Positive cascading effects of epiphytes enhance the persistence of a habitat‐forming macroalga and the biodiversity of the associated invertebrate community under increasing stress

Abstract

Enhanced persistence of stress sensitive species in harsh environments due to amelioration of physical stress by habitat‐forming species has been widely documented. By contrast, less attention has been given to positive species interactions that may enhance stress tolerance in habitat‐forming species, with positive cascading effects on biodiversity and ecosystem functioning. We used a combination of field surveys and experiments to assess the effects of the epiphyte Jania rubens, on its subtidal macroalgal host Halopithys incurva, and their cascading effects on the associated invertebrate community, along a depth gradient associated with increasing stress (i.e. light stress at shallower depths). Correlative studies showed that the biomass and photosynthetic efficiency of H. incurva increased with depth, along with a decrease of epiphyte biomass. The experimental manipulation of epiphytes (removal in shallow water and addition in deep water) revealed that their effects on H. incurva physiology varied from positive in shallow habitats to negative in deep habitats. These results suggest that reduction of light/UV stress by J. rubens allows H. incurva to persist in shallow‐water habitats that would be otherwise unsuitable. In addition, colonization by large clumps of J. rubens increased the abundance and diversity of associated invertebrates in shallow habitat, suggesting that positive feedbacks between H. incurva, acting as the primary habitat‐former, and J. rubens, acting as a secondary habitat‐former, generate a facilitation cascade. Synthesis. Our study suggests that the persistence of some habitat‐forming species and their ability to support biodiversity may rely upon physical stress reduction by other species (e.g. epiphytes in our case) that are generally neglected when planning conservation strategies. A deeper understanding of context dependency in positive species interactions is essential for predicting patterns of species distribution under increasingly stressful climate scenarios.

Habitat‐complexity regulates the intensity of facilitation along an environmental stress gradient

“…Specifically, our results highlight that an increase on the relative importance of foundation species towards stressful environmental conditions does not always hold true (Meysick et al 2019). Mechanisms responsible for the facilitative effect are often context‐dependent (McAfee and Bishop 2019, Ravaglioli et al 2020, Uyà et al 2019) and, as demonstrated here, understanding the interplay among facilitator traits and environmental stress likely has important consequences for the importance and intensity of positive interactions. Understanding these relationships and under what conditions habitat‐forming species provide the most benefit to associated biodiversity is essential given their critical role in environmental management.…”

“…When interacting species have similar means of resource acquisition, a shift in the direction of the interaction along environmental stress gradients is often observed (Callaway et al 2002, Maestre et al 2009, Bulleri et al 2011). For example, plant–plant interactions often shift from competition to facilitation with increasing environmental stress (Maestre et al 2009, Song et al 2019, Ravaglioli et al 2020). However, foundation species and their associated fauna often belong to different trophic levels and, in such cases, direct negative effects through competition are negligible or absent.…”

Experimental evidence root‐associated microbes mediate seagrass response to environmental stress

“…The stress-gradient hypothesis has traditionally been applied to explain interactions among plant species which often shift from competition to facilitation with increasing environmental stress (Baumeister & Callaway, 2006;Callaway, 2007). More recently, the principle has been applied to habitat-biodiversity relationships, where the facilitative effects of key habitat-forming species increase with increasing environmental stress (Ravaglioli et al, 2021;Wright & Gribben, 2017). Emerging evidence suggests that interactions between terrestrial plants and micro-organisms may also become more positive under stress (Rutten & Gómez-Aparicio, 2018), although results in this emerging area are equivocal (David et al, 2018(David et al, , 2020).…”

Facilitation of animals is stronger during summer marine heatwaves and around morphologically complex foundation species

“…Processes that control community dynamics are context dependent, making it a challenge to rank ecological test-factors according to their relative importance and discover general ecological rules (Lawton, 1999). However, by using a four-factorial experimental approach we could identify context dependency (i.e., signifi- and the environmental conditions associated with seasonality, intertidal elevation, subtidal depth, and latitude (Angelini et al, 2015;Bishop et al, 2012;Navarro-Mayoral et al, 2020;Ravaglioli et al, 2021;Thomsen et al, 2016). For example, Navarro-Mayoral et al, (2020) showed that epifauna were more diverse and abundant in summer and in shallow habitat compared to winter and deep habitats, likely because secondary foundation species were more common under the former conditions.…”

“…Today, facilitation of animals from co‐occurring foundation species has been documented across habitats, ecosystems, and bioregions (Angelini et al, 2011 ; Kazanidis et al, 2022 ; Thomsen et al 2018b ). It has also been shown that facilitation of animals can vary with the density of the foundation species, the elevation and latitudes where the foundation species live (Angelini et al, 2015 ; Bishop et al, 2012 ; Ravaglioli et al, 2021 ), and the morphological complexity of the co‐occurring foundation species (Thomsen et al, 2022 ). However, little is known about the temporal dynamics of facilitation of animals associated with co‐occurring foundation species, e.g., if facilitation changes within and between seasons (Gribben et al, 2019 ; Smith et al, 2023 ) or during periods of unusually high temperature (Chen et al 2021b ).…”