One on Top of the Other: Exploring the Habitat Cascades Phenomenon in Iconic Biogenic Marine Habitats

Abstract

Biogenic habitats often form hot spots of biodiversity. However, the role of epibiosis and the ‘habitat cascades’ phenomenon in enhancing structural heterogeneity and biodiversity in biogenic habitats in remote and difficult-to-access areas is little known. In this work, we provide the first insight by exploring epibiosis across remote habitats that often support high levels of biodiversity, i.e., cold-water coral reefs and marine caves. The present study acts as a stepping-stone for the further exploration of ‘habitat cascades’ in habitats where scientific knowledge about this phenomenon is limited.

Over the last couple of decades, studies in terrestrial and shallow-water ecosystems (kelp forests and sandy seagrass beds) unraveled and described a novel phenomenon titled ‘habitat cascades’ [1]. Habitat cascades occur when there are indirect positive effects on focal organisms mediated by successive biogenic formation or habitat modification formed by basal and intermediate habitat formers [1]. Habitat cascades are a mechanism that enhances species abundance and diversity [1]. However, apart from kelp forests and seagrass beds, it is largely unknown if habitat cascades are present in other ecosystems, e.g., hard biogenic habitats, and what their role is in biodiversity [2]. This major knowledge gap is even larger for ‘dark habitats’ such as remote deep-sea ecosystems (e.g., cold-water coral reefs) and marine caves, even though these ecosystems are often regarded as hot spots of marine biodiversity [3,4,5].

It was only recently that studies by Kazanidis et al. [6,7] showed that habitat cascades were present in the Mingulay Reef Complex, a cold-water coral reef formed by the scleractinian coral Lophelia pertusa (Linnaeus, 1758), now known as Desmophyllum pertusum (Linnaeus, 1758), which acts as a basal habitat former and hosts intermediate habitat formers [3,4]. Kazanidis et al. [6] showed that a small group of intermediate habitat formers composed of bivalves, tunicates and empty polychaete tubes was colonized by diverse epifaunal communities of focal organisms mainly composed of bryozoans, molluscs and barnacles. Based on these findings, it was suggested that the intermediate habitat formers (bivalves, tunicates and empty polychaete tubes) increased habitat heterogeneity and enhanced biodiversity through habitat cascades [6] (

Table 1. Examples of hard-substrate habitat cascades in dark marine habitats.

Habitat (Region)	Habitat Cascades: Basal Habitat Formers → Intermediate Habitat Formers → Focal Organisms
Cold-water coral reefs (Mingulay Reef Complex, NE Atlantic)	Cold-water corals → Molluscs → Bryozoans, brachiopods Cold-water corals → Serpulid polychaetes → Barnacles, bryozoans Cold-water corals → Eunicid polychaetes → Anthozoans, tunicates
Biogenic stalactites in marine caves (Mediterranean Sea)	Serpulid polychaetes → Other serpulids and encrusting bryozoans → Epibiota (e.g., sponges, brachiopods, foraminiferans)
	Serpulid polychaetes → Other serpulids and encrusting bryozoans → Cavity-dwelling taxa (e.g., insinuating/boring sponges, boring bivalves, heterotrophic bacterial communities)

) in a similar way that epiphytes do in tropical rainforests [8]. At shallower depths, the serpulid polychaete Protula tubularia (Montagu, 1803) has been found to form a core of aggregates, also known as ‘biostalactites’, which so far have been discovered in the marine caves of Italy, Greece and Cyprus in the Mediterranean Sea [9,10,11,12,13]. These biogenic formations act as the basal habitat former and provide the substrate for intermediate habitat formers such as other serpulids and encrusting bryozoans, which in turn can be covered by epibionts (e.g., sponges, brachiopods and foraminiferans). The cavities of the framework formed by the basal and intermediate formers could also be subsequently colonized by focal cavity-dwelling taxa (e.g., sponges and bivalves), which play an active role in the bioconstruction process [12,14,15] (Table 1). Some mobile taxa could also possibly shelter in the microcavities of these frameworks. These bioconstructions represent ideal niches also for heterotrophic bacterial communities (e.g., sulfate-reducing bacteria) which—fed by organic substances produced mostly by metazoans—develop in the microcavities of the primary framework and, through their metabolic activities, induce micrite deposition. This micrite instantly cements and contributes to strengthening the biostructure [11,12,16,17,18,19]. In the general development of biostalactites, bacteria have a dual role in the frame of the habitat cascades; they act both (1) as focal organisms, as their vital functions depend on the organic matter produced by Protula tubularia (representing the basal habitat former) and serpulids, encrusting bryozoans, sponges, brachiopods and foraminiferans (representing the intermediate formers); and (2) as basal habitat-former organisms, as they form cemented substrates for new generations of epibionts.

Recent studies have advanced scientific knowledge about the role of habitat cascades and especially the role of heterogeneity within and among co-occurring habitat formers in increasing biodiversity in mangroves, seagrasses, marshes, muds and rocky reefs [20]. There are still, however, major knowledge gaps about the habitat cascades phenomenon in remote environments such as marine caves and the deep sea, which is the largest biome on Earth. These gaps hinder an advanced understanding of habitat cascades on a global scale and especially the mechanisms that shape the structure and functioning of biogenic habitats in remote areas, which are often hot spots of marine biodiversity. Some key questions include the following:

(1)

Is the ‘habitat cascades’ phenomenon present in remote areas, and if yes, what is its role in shaping local biodiversity?

(2)

What is the role of environmental parameters (e.g., depth, habitat type, food availability) in the presence and magnitude of habitat cascades?

(3)

Are there common biological traits across the organisms that facilitate habitat cascades across different types of habitats?

In the present study, we provide a series of interesting images showing the habitat cascades phenomenon from two distinct biogenic habitats: the Mingulay cold-water coral reef in Scotland (Figure 1) and marine caves from the Eastern Mediterranean Sea (Figure 2 and Figure 3). The present article is a forerunner and part of a wider examination of habitat cascades’ role in the biodiversity and ecology of hard-substrate biogenic habitats.