Sea urchins are an important structuring force in the marine ecosystems worldwide. The herbivory exerted by several species of these echinoderms typically plays a relevant role in their community structure by controlling algae distribution, composition, and biomass (Lawrence, 1975; Lessios et al. 1984; Harrold and Pearse, 1987). The relevance of sea urchin’s role in the community becomes more evident when large variations in sea urchin densities occur, both when large events of "die-offs" or "outbreaks" affect their populations (Lessios et al. 1984; Uthicke et al. 2009; Sangil and Hernández, 2022). Depending on the size of the sea urchin density changes and the resilience and hysteresis of the system, these events may act as key transition points between alternate-stable states, such as macroalgae beds or barren grounds, mainly dominated by crustose coralline algae (CCA) (Ling et al. 2015). The relationships between sea urchin density and algal communities are typically non-linear, and transitions between macroalgal and barren states usually occur when sea urchin abundance reaches a determined threshold. This threshold is typically higher than the density necessary to maintain an overgrazed rocky bottom (Scheffer and Carpenter, 2003; Ling et al. 2015).
Once the ecosystem shifts into a new state, it is common to observe changes not only in the algal community, but also in their species composition and interactions. These changes may promote positive feedback mechanisms that can lead to the persistence of a new state over time, even when the initial conditions are restored (i.e., hysteresis) (Steneck, 1998; Guidetti and Sala, 2007; Baskett and Salomon, 2010; Bonaviri et al. 2012). Some of these mechanisms have been studied extensively over the past few decades. For instance, macroalgal beds can be sustained by different species of predators and micropredators, which prevents demographic explosions of sea urchins (Hernández et al. 2010; Jennings and Hunt, 2011; Bonaviri et al. 2012; Filbee-Dexter and Scheibling, 2014; Ling et al. 2015; Glasby and Gibon, 2020). On the other hand, barren grounds can be maintained through mechanisms such as diet switches of sea urchins, their plasticity to modify their sizes according to population density, or by the facilitation of juvenile sea urchin survivorship due to the refugia offered by the adult sea urchin spine canopy (Chapman, 1981; Andrew and Choat, 1985; Zhang et al. 2011; Cabanillas-Terán et al. 2015).
On the Canary Islands, an archipelago located in the Eastern Atlantic, the sea urchin Diadema africanum (Rodríguez, Hernández, Clemente and Coppard, 2013), plays a key role in wave-protected subtidal rocky bottoms by regulating the alternance between macroalgal beds and barren grounds (Hernández et al. 2008a). The desirable macroalgal beds represent a crucial energy source that supports the local food web in the archipielago. When these systems reach maturity, they often show a predominance of the brown algae Lobophora schneideri, an ecosystem engineer known for enhancing the richness of invertebrates and fish (Tuya et al. 2004; Hernández et al. 2008a, b; Sangil et al. 2014a). In contrast, D. africanum densities of 4 ind/m2 are sufficient to promote and sustain the undesirable barren states. This community encompasses large extensions of hard substrates dominated by CCA, such as Hydrolithon and Neogonolithon, and is characterized by maintain low levels of primary productivity and species richness (Tuya et al. 2004; Hernández et al. 2008a; Ortega et al. 2009; Sangil et al. 2014a, b). The ongoing rise in sea surface temperature, which has been linked to increased settlement pulses and post-settlement survival of D. africanum, coupled with the depletion of sea urchin predators due to overfishing, have been suggested as the primary factors driving the progressive expansion of barren states associated with this key herbivore in the archipelago over the last decades (Aguilera et al. 1994; Casañas et al. 1998; Brito et al. 2004; Hernández et al. 2010, 2017; Vieira et al. 2020). However, in 2010 and 2018, barren grounds in the Canaries showed several signs of decline when recurrent mass mortality events affecting D. africanum decimated their populations by 99% (Clemente et al. 2014; Hernández et al. 2020a). Subsequently, the drastic diminution in the abundances of this key herbivore prompted a new phase shift towards macroalgal beds (Sangil and Hernández, 2022). The effects that this phase shift may have over the population dynamics of this key echinoid remains unclear, but prior to these events, notable differences in juvenile D. africanum abundance between barren grounds and macroalgal/seagrass beds under similar larval supply conditions were observed (Clemente et al. 2009; García-Sanz et al. 2014). This may be suggesting that early life processes linked to alternative stable states can play a role in controlling D. africanum populations.
D. africanum is known to produce high-energy eggs, which may provide them with the ability to survive in the oligotrophic waters of the archipelago during their planktotrophic phase, which lasts for approximately 40 days and facilitates long-distance dispersal across the open ocean until they are ready to settle (Hernández et al. 2020b). This settlement phase encompasses all the processes necessary for the transition from pelagic to benthic life, including substrate selection and metamorphosis. Certain algal species, such as CCAs, are able to have a great influence on the sea urchin settlement phase, by providing competent larvae with appropriate cues to initiate settlement (Pearce and Scheibling, 1990; Huggett et al. 2006; Swanson et al. 2006; Dworjanyn and Pirozzi, 2008; Pilnick et al. 2023; Wijers et al. 2024). Conversely, although lesser studied, some algal species are able to constrain sea urchin settlement success due to the release of toxic compounds (Norris and Fernical, 1982; Agatsuma et al. 2008; Li et al. 2011; Wijers et al. 2024). Once settlement and metamorphosis are completed, early sea urchin recruits still have a long path before reaching adulthood, becoming less vulnerable to predation and acquiring the capacity to reproduce in the process.
Given the importance of this early phases on determine adult densities of sea urchins (Rowley, 1989), it stands to reason that the unprecedented phase shift towards macroalgae beds driven by the mass mortalities of D. africanum could be affecting the population dynamics of this species. For example, macroalgal beds and barren grounds may exhibit different settlement rates of D. africanum due to the differences in the availability of potential settlement cues. Additionally, these distinct macroalgal communities, which host contrasting predatory guilds, may have different influences on the early benthic ecology of this species.. For example, considering the observed susceptibility of D. africanum to predation at small sizes (Clemente et al. 2007), it is possible that micropredation on early settlers could represent a significant bottleneck for this sea urchin population dynamics, as has been suggested for other species (McNaught, 1999; Balch and Scheibling, 2000; Williams et al. 2010; Bonaviri et al. 2012).
In this context, by using modified artificial larval collectors in the field, we aimed to assess the influence of two benthic mature community algae, Lobophora schneideri and encrusting coralline algae, both representative of macroalgal and barren states, respectively, on the settlement rates of D. africanum. Additionally, we explored possible correlations with decapods that could act as predators of D. africanum settlers, thereby providing new perspectives for understanding the stability of the shallow rocky benthic community in the Canary Islands.