Davide Maggioni

New insights into the symbiosis between zanclea (cnidaria, hydrozoa) and scleractinians

Hydroids in the genus Zanclea are a recently discovered component of the fauna associated with reef‐building corals. The phylogenetic relationships among these species are not well known. The present work is based on field surveys in the Republic of Maldives, and for the first time, morphological and molecular analyses are integrated to distinguish a new hydroid species and provide new information on the ecology of this symbiosis. This new hydroid, Zanclea gallii sp. n., was associated with the scleractinian Acropora muricata; it was living sympatrically with its congener Zanclea sango, which was observed for the first time at this locality on the new scleractinian host Pavona varians. The relationships between these two hydroids and other available scleractinian‐associated Zanclea were investigated using two molecular markers, nuclear 28S rDNA and mitochondrial 16S rRNA. Zanclea gallii sp. n. and Z. sango were recovered as distinct lineages within a monophyletic group of scleractinian‐associated Zanclea based on both molecular and morphological data. All Zanclea species that were observed living in association with scleractinians belong to the ‘polymorpha group’ and share the morphological characteristic ‘polymorphic colony’. The genus Leptoseris is the 16th host coral identified for Zanclea. Compared with the frequency of the Z. gallii sp. n. association with A. muricata and Z. sango with the scleractinian P. varians, the latter is twice as common; however, the former exhibited higher Zanclea polyps concentrations over the colony surface. Overall, the Zanclea survey indicates that these diminutive hydroids are more commonly associated with coral than previously known.

Zanclea–coral association: new records from Maldives

To date, few hydroids have been observed to be associated with anthozoans, and only three Pacific Zanclea species are known to live in symbiosis with scleractinian corals, namely Zanclea gilii, Z. margaritae, and Z. sango (Boero et al. 2000; Pantos and Bythell 2010; Hirose and Hirose 2011). Here, we report the first evidence of this kind of association in the Indian Ocean. During recent expeditions to Magoodhoo Island (3 04¢N; 72 57¢E, Faafu Atoll, Republic of Maldives), numerous Zanclea spp. colonies wereobserved to live in symbiosis with scleractinians up to about 10 m depth. Specimens belonging to Zanclea spp. were found not only on Acropora muricata and Pavona sp., which are scleractinians previously known to be involved in this association, but also on coral colonies belonging to Favia favus, Favites halicora, Leptastrea purpurea, Montipora sp., Porites cylindrica, and Symphyllia sp. (Fig. 1a–f). Thus, our results extend the geographic distribution and the host range of this symbiosis, strongly suggesting that associations between hydroids and scleractinians could be much more widespread than previously thought, which is consistent with the scenarios depicted by recent molecular studies (Fontana et al. 2012). The benefits and costs of this symbiosis are still not clear. Although trophic and/or protection mutualism seems a plausible explanation of the relationship, a possible relationship between the occurrence of hydroids and coral diseases has also been proposed (Pantos and Bythell 2010). The potential implications of the hydroid–scleractinian symbiosis for coral health, its wide distribution, and the number of species it involves indicate urgent need for further investigations.

The Hidden Diversity of Zanclea Associated with Scleractinians Revealed by Molecular Data

Scleractinian reef corals have recently been acknowledged as the most numerous host group found in association with hydroids belonging to the Zanclea genus. However, knowledge of the molecular phylogenetic relationships among Zanclea species associated with scleractinians is just beginning. This study, using the nuclear 28S rDNA region and the fast-evolving mitochondrial 16S rRNA and COI genes, provides the most comprehensive phylogenetic reconstruction of the genus Zanclea with a particular focus on the genetic diversity among Zanclea specimens associated with 13 scleractinian genera. The monophyly of Zanclea associated with scleractinians was strongly supported in all nuclear and mitochondrial phylogenetic reconstructions. Furthermore, a combined mitochondrial 16S and COI phylogenetic tree revealed a multitude of hidden molecular lineages within this group (Clades I, II, III, V, VI, VII, and VIII), suggesting the existence of both host-generalist and genus-specific lineages of Zanclea associated with scleractinians. In addition to Z. gallii living in association with the genus Acropora, we discovered four well-supported lineages (Clades I, II, III, and VII), each one forming a strict association with a single scleractinian genus, including sequences of Zanclea associated with Montipora from two geographically separated areas (Maldives and Taiwan). Two host-generalist Zanclea lineages were also observed, and one of them was formed by Zanclea specimens symbiotic with seven scleractinian genera (Clade VIII). We also found that the COI gene allows the recognition of separated hidden lineages in agreement with the commonly recommended mitochondrial 16S as a DNA barcoding gene for Hydrozoa and shows reasonable potential for phylogenetic and evolutionary analyses in the genus Zanclea. Finally, as no DNA sequences are available for the majority of the nominal Zanclea species known, we note that they will be necessary to elucidate the diversity of the Zanclea-scleractinian association.

First record of coral-associated Zanclea (Hydrozoa, Zancleidae) from the Red Sea

Although corals are known to host a variety of marine organisms, to date few benthic hydrozoans have been observed to be associated with anthozoans. However, three species belonging to the genus Zanclea have recently been discovered that inhabit reef-building scleractinians. Here we report the first evidence of such Zanclea-coral associations from the Red Sea, extending their known geographical distributions and host range.

A cryptic species in the Pteroclava krempfi species complex (Hydrozoa, Cladocorynidae) revealed in the Caribbean

Symbiotic relationships on coral reefs involving benthic hosts other than scleractinian corals have been poorly investigated. The hydroid Pteroclava krempfi is a widespread species known to be mainly associated with alcyonacean octocorals in the Indo-Pacific. In the present study, P. krempfi was discovered in association with octocorals of the genus Antillogorgia (Gorgoniidae) at two localities in the Caribbean Sea (St. Eustatius in the eastern Caribbean and Bocas del Toro in the western part), updating its host range with an additional genus and family. The Caribbean specimens showed no morphological differences and the shape of their polyps was consistent with the original P. krempfi description. A multi-locus phylogeny reconstruction of the P. krempfi species complex based on both mitochondrial and nuclear loci revealed three separate molecular clades. Two of them were composed of P. krempfi associated with the families Plexauridae and Alcyoniidae from the Maldives, whereas a new highly supported molecular lineage included all Caribbean specimens of P. krempfi associated with the family Gorgoniidae. These three divergent molecular clades represent distinct cryptic taxa within the P. krempfi species complex, in which the main interspecific difference consists of their host families.

The cellular stress response of the scleractinian coral Goniopora columna during the progression of the black band disease

Black band disease (BBD) is a widespread coral pathology caused by a microbial consortium dominated by cyanobacteria, which is significantly contributing to the loss of coral cover and diversity worldwide. Since the effects of the BBD pathogens on the physiology and cellular stress response of coral polyps appear almost unknown, the expression of some molecular biomarkers, such as Hsp70, Hsp60, HO-1, and MnSOD, was analyzed in the apparently healthy tissues of Goniopora columna located at different distances from the infection and during two disease development stages. All the biomarkers displayed different levels of expression between healthy and diseased colonies. In the healthy corals, low basal levels were found stable over time in different parts of the same colony. On the contrary, in the diseased colonies, a strong up-regulation of all the biomarkers was observed in all the tissues surrounding the infection, which suffered an oxidative stress probably generated by the alternation, at the progression front of the disease, of conditions of oxygen supersaturation and hypoxia/anoxia, and by the production of the cyanotoxin microcystin by the BBD cyanobacteria. Furthermore, in the infected colonies, the expression of all the biomarkers appeared significantly affected by the development stage of the disease. In conclusion, our approach may constitute a useful diagnostic tool, since the cellular stress response of corals is activated before the pathogens colonize the tissues, and expands the current knowledge of the mechanisms controlling the host responses to infection in corals.

Molecular evidence for cryptic species in Pteroclava krempfi (Hydrozoa, Cladocorynidae) living in association with alcyonaceans

Hydrozoans are able to establish intimate relationships with several other organisms. The hydroid Pteroclava krempfi lives in association with different alcyonacean taxa from Indo-Pacific and Atlantic coral reefs, growing partially embedded within host tissues. In this study, we found P. krempfi associated with four alcyonacean hosts from the Maldives, namely Sinularia, Sarcophyton, Lobophytum and Paraplexaura, the latter representing a new record. We provided the first molecular phylogenetic evaluation of the genus Pteroclava. Pteroclava krempfi clustered with Cladocoryne floccosa, confirming its position into the family Cladocorynidae. We also performed the first morpho-molecular assessment of P. krempfi diversity. All the colonies growing on different hosts revealed polyps and medusae matching published descriptions of P. krempfi, showing no morphological differences. However, analysing both nuclear and mitochondrial DNA, two highly supported molecular lineages were identified. These two clades were highly divergent and were specifically associated with hosts belonging to different families (Alcyoniidae and Plexauridae). Therefore, our results suggest that P. krempfi from the Maldives is a complex of cryptic species in which the main diagnostic feature between different species could be the host specificity.

Widespread occurrence of coral diseases in the central Maldives

Coral diseases are one of the most important causes of coral reef decline worldwide. Although they are well investigated in some areas of the Caribbean and the Great Barrier Reef, they have been poorly studied in the Indian Ocean, and particularly in the Maldives, where the presence of coral pathologies has been reported only recently. In order to fill this gap, we investigated the prevalence, local host range and distribution of five coral diseases, namely brown band disease, skeleton eroding band, black band disease (BBD), ulcerative white spot and white syndrome (WS), in the central part of the Maldivian Archipelago, focussing, in particular, on the dominant coral genus Acropora. We estimated an overall disease prevalence of approximately 1.51%. Male North Atoll was the most affected area; however, coral diseases were present at all study sites. WS was the most widespread disease, whereas BBD affected the highest number of scleractinian genera. We found symptoms of disease on 18 genera belonging to eight families. Acropora was the most affected genus in terms of pathogen diversity. These results provide baseline disease levels for the Maldives and can therefore serve as gauge for monitoring future change.

Slow progression of black band disease in Goniopora cf. columna colonies may promote its persistence in a coral community

Coral diseases have been little investigated in the Indian Ocean and especially in the Republic of Maldives, where they were firstly observed in 2010. Through repeated monitoring, we observed a peculiar slow progression of Black Band Disease in several large colonies of the reef-building coral Goniopora cf. columna in the Maldivian reefs of Magoodhoo Island (Faafu Atoll). We argue that this may ensure the local persistence of the disease, possibly promoting long-term mortality of other, more susceptible coral species.

Pteroclava krempfi-octocoral symbiosis: new information from the Indian Ocean and the Red Sea

Some hydroids are known to form strict relationships with anthozoans. In this study we report the first evidence of the association between Pteroclava krempfi (Hydrozoa: Capitata: Cladocorynidae) and octocorals of the alcyonacean genera Sarcophyton, Lobophytum and Sinularia observed in the Republic of Maldives and in the Red Sea. Our observations contribute to an expansion of both the recorded host-range and geographical distribution of this symbiosis, indicating that the association between hydroids and alcyonaceans is more widespread than previously known.