Distribution of epiphytic macroalgae on the thalli of their hosts in Cuba

We investigated the distribution of epiphytic macroalgae on the thalli of their hosts at eight localities along the southeastern coast of Cuba between June 2010 and March 2011. We divided he epiphytes in two groups according to their distribution on the host: those at the base of the thallus and those on its surface. We determining the dissimilarity between the zones and the species involved. We identified 102 taxa of epiphytic macroalgae. There were significant differences between the two zones. In 31 hosts, the number of epiphytes was higher on the surface of the thallus, whereas the number of epiphytes was higher at the thallus base in 25 hosts, and the epiphytes were equally distributed between the two zones in five hosts (R=−0.001, p=0.398). The mean dissimilarity between the two zones, in terms of the species composition of the epiphytic macroalgae, was 96.64%. Hydrolithon farinosum and Polysiphonia atlantica accounted for 43.76% of the dissimilarity. Among macroalgae, the structure of the thallus seems to be a determinant of their viability as hosts for epiphytes.


Introduction
The structure of intertidal marine communities is determined by a combination of physical factors and biotic interactions (Little & Kitching 1996;Wernberg & Connell 2008).The establishment of marine macroalgae involves a number of complex physical interactions, as well as biological, ecological and chemical processes at the microscale, from the release of propagules by reproductive adults to their migration to appropriate substrates, initial adhesion to a surface, permanent attachment and development (Reed 1990a;Brawley & Johnson 1992;Vreeland & Epstein 1996).Because macroalgae constitute a key component of coastal communities, they are associated with other organisms and processes and have been central to the debate about the nature and scope of the structure and dynamics of those communities (Foster 1990(Foster , 1991;;Paine 1991;Underwood 2000).
In the intertidal zone, environmental gradients also occur at smaller scales, such as within the host zone of receptivity, where there is a light intensity gradient between the periphery and the interior of the thallus, and along host fronds, where there is a gradient in biomass, which decreases progressively from the holdfast to the frond tip.The investigation of the distribution of epiphytes at different scales is a potentially productive approach.It is important to understand the patterns of abundance of all sympatric epiphytic species along the various gradients, because interspecific relationships could represent one of the factors that explain their distribution (Longtin et al. 2009).
The texture and structure of the host thalli are frequently exploited by epiphytes, thus increasing habitat complexity (Hacker & Steneck 1990).The epiphytic macroalgae with a filamentous or branched structure usually present a high degree of structural complexity and might therefore increase the suitability of host algae as habitats for mesoherbivores (Martin-Smith 1993).
In marine communities, the plant substrates that are the most widely colonized by are seagrasses and macroalgae, because they provide the necessary space, shelter and nutrition (Aguilar-Rosas & Galindo 1990).Macroalgae morphology might be related to the density of the community (Reed 1990b;Ang & DeWreede 1992).High densities of adults can help reduce desiccation during low tide due to overlapping thalli, as well as reducing water flow, providing shade and microhabitats below, which can affect the structure of the community (Bruno et al. 2003).
The host macroalgae differ considerably in their suitability as substrates for epiphytes.This difference might be related to the longevity of the species, which is a determining factor in the process of substrate colonization by epiphytes; in some cases, this phenomenon is more evident in the older parts of the thallus (Aguilar-Rosas & Galindo 1990).In Zostera noltii, Lebreton et al. (2009) found that the number of diatoms was higher on young leaves than on old leaves.
The suitability of macroalgae as substrates for epiphytes can also vary depending on the morphological characteristics of the base; the degree of branching; the roughness and texture of the surface; the production of allelopathic substances such as mucilage; and the thallus growth rate (Lobban & Harrison 1997).When the thallus surface has little mucilage, it provides favorable conditions for the establishment of epiphytes (Paula & Oliveira-Filho 1980;Széchy et al. 2006).
In tropical and subtropical regions, studies have shown reductions in the size of communities that develop on rocky shores, especially communities of macroalgae and epiphytes.Such studies have been limited to identifying epiphytic macroalgae species without studying the basic aspects of their ecology (Aguilar et al. 1998;Saad-Navarro & Riosmena-Rodrígez 2005).Understanding the spatial scales at which the rocky intertidal zone communities vary provides the necessary information to initiate the study of the relative importance of the various factors that can affect these communities and how those factors interact (Underwood et. al. 2000).Therefore, the objective of the present study was to determine the distribution of epiphytic macroalgae on the thallus of their hosts.

Study area
The study was conducted in the rocky intertidal zone between the municipalities of Aguadores and Baconao, Cuba, within the Baconao Biosphere Reserve (Managed Resource Protected Area), at eight locations (Fig. 1.): Aguadores 1, Aguadores 2; Sardinero; Juticí; Cajobabo; Verraco, Acuario and Baconao.Located east of the city of Santiago de Cuba, the study zone occupies an area of 5635 hectares of sea on the southeastern coast of the country, between Maisí and Cabo Cruz.It is characterized by a rocky intertidal zone with extensive fields of limestone (surface karst formation).

Sampling design
Samples were collected on a quarterly basis between June 2010 and March 2011, although inclement weather precluded sample collection in the month of September.Therefore, with the aim of collecting the greatest number of epiphytic species (Lecha & Chugaev 1989), we performed three samplings: one during the rainy season (in June); and two during the dry season (in December and in March).Samples were collected at low tide in the intertidal zone, which is characterized by short intervals of immersion and emersion.
We collected all epiphytic macroalgae and their hosts in 15 square metal containers (25 cm × 25 cm × 25 cm) distributed at random (Jover et al. 2012).All macroalgae that were growing on other macroalgae were classified as epiphytes, according to the criteria of Borowitzka et al. (2006).In accordance with Montañés et al. (2003), the epiphytic macroalgae were separated into two groups by their location on the thallus of the host: at the base or on the surface.The morphofunctional classification of the groups followed the criteria established by Littler & Littler (1984) and Steneck & Dethier (1994).

Data analysis
For each host macroalga and each zone of the thallus, we determined epiphyte species richness on the basis of the number of species observed (Ludwing & Reynolds 1988).
The origin and significance of differences between the zones of the host thalli were determined by analysis of similarity, with 999,999 permutations applied to the similarity matrix (Clarke & Warwick 2001).The similarity matrix was derived from the species presence and absence data using the Jaccard index.The principal species responsible for the dissimilarity were identified by similarity percentage analysis (Clarke 1993).These nonparametric multivariate tests were conducted with the statistical program Primer, version 6 (Clarke & Gorley 2006).

Epiphytic macroalgae and their hosts: flora
The observed number in the rocky intertidal zone of the Aguadores-Baconao sector, we observed 102 taxa of epiphytic macroalgae (18 Phaeophyceae, 53 Rhodophyceae and 31 Chlorophyceae), belonging to 14 orders, 25 families and 52 genera.The most well-represented order was Ceramiales, with 30 species, accounting for 29.4% of the total.Among the Phaeophyceae and Chlorophyceae, respectively, the most well-represented orders were Dictyotales and Cladophorales, with 13 species each.
Among the host macroalgae, we identified 61 taxa: 17 Phaeophyceae, 25 Rhodophyceae and 19 Chlorophyceae, belonging to 14 orders, 23 families and 39 genera.The most well-represented orders were Dictyotales and Ceramiales, with 11 species each.The orders Cladophorales and Siphonocladales presented six species each.The Phaeophyceae genus Dictyota presented the greatest number of species, with six.

Distribution of epiphytic macroalgae on the host thalli
The distribution of epiphytes on the host thalli varied considerably.In 31 host species, the number epiphyte species was higher on the surface of the thallus than at its base, whereas the inverse was observed in 25, and the number epiphyte species was comparable between the two zones in five host species.Epiphytes were located only on the surface of the thallus in nine host species and only at its base in three.The cumulative species richness (both zones) was 89 species.The greatest epiphyte species richness was recorded for macroalgae with thalli that were more complex, belonging to the corticated, leathery, leafy and globose morphofunctional groups (Tab.1).
The total R value for the comparison between the two areas was −0.001 (p=0.398).The mean dissimilarity between the surface and the base of the host thallus, in terms of the species composition of epiphytic macroalgae, was 96.64%.The species Hydrolithon farinosum (J.V.Lamouroux) D.Penrose & Y.M.Chamberlain and Polysiphonia atlantica Kapraun & J.N.Norris accounted for 43.76% of the dissimilarity.
The species that accounted for the majority of the mean similarity among epiphytic macroalgae at the base of the host thallus (2.99%) was Hydrolithon farinosum, which accounted for 59.36%.In addition, H. farinosum accounted for 92.37% of the mean similarity among epiphytic macroalgae on the surface of the host thallus (4.51%).
The following were the most common species occurring on the surface of the thallus: Padina sanctae-crucis Børgesen

Epiphytic macroalgae and their hosts: typical flora
The 102 taxa of epiphytic macroalgae observed here correspond to 21% of those identified for the waters of Cuba, whereas the host species correspond to 12.5% (Suárez 2005).The level of species richness observed here was high in comparison with those previously reported for Cuban waters.That might be due, in part, to the community approach taken in our study of the hosts, given that the majority of investigations of the hosts of epiphytic macroalgae have been conducted at the population level.
The greater epiphyte richness observed among hosts belonging to the morphofunctional groups with higher thallus complexity is due to the fact that those groups present morphological differences among their component species, which makes them responsible for increasing the spatial heterogeneity of the community.In addition, species with differentiated blades and thalli have greater morphological complexity, are more resistant to adverse conditions and confer greater stability upon the community (Littler & Littler 1980;1984).

Distribution of epiphytic macroalgae on the host thallus
Greater epiphyte species richness on the surface of the thallus might be determined by the protection that provides against the extreme conditions in the intertidal zone, such as desiccation and wave exposure, as well as avoiding the competition for light that could lead to the overlapping of host thalli.In turn, macroalgae hosts with more epiphytes at the thallus base could better withstand those adversities and tolerate competition for light.The various structures that give rise to the thalli differ in terms of desiccation and solar irradiation.Longtin et al. (2009) found that these two factors were more intense in the distal segments of the thallus than at its base.
The variation in the accumulated epiphyte species richness in the rocky intertidal zone at the Aguadores-Baconao site is related to the complexity, rather than the zonation, of the host thalli.Montañés et al. (2003) argued that not only the habits but also the organizational type of epiphytes directly conditions their adhesion sites and preference for Acta bot.bras.27(4): 815-826.2013.different parts of the host.The morphology of the host thallus is also crucial, it is expected that structurally complex thalli favor colonization by a greater number of epiphytes, because they create a greater number of niches and shelters (Ayala & Martín 2003).Apparently morphologically complex thalli, such as those of leathery corticate algae, create protected microhabitats (Kendrick & Burt 1997;Lavery & Vanderklift 2002).In addition, the texture and structure of the thalli are frequently used by epiphytes, increasing the complexity of the habitat (Hacker & Steneck 1990).
The fact that the similarity in overall shape was near zero indicates no difference in the distribution of epiphytic macroalgae, which might be attributable to the similarity between the base of the thallus and its surface, in terms of epiphyte species richness.However, the dissimilarity values are very high, given the existence of quite significant differences in epiphyte species composition and in the proportional contributions of individual species.
Species such as Hydrolithon farinosum, Centroceras clavulatum and Cladophora albida showed no preference for any specific area of the host thallus, presenting high values of frequency of appearance at its base and on its surface.This behavior could be determined by the low complexity of the host thalli, given the possibility that the developmental requirements of those species might not be as specific as are those of other epiphytes.
The hosts that did not have epiphytes adhering to the thallus base were typically the simpler forms, with few occurrences during the sampling periods.Macroalgae that host a great number of epiphytes in general or at the thallus base might have greater viability in the ecosystem, as has been suggested by various authors (Davis et al. 1989;Wahl 1989).The significantly low number of species hosting epiphytes of the thallus surface might be attributable to the epiphytes having a preference for zones that provide more light and more nutrients (Pedersen & Borum 1996;Lobban & Harrison 1997;Kraberg & Norton 2007).Ulva flexuosa and Bryopsis plumosa both present thalli that are structurally simple, with very smooth blade surfaces.
We conclude that the development of epiphytes can be influenced not only by the extreme physical conditions in the rocky intertidal zone but also by the structural characteristics of the host thalli and of the epiphytes, their ability to adhere to other macroalgae thalli or allow their own thalli to be adhered to by others.

Figure 1 .
Figure 1.Location of the Aguadores-Baconao coastal sector and of the individual sampling sites.

Table 1 .
Characteristics of the macroalgae hosting epiphytic macroalgae, including morphofunctional group, thallus zone in which the epiphytes were found, and epiphyte species composition, in a rocky intertidal zone in the Baconao Biosphere Reserve, in Cuba.

Table 1 .
For the names of the species corresponding to the numbers shown, see the taxonomic list in the Results section.Continuation. *