Positive species interactions structure rhodolith bed communities at a global scale

Abstract

Rhodolith beds are diverse and globally distributed habitats. Nonetheless, the role of rhodoliths in structuring the associated species community through a hierarchy of positive interactions is yet to be recognised. In this review, we provide evidence that rhodoliths can function as foundation species of multi-level facilitation cascades and, hence, are fundamental for the persistence of hierarchically structured communities within coastal oceans. Rhodoliths generate facilitation cascades by buffering physical stress, reducing consumer pressure and enhancing resource availability. Due to large variations in their shape, size and density, a single rhodolith bed can support multiple taxonomically distant and architecturally distinct habitat-forming species, such as primary producers, sponges or bivalves, thus encompassing a broad range of functional traits and providing a wealth of secondary microhabitat and food resources. In addition, rhodoliths are often mobile, and thus can redistribute associated species, potentially expanding the distribution of species with short-distance dispersal abilities. Key knowledge gaps we have identified include: the experimental assessment of the role of rhodoliths as basal facilitators; the length and temporal stability of facilitation cascades; variations in species interactions within cascades across environmental gradients; and the role of rhodolith beds as climate refugia. Addressing these research priorities will allow the development of evidence-based policy decisions and elevate rhodolith beds within marine conservation strategies.

Keywords: benthic habitats; encrusting coralline algae; facilitation cascades; foundation species; maerl beds; marine biodiversity; rhodoliths.

Fig. 1

(A) Rhodolith beds from the Fernando de Noronha Archipelago, Brazil, ~ 20 m depth (photograph credit: Ronaldo Francini‐Filho). (B) Rhodolith beds from the Madeira Archipelago, Portugal (photograph credit: Pedro Neves). Bottom images illustrate maerl and rhodolith nodules of different shapes (photograph credits: Eli Rinde and João Silva).

Fig. 2

Habitat‐forming species in rhodolith/maerl beds. (A) Laminaria ochroleuca from Galicia, Spain, depth 11 m (photograph credit: Ignacio Bárbara. (B) Diverse macroalgal assemblages supported by rhodoliths at the Fernando de Noronha Archipelago, Brazil, depth 40 m (photograph credit: Zaira Matheus). (C) The tubular sponge, Haliclona simulans, supporting ophiurans, gastropods and hosting cuttlefish eggs in Brittany, France, depth 7 m (photograph credit: Erwan Amice). (D) Unidentified concave sponge from the Fernando de Noronha Archipelago, Brazil, depth 40 m (photograph credit: Zaira Matheus). (E) The bivalve Limaria hians in the north of Norway, depth 15 m (photograph credit: Jason Hall‐Spencer). (F) The flat oyster Ostrea edulis supporting fish spawning, hydroids, seaweeds, encrusting sponges, ascidians and galatheidaes in a maerl bed of Brittany, France, depth 3 m (photograph credit: Erwan Amice).

Fig. 3

Positive interactions within facilitation cascades in rhodolith beds. (A) Rhodoliths (the basal species) promote the establishment of kelp on sedimentary bottoms through the provisioning of hard substrates for attachment. The holdfast, stipe and blades of kelp (secondary facilitator) can provide habitat and/or food to fish and invertebrates, directly or indirectly by supporting epibiota (e.g. macroalgae) that act as tertiary facilitators. (B) Rhodoliths facilitate the establishment of sponges which, in turn, can stabilise beds through the binding of nodules. Sponges (secondary facilitators) can provide habitat for a variety of invertebrates and sustain the growth of macroalgae by recycling nutrients. (C) Bivalves growing on rhodoliths can facilitate invertebrates and macroalgae by providing interstitial or attachment space. In all cases, species at the second or upper level within the facilitation cascade can be used as food by consumers (i.e. herbivores or predators). Arrows show the positive effects of one species on another, with the number of plus signs indicating the level of the facilitative interaction within the cascade. Some of the functions performed by rhodoliths, such as the creation of microhabitat and provisioning of attachment surface, can continue when they are dead (represented in grey); for convenience, dead rhodoliths are illustrated below the living layer, although, in real beds, the surficial layer is often composed of a variable proportion of live and dead nodules. Magnifying lenses provide details of macroalgae and invertebrates supported by secondary facilitators (Illustration by ©Lúcia Antunes, www.luciaantunes.com).

Fig. 4

(A–C) Schematic representation of potential experiments assessing the effects of rhodolith bed traits on associated species. (A) A comparison between live and dead rhodoliths. (B) Comparisons among rhodolith assemblages composed of a different number of species or morphospecies (e.g. natural assemblage versus two‐species assemblages versus monospecific assemblages); in this example, natural rhodolith assemblages are composed of four species across a branching gradient. (C) Comparisons between assemblages composed of the same rhodolith species, but differing in their density (natural versus reduced versus total removal). (D, E) Schematic representation of potential experiments assessing the effects of upper‐level facilitators on rhodoliths and associated assemblages. (D) Different densities of the secondary facilitator (natural versus total removal versus reduced density versus increased density). (E) Different densities of the tertiary facilitator (natural versus total removal versus reduced density versus increased density); in these examples, the secondary and tertiary facilitators are a canopy‐forming and an epiphytic macroalga, respectively. For each of the illustrated experimental tests, double‐headed arrows indicate comparisons with the natural controls and lateral close‐ups represent the response variable/s (the rhodoliths, the canopy‐forming macroalga and the invertebrate assemblage) that can be potentially taken into account to assess positive/negative effects of each of the three levels included in the cascade. The illustrated densities of the basal, secondary and tertiary facilitators are simple examples of possible manipulations which can be extended to the upper levels of a cascade. A detailed account of experimental designs for disentangling the effects of species richness from those of species identity and density can be found in Benedetti‐Cecchi (2004).