ten coral genera (Figure 1, Video S1, Table 1). Additionally, I observed various species from the phyla Annelida and Ctenophora, and other Echinodermata, Mollusca, and Cnidaria members interacting with gamete bundles (Appendix S1: Figure S1C–F; Video S1), suggesting possible predation. Predation often began immediately upon gamete release but sometimes even earlier. For instance, branching Acropora corals retain egg-sperm bundles at the polyp edge before release, during which crabs were commonly observed nibble on them, occasionally pulling bundles from polyps (e.g., from the zoanthid Palythoa in Figure 1C). Similarly, before sunset-spawning corals released gametes, schools of fish (e.g., sergeant majors, butterflyfish) swam frantically from one coral to another and fed directly from their surfaces, as seen elsewhere (Chamberland et al., 2017; Muller & Vermeij, 2011), hinting at an ability to anticipate spawning events.

Other predators employed diverse, specialized mechanisms and feeding techniques, shaped by their life history, anatomy, and behavior. The sessile gastropods, worm-snails, which inhabit calcareous tubes attached to the substrate, captured coral gamete bundles in mucus nets before pulling them into their mouths (Figure 1E; Appendix S1: Figure S1B). Coral-inhabiting barnacles used their feeding limbs fans (cirri) to capture and consume gamete bundles (Figure 1G,H; Appendix S1: Figure S1D). Sometimes, the barnacles rhythmically extended and retracted their cirri to consume gamete bundles, and in other cases, they were holding their cirri extended to accumulate plenty of coral eggs. Brittle stars commonly extended their arms from hiding spots within coral colonies, waving and coiling them to capture gametes (Figure 1D), as recently reported in the Caribbean (Williamson et al., 2023). Giant basket stars, which have become increasingly abundant in the region, positioned themselves above spawning corals, intercepting large quantities of gamete bundles (Video S1). Additional suspension- and filter-feeders occasionally captured coral gametes, including sea anemones and hydrozoans (Figure 1F), bivalves, benthic comb jellies (Appendix S1: Figure S1E), and feather stars (Appendix S1: Figure S1F). All these organisms exhibit distinct predation strategies, differing from the open-water predation of fish, which is largely limited to times of sufficient light for visual feeding.

As coral populations decline due to habitat degradation, climate change, and other stressors (Donovan et al., 2021; Gutierrez et al., 2024; Hughes et al., 2017), the total volume of released gametes also decreases. If invertebrate predator populations remain stable or even increase due to shifts in reef community structure, their relative impact on fertilization success could grow disproportionately, especially if selective predation occurs (e.g., targeting gamete bundles or only eggs rather than sperm), potentially driving the sperm-to-egg ratio away from optimal levels (Nozawa et al., 2015; Oliver & Babcock, 1992; Teo & Todd, 2018). Such dynamics may exacerbate Allee effects, with profound consequences for coral reproductive success and resilience (Chamberland et al., 2017; Mumby et al., 2024; Shlesinger & Loya, 2019b). The extent to which invertebrate predation reduces reproductive success remains unknown, but unlike the more conspicuous, crepuscular predation by fish, invertebrate predators remain active throughout the night. This suggests a more prolonged and pervasive predation pressure than previously assumed. Moreover, if nighttime spawning evolved primarily to evade predation, the potentially substantial nocturnal activity of cryptic invertebrate predators raises the possibility that nighttime spawning may have also evolved, at least in part, to protect delicate gametes from damaging daytime radiation (Wellington & Fitt, 2003).

The overlooked role of invertebrates as gamete consumers suggests that coral spawn is a more integral part of reef trophic networks than recognized, especially in regions where coral populations or communities spawn over extended periods (Chamberland et al., 2017; Gouezo et al., 2020; Jamodiong et al., 2018; Mangubhai & Harrison, 2008; Shlesinger & Loya, 1985, 2019b; Wild et al., 2004). The transfer of energy and material from coral gametes to diverse reef organisms underscores unappreciated food web connections, highlighting the importance of nocturnal research in ecology. Many aspects of reef life remain hidden in darkness, and cryptic interactions such as these often go unnoticed without dedicated nocturnal studies. While fish predation on coral spawn is well recognized, invertebrate predators may also exert a substantial impact due to their sustained presence throughout the night. These observations highlight fundamental gaps in our understanding of reef dynamics. Coral reefs are intricate ecosystems, and the interactions governing their resilience remain far from fully understood.

The author declares no conflicts of interest.