Results

Publications

2017

D. Cepeda, D. Martin, T.A. Britayev, A.M. Al-Aidaroos & P. Lattig. A new species of Haplosyllis (Annelida: Syllidae) from Saudi Arabian Red Sea, with new data on H. eldagainoae and a dichotomous key of the Indo-Pacific species. Mar Biodiv. DOI: 10.1007/s12526-017-0675-6.
ABSTRACT

Knowledge of the Haplosyllis species in the Saudi Arabian Red Sea is rather limited, since the so-called cosmopolitan Haplosyllis spongicola and Haplosyllis djiboutiensis apparently present all along the region are the only reported species. However, both are revealed to be species-complexes, the former mostly composed of European species and the later distributed in the Indo-Pacific area. Recently, several new species have been described following more comprehensive taxonomic studies in the respective areas. Haplosyllis leylae sp. nov. can be framed within the "djiboutiensis" complex. The new species, which is herein fully described and illustrated, can be clearly distinguished by the combined presence of numerous small dorsal granules, the low number of articles on each dorsal cirrus, and the chaetal morphology. A dichotomous key of the Indo-Pacific species of Haplosyllis and new information on Haplosyllis eldagainoae are also included.

T.A. Britayev, E. Mekhova, Y. Deart & D. Martin. Do syntopic host species harbour similar symbiotic communities? The case of Chaetopterus spp. (Annelida: Chaetopteridae). PeerJ 5: e2930. doi: 10.7717/peerj.2930.
ABSTRACT

To assess whether closely related host species harbour similar symbiotic communities, we studied two polychaetes, Chaetopterus sp. (n = 11) and Chaetopterus cf. appendiculatus (n = 83) living in soft sediments of Nhatrang Bay (South China Sea, Vietnam). The former harboured the porcellanid crabs Polyonyx cf. heok and Polyonyx sp., the pinnotherid crab Tetrias sp. and the tergipedid nudibranch Phestilla sp. The latter harboured the polynoid polychaete Ophthalmonoe pettiboneae, the carapid fish Onuxodon fowleri and the porcellanid crab Eulenaios cometes, all of which, except O. fowleri, seemed to be specialized symbionts. The species richness and mean intensity of the symbionts were higher in Chaetopterus sp. than in C. cf. appendiculatus (1.8 and 1.02 species and 3.0 and 1.05 individuals per host respectively). We suggest that the lower density of Chaetopterus sp. may explain the higher number of associated symbionts observed, as well as the 100% prevalence (69.5% in C. cf. appenciculatus). Most Chaetopterus sp. harboured two symbiotic species, which was extremely rare in C. cf. appendiculatus, suggesting lower interspecific interactions in the former. The crab and nudibranch symbionts of Chaetopterus sp. often shared a host and lived in pairs, thus partitioning resources. This led to the species coexisting in the tubes of Chaetopterus sp., establishing a tightly packed community, indicating high species richness and mean intensity, together with a low species dominance. In contrast, the aggressive, strictly territorial species associated with C. cf. appendiculatus established a symbiotic community strongly dominated by single species and, thus, low species richness and mean intensity. Therefore, we suggest that interspecific interactions are determining species richness, intensity and dominance, while intraspecific interactions are influencing only intensity and abundance. It is possible that species composition may have influenced the differences in community structure observed. We hypothesize that both host species could originally be allopatric. The evolutionary specialization of the symbiotic communities would occur in separated geographical areas, while the posterior disappearance of the existing geographical barriers would lead to the overlapped distribution.

 

G. Fernández-Leborans, S. Román, D. Martin. A new deep-sea suctorian-nematode epibiosis (Loricophrya-Tricoma) from the Blanes submarine canyon (NW Mediterranean). Microbial Ecology. doi:10.1007/s00248-016-0923-5.
ABSTRACT

During a pluri-disciplinary study carried out within the frame of the Spanish research project DOS MARES, multicore samples were collected along the Blanes submarine canyon and its adjacent open slope to study the structure and dynamics of the meiofaunal organisms, mainly nematodes. Among the 5808 nematode individuals identified, only 190 of them belonged to the genus Tricoma (Desmoscolecidae), and only two harboured epibiont suctorian ciliates. The three specimens were located near the tail of the basibionts. A careful examination of the ciliates revealed that they were suctorians, which are here described as a new species of Loricophrya, namely L. mediterranea sp. nov. The new species is characterized by having a conical, slightly elongated lorica, narrowing towards posterior end; an anterior end inward curved, surrounding the lorica opening; a body placed near the lorica opening, occupying 1/3 of the lorica length, 4–8 capitate tentacles, and a peripheral, oval to sausage-shaped macronucleus. Our findings represent the first known report of an association with a deep-sea species of Tricoma, and the first record in the Mediterranean Sea, for a species of Loricophrya. The significance of the relationships between suctorian ciliates and their host in extreme environments such as deep-sea submarine canyons is discussed.

2016

P. Lattig, I. Muñoz, D. Martin, P. Abelló & A. Machodrom. Comparative phylogeography of two symbiotic dorvilleid polychaetes (Iphitime cuenoti and Ophryotrocha mediterranea) with contrasting host and bathymetric patterns. Zoological Journal of the Linnean Society. doi: 10.1111/zoj.12453.
ABSTRACT

Two symbiotic polychaetes living in brachyuran crabs in the western Mediterranean and the nearby eastern Atlantic, Iphitime cuenoti and Ophryotrocha mediterranea, were analysed to determine their phylogeographical patterns and the possible effects of known oceanographic barriers in the study area. The analysed species live in hosts inhabiting well-differentiated depths, a factor that may be crucial for understanding the different patterns observed in each species. Iphitime cuenoti was found in four different host crabs between 100 and 600 m depth and showed some level of genetic homogeneity, reflected in a star-like haplotype network. Furthermore, barrier effects were not observed. By contrast, O. mediterranea was exclusively found in a single host crab species living between 600 and 1200 m depth. Phylogeographical analyses showed two lineages that pre-date the existence of current barriers. The geological history of the study area, including the most recent glaciation events, probably led to a secondary contact between the lineages, thus forming a single metapopulation. The phylogeographical pattern found in each species may be explained by differences in dispersal ability, habitat, and host crab specificity that have led them to be differentially affected by historical events. This study is the first to use a phylogeographical approach on symbiotic polychaetes.

T. N. Molodtsova, T. A. Britayev & D. Martin. Cnidarians and their polychate symbionts. In: Goffredo, S. & Dubinsky, Z. (Eds.) The Cnidaria, past, present and future. The world of Medusa and her sisters. Springer International Publishing, Switzerland. Pp. 1-26. DOI 10.1007/978-3-319-31305-4_25
ABSTRACT

Cnidarians, especially skeleton-bearing anthozoans and hydrocorals, are known to host abundant and diverse symbiotic fauna encompassing members of the majority of metazoan taxa, ranging from sponges and flat worms to fishes. Members of the class Polychaeta are between the most diverse and perhaps the least studied taxa of coral symbionts. The last revision (Martin and Britayev, Oceanogr Mar Biol 36:217–340, 1998) reckoned about 60 species of symbiotic polychaetes associated with more than 100 species of cnidarian hosts. However, this number is considerably underestimated. Some populations of scleractinians, sea fans and black corals show up to 100 % infestation by symbiotic polychaetes. Close association and inter-relation of highly host-specific symbionts and cnidarian hosts often lead to dramatic changes in the host morphology. At the moment, actual mechanisms of most of mutual relations between host and symbiont in such associations are generally unknown. The objective of the present paper is to summarize data on species composition and ecology of polychaetes associated with cnidarians. In our review, we report 281 species of cnidarian hosts involved in 324 relationships with symbiotic polychaetes. Most polychaete-hosting cnidarians belong to skeleton-bearing taxa, particularly Scleractinia (125 species or 44.48 % of the total cnidarian hosts), Alcyonaria (73 species or 25.97 %) and Hydrozoa (60 species or 21.35 %). About 120 species of symbiotic polychaetes of ten families are reported from cnidarian hosts. Polynoidae include the highest number of cnidarian-associated polychaetes (almost one half of the currently known species), followed by Syllidae and Serpulidae. Host symbiont interrelations, host specificity, location, infestation characteristics and adaptive modifications of symbionts, as well as host reaction on symbionts presence, have been considered. Our review highlights that (1) every group of cnidarians seems to have their own assemblage of symbiotic polychaetes, (2) some deep-sea alcyonaceans and black corals have never been reported without their often undetermined polynoid symbionts so that its presence has been considered as a species-specific, robust taxonomic character, and (3) we certainly expect the polychaete symbionts associated with deep-sea corals to be a hidden hot-spot of diversity, with many species still waiting to be described.

T.A. Britayev & D. Martin. Chaetopteridae Audouin & Milne Edwards, 1833 Chapter in: Westheide, W. & Purschke, G. (Eds.), Handbook of Zoology. A Natural History of the Phyla of the Animal Kingdom. Annelida: Polychaeta. De Gruyter, Osnabrück.
ABSTRACT

Cnidarians, especially skeleton-bearing anthozoans and hydrocorals, are known to host abundant and diverse symbiotic fauna encompassing members of the majority of metazoan taxa, ranging from sponges and flat worms to fishes. Members of the class Polychaeta are between the most diverse and perhaps the least studied taxa of coral symbionts. The last revision (Martin and Britayev, Oceanogr Mar Biol 36:217–340, 1998) reckoned about 60 species of symbiotic polychaetes associated with more than 100 species of cnidarian hosts. However, this number is considerably underestimated. Some populations of scleractinians, sea fans and black corals show up to 100 % infestation by symbiotic polychaetes. Close association and inter-relation of highly host-specific symbionts and cnidarian hosts often lead to dramatic changes in the host morphology. At the moment, actual mechanisms of most of mutual relations between host and symbiont in such associations are generally unknown. The objective of the present paper is to summarize data on species composition and ecology of polychaetes associated with cnidarians. In our review, we report 281 species of cnidarian hosts involved in 324 relationships with symbiotic polychaetes. Most polychaete-hosting cnidarians belong to skeleton-bearing taxa, particularly Scleractinia (125 species or 44.48 % of the total cnidarian hosts), Alcyonaria (73 species or 25.97 %) and Hydrozoa (60 species or 21.35 %). About 120 species of symbiotic polychaetes of ten families are reported from cnidarian hosts. Polynoidae include the highest number of cnidarian-associated polychaetes (almost one half of the currently known species), followed by Syllidae and Serpulidae. Host symbiont interrelations, host specificity, location, infestation characteristics and adaptive modifications of symbionts, as well as host reaction on symbionts presence, have been considered. Our review highlights that (1) every group of cnidarians seems to have their own assemblage of symbiotic polychaetes, (2) some deep-sea alcyonaceans and black corals have never been reported without their often undetermined polynoid symbionts so that its presence has been considered as a species-specific, robust taxonomic character, and (3) we certainly expect the polychaete symbionts associated with deep-sea corals to be a hidden hot-spot of diversity, with many species still waiting to be described.

J. Parapar, J. Moreira, & D. Martin. On diversity of the SE Indo-Pacific species of Terebellides (Annelida; Trichobranchidae), with the description of a new species. PeerJ 4: e2313. DOI 10.7717/peerj.2313.
ABSTRACT

The study of material collected during routine monitoring surveys dealing with oil
extraction and aquaculture in waters off Myanmar (North Andaman Sea) and in the
Gulf of Thailand, respectively, allowed us to analyse the taxonomy and diversity of the
polychaete genus Terebellides (Annelida). Three species were found, namely Terebellides cf. woolawa, Terebellides hutchingsae spec. nov. (a new species fully described and illustrated), and Terebellides sp. (likely a new species, but with only one available specimen). The new species is characterised by the combination of some branchial (number, fusion and relative length of lobes and papillation of lamellae), and thoracic (lateral lobes and relative length of notopodia) characters and is compared with all species described or reported in the SW Indo-Pacific area, as well as with those sharing similar morphological characteristics all around the world. The taxonomic relevance of the relative length of branchial lobes and different types of ciliature in branchial lamellae for species discrimination in the genus is discussed. A key to all Terebellides species described in SE Indo-Pacific waters is presented.

J. Parapar, J. Moreira, J. Gil & D. Martin. A new species of the genus Terebellides (Polychaeta, Trichobranchidae) from the Iranian coast. Zootaxa 4117(3):321-340
ABSTRACT

Based on specimens collected during several sampling programmes along the Iranian coast, Persian Gulf, a new species of the genus Terebellides (Polychaeta, Trichobranchidae) is herein described as Terebellides persiae spec. nov. The new species is primarily characterised by the presence of a large dorsal thoracic hump in larger specimens and ciliated papillae on the branchial lamellae. The new species is compared with other taxa belonging to Terebellides described or reported with any of both characters. SEM and micro-CT have been used to study T. persiae spec. nov. and provide several new details on external characters and internal organs, respectively. A key for the identification of the species of Terebellides with dorsal hump is provided.

L. Garate, A. Blanquer, M.J. Uriz. Contrasting growth and survival of two cryptic sponge species sharing habitats in western Mediterranean. Front. Mar. Sci. Conference Abstract: XIX Iberian Symposium on Marine Biology Studies. doi: 10.3389/conf.FMARS.2016.05.00170.
M. Guardiola, J. Frotscher, M.J. Uriz. High genetic diversity, phenotypic plasticity, and invasive potential of a recently introduced calcareous sponge, fast spreading across the Atlanto‑Mediterranean basin. Mar Biol (2016) 163:123. doiI 10.1007/s00227-016-2862-6
ABSTRACT

Sponges are considered poor invaders, and no genetic studies on introduced sponges have been performed up to now. Paraleucilla magna is the first calcareous sponge introduced to the Mediterranean and Northeastern Atlantic. The study aimed at investigating the genetic makeup and connectivity of the introduced populations of
P. magna and at exploring signs of local phenotypic adaptation, to gain insight on the species invasive potential. Ten populations along the species introduction range (Brazil,
Açores, Madeira, and continental Europe) were genetically characterized by using nine microsatellite markers. Most populations were genetically structured as suggested
by significant Dst and Fst values, significant differences among populations (AMOVA) and the presence of private alleles. The analyzed populations belonged to three genetically homogeneous groups (K) according to the Bayesian algorithm (structure software) and the UPGMA dendrogram. Genetic diversity within populations was higher than expected. Recurrent introductions of non-randomly selected individuals from the native sources may have contributed to the heterozygote deficit found in all populations by forming pedigree structures with mating among relatives. Moreover, the species biological cycle was monitored in a population established on native Mediterranean assemblages (41°40′27″N, 2°47′25″E) and compared with the species cycle in other habitats. Contrasting life spans, growth habits, and reproduction cycles, depending on the habitat conditions, were recorded. To summarize, high genetic diversity, phenotypic local adaptation, and high reproduction rates altogether allow predicting the fast proliferation of P. magna in newly colonized regions and point to its strong invasive potential.

M. Carella, G. Agell, P. Cárdenas, M.J. Uriz. Phylogenetic Reassessment of Antarctic Tetillidae (Demospongiae, Tetractinellida) Reveals New Genera and Genetic Similarity among Morphologically Distinct Species. PLoSONE 11(8). doi:10.1371/journal.pone.0160718.
ABSTRACT

Species of Tetillidae are distributed worldwide. However, some genera are unresolved and only a few genera and species of this family have been described from the Antarctic. The incorporation of 25 new COI and 18S sequences of Antarctic Tetillidae to those used recently for assessing the genera phylogeny, has allowed us to improve the resolution of some poorly resolved nodes and to confirm the monophyly of previously identified clades. Classical genera such as Craniella recovered their traditional diagnosis by moving the Antarctic Tetilla from Craniella, where they were placed in the previous family phylogeny, to Antarctotetilla gen. nov. The morphological re-examination of specimens used in the previous phylogeny and their comparison to the type material revealed misidentifications. The proposed monotypic new genus Levantinella had uncertain phylogenetic relationships depending on the gene partition used. Two more clades would require the inclusion of additional species to be formally established as new genera. The parsimony tree based on morphological characters and the secondary structure of the 18S (V4 region) almost completely matched the COI M1-M6 and the COI+18S concatenated phylogenies. Morphological synapomorphies have been identified for the genera proposed. New 15 28S (D3-D5) and 11 COI I3-M11 partitions were exclusively sequenced for the Antarctic species subset. Remarkably, species within the Antarctic genera Cinachyra (C. barbata and C. antarctica) and Antarctotetilla (A. leptoderma, A. grandis, and A. sagitta), which are clearly distinguishable morphologically, were not genetically differentiated with any of the markers assayed. Thus, as it has been reported for other Antarctic sponges, both the mitochondrial and nuclear partitions used did not differentiate species that were well characterized morphologically. Antarctic Tetillidae offers a rare example of genetically cryptic (with the traditional markers used for sponges), morphologically distinct species.

A. Riesgo, R. Pérez-Portela, L. Pita, G. Blasco, P.M. Erwin and S. López-Legentil. Population structure and connectivity in the Mediterranean sponge Ircinia fasciculata are affected by mass mortalities and hybridization. Heredity, 1-13. doi:10.1038/hdy.2016.41.
ABSTRACT

Recent episodes of mass mortalities in the Mediterranean Sea have been reported for the closely related marine sponges Ircinia fasciculata and Ircinia variabilis that live in sympatry. In this context, the assessment of the genetic diversity, bottlenecks and connectivity of these sponges has become urgent in order to evaluate the potential effects of mass mortalities on their latitudinal range. Our study aims to establish (1) the genetic structure, connectivity and signs of bottlenecks across the populations of I. fasciculata and (2) the hybridization levels between I. fasciculata and I. variabilis. To accomplish the first objective, 194 individuals of I. fasciculata from 12 locations across the Mediterranean were genotyped at 14 microsatellite loci. For the second objective, mitochondrial cytochrome c oxidase subunit I sequences of 16 individuals from both species were analyzed along with genotypes at 12 microsatellite loci of 40 individuals coexisting in 3 Mediterranean populations. We detected strong genetic structure along the Mediterranean for I. fasciculata, with high levels of inbreeding in all locations and bottleneck signs in most locations. Oceanographic barriers like the Almeria-Oran front, North-Balearic front and the Ligurian-Thyrrenian barrier seem to be impeding gene flow for I. fasciculata, adding population divergence to the pattern of isolation by distance derived from the low dispersal abilities of sponge larvae. Hybridization between both species occurred in some populations that might be increasing
genetic diversity and somewhat palliating the genetic loss caused by population decimation in I. fasciculata.

S. López-Legentil, X.Turon, P.M. Erwing. Feeding cessation alters host morphology and bacterial communities in the ascidian Pseudodistoma crucigaster. Frontiers in Zoology, 13:2. DOI 10.1186/s12983-016-0134-4
ABSTRACT

Background: Ascidians can associate with abundant and diverse consortia ofmicrobial symbionts, yet these
communities remain unexamined for the majority of host ascidians and little is known about host-symbiont interactions.
Methods: We coupled electron microscopy and 16S rRNA gene tag pyrosequencing to investigate the bacterial
communities associated with the colonial ascidian Pseudodistoma crucigaster, a species endemic to theMediterranean Sea
that has a life cycle with two phases: actively-filtering (active) and non-filtering (resting) forms.
Results: Resting colonies exhibited a reduced branchial sac (feeding apparatus) and a thickened cuticle. Electron
microscope images also suggested higher abundance of colonizing microorganisms on surfaces of resting colonies.
Accordingly, bacterial sequences associated with environmental sources (sediment and biofilms, >99 % similarity) were
detected exclusively in resting colonies. Bacterial communities of P. crucigaster colonies (active and resting) were
dominated by 3 core taxa affiliated (>94 % similarity) with previously described symbiotic Alphaproteobacteria in marine
invertebrates. Shifts in rare bacteria were detected when ascidians entered the resting phase, including the appearance of
strictly anaerobic lineages and nitrifying bacterial guilds.
Conclusions: These findings suggest that physical (thickened cuticle) and metabolic (feeding cessation) changes
in host ascidians have cascading effects on associated bacteria, where modified oxygen concentrations and
chemical substrates for microbial metabolism

A. Blanquer, M.J. Uriz, E. Cebrian, P. E. Galand Snapshot of a bacterial microbiome shift during the early symptoms of a massive sponge die-off in the western Mediterranean. Front. Microbiol. 7:752. doi:10.3389/fmicb.2016.00752
ABSTRACT

Ocean warming is affecting marine benthic ecosystems through mass mortality events that involve marine invertebrates, in particular bivalves, corals, and sponges. Among these events, extensive die-offs of Ircinia fasciculata sponges have been recurrently reported in western Mediterranean. The goal of our study was to test whether the temperature-related mass sponge die-offs were associated with or preceded by an early unbalanced bacterial microbiome in the sponge tissues. We took advantage of the early detection of disease and compared the microbiomes of healthy vs. early diseased I. fasciculata tissues. Our results showed a microbiome shift in early diseased tissues. The abundance of Gammaproteobacteria and Acidobacteria increased and that of Deltaproteobacteria decreased in diseased vs. healthy tissues. The change in community composition was also noticeable at the OTU level. Diseased tissues contained more bacterial sequences previously identified in injured or stressed sponges and corals than
48 healthy tissues. Bacterial diversity increased significantly in diseased tissues,  which contained a higher number of low abundance OTUs. Our results do not support the hypothesis of one particular pathogen, whether a Vibrio or any other bacteria, triggering the Northwestern Mediterranean mass mortalities of I. fasciculata. Our data rather suggest an early disruption of the bacterial microbiome balance in healthy sponges through a shift in OTU abundances, and the purported consequent decline of the sponge fitness and resistance to infections. Opportunistic bacteria could colonize the sponge tissues, taking benefit of the sponge weakness, before one or more virulent pathogens might proliferate ending in the mass sponge die-off.

2015

D. Sipkema, S. de Caralt, J.A. Morillo, W.A Al-Soud, S-.J. Sorensen, H. Smidt, M. J. Uriz. Similar sponge-associated bacteria can be acquired via both vertical and horizontal transmission. Environmental Microbiology 17(10), 3807–3821. doi: 10.1111/1462-2920.12827.
ABSTRACT

Marine sponges host diverse communities of microorganisms that are often vertically transmitted from mother to oocyte or embryo. Horizontal transmission has often been proposed to co-occur in marine sponges, but the mechanism is poorly understood. To assess the impact of the mode of transmission on the microbial assemblages of sponges, we analysed the microbiota in sympatric sponges that have previously been reported to acquire bacteria via either vertical (Corticium candelabrum and Crambe crambe) or horizontal transmission (Petrosia ficiformis). The comparative study was performed by polymerase chain reaction-denaturing gradient gel electrophoresis and pyrosequencing of barcoded PCR-amplified 16S rRNA gene fragments. We found that P. ficiformisand C. candelabrum each harbour their own species-specific bacteria, but they are similar to other high-microbial-abundance sponges, while the low-microbial-abundance sponge C. crambe hosts microbiota of a very different phylogenetic signature. In addition, nearly 50% of the reads obtained from P. ficiformis were most closely related to bacteria that were previously reported to be vertically transmitted in other sponges and comprised vertical–horizontal transmission phylogenetic clusters (VHT clusters). Therefore, our results provide evidence for the hypothesis that similar sponge-associated bacteria can be acquired via both vertical and horizontal transmission.

S. López-Legentil, P.M. Erwig, M. Turon, O. Yarden. Diversity of fungi isolated from three temperate ascidians. Symbiosis. doi: 10.1007/s13199-015-0339-x
ABSTRACT

Ascidians are known to harbor diverse and hostspecific

bacterial and archaeal communities in their tunic.

However, to date, only one ascidian species has been investigated

to assess symbiotic relationships with fungi and

the extent of their diversity. In this study, we isolated and

identified 37 strains of fungi in association with three common

ascidian species in the NW Mediterranean Sea:

Cystodytes dellechiajei, Didemnum fulgens, and

Pycnoclavella communis, and 15 additional strains from

concentrated seawater samples collected around the animals.

Most of the isolated fungi were classified within four

orders: Eurotiales (predominantly Penicillium spp.),

Pleosporales, Hypocreales (predominantly Trichoderma

spp.), and Capnodiales (Cladosporium spp.). Three additional

fungal isolates from C. dellechiajei and D. fulgens

belonged to the orders Helotiales, Phylachorales and

Microascales, and matched to well-known plant and human

pathogens (Botrytis cinerea, Plectosphaerella cucumerina

and Scopulariopsis brevicaulis). Host-specificity of

ascidian-associated fungi was not apparent and thus the

significance of ascidian-fungal associations for ascidian

wellbeing and their possible ecological roles remain

unknown.

S. López-Legentil, X.Turon, R. Espluga, P.M. Erwing. Temporal stability of bacterial symbionts in a temperate ascidian. Front. Microbiol. 6:1022. doi:10.3389/fmicb.2015.01022
ABSTRACT

 In temperate seas, both bacterioplankton communities and invertebrate life cycles follow a seasonal pattern. To investigate whether the bacterial community associated with the Mediterranean ascidian Didemnum fulgens exhibited similar variations, we monitored its bacterial community structure monthly for over a year using terminal restriction fragment length polymorphism and clone library analyses based on a nearly full length fragment of the 16SrRNA gene. D.fulgens harbored a bacterial consortium typical of ascidians, including numerous members of the phylum Proteobacteria,and a few members of the phyla Cyanobacteria and Acidobacteria. The overall bacterial community in D.fulgens had a distinct signature from the surrounding seawater and was stable overtime and across seasonal fluctuations in temperature. Bacterial symbionts were also observed around animal cells in the tunic of adult individuals and in the inner tunic of D.fulgens larvae by transmission electron microscopy. Our results suggest that,as seen for sponges and corals, some species of ascidians host stable and unique bacterial communities that are at least partially inherited by their progeny by vertical transmission.

J. González-Ramos, G. Agell, M.J. Uriz. Microsatellites from sponge genomes: the number necessary for detecting genetic structure in Hemimycale columella populations. Aquat. Biol. Vol. 24: 25–34. doi: 10.3354/ab00630.
ABSTRACT

Using next-generation sequencing technology, we designed a pool of microsatellite
primers and amplified them in 2 physically isolated populations of the Atlanto-Mediterranean
sponge Hemimycale columella, which exhibits particular evolutionary, biological, and ecological
features. The species has contrasting life cycles in shallow and relatively deep waters, and
releases small, predictably low-dispersal larvae. This study experimentally evaluated how many
polymorphic microsatellites would be necessary to detect genetic structure in H. columella populations,
and whether or not the use of compound loci is advisable. By sequencing 1/2 454 GS-FLX
run, we obtained a total of 4208 sequences enclosing microsatellite motifs. We selected 20 microsatellites,
15 of which proved adequate for the genetic study of the sponge populations. The 2 analyzed
populations were genetically structured with all microsatellite combinations assayed, and
the values of the Dest and FST statistics did not increase with increasing number of loci. A weak signal
of genetic structure, however, was shown in bar plots representing membership coefficients
for each individual to each sampling location even with all loci. We conclude that a few polymorphic
loci can detect structure in H. columella populations, but using 12 or more loci notably
enhances the power of the analyses. The study also describes a low-cost protocol for obtaining
microsatellites by the hundreds from non-model, ecologically relevant species, which can be used
to provide information about population isolation, adaptation, and vulnerability.

P.M. Erwing, R. Coma, P. López-Sendino, E. Serrano, M. Ribes. Stable symbionts across the HMA-LMA dichotomy: Low seasonal and inter-annual variation in sponge-associated bacteria from taxonomically diverse hosts. FEMS Microbiology Ecology, 91. doi: 10.1093/femsec/fiv115
ABSTRACT

Marine sponges host bacterial communities with important ecological and economic roles in nature and society, yet these benefits depend largely on the stability of host-symbiont interactions and their susceptibility to changing environmental conditions. Here, we investigated the temporal stability of complex host-microbe symbioses in a temperate, seasonal environment over three years, targeting sponges across a range of symbiont density (high and low microbial abundance, HMA and LMA) and host taxonomy (six orders). Symbiont profiling by terminal restriction fragment length polymorphism analysis of 16S rRNA gene sequences revealed that bacterial communities in all sponges exhibited a high degree of host specificity, low seasonal dynamics and low interannual variability: results that represent an emerging trend in the field of sponge microbiology and contrast sharply with the seasonal dynamics of free-living bacterioplankton. Further, HMA sponges hosted more diverse, even and similar symbiont communities than LMA sponges and these differences in community structure extended to core members of the microbiome. Together, these findings show clear distinctions in symbiont structure between HMA and LMA sponges while resolving notable similarities in their stability over seasonal and inter-annual scales, thus providing insight into the ecological consequences of the HMA-LMA dichotomy and the temporal stability of complex host-microbe symbioses.

S. Taboada, A. Riesgo, G. Blasco, J. Solà, J.R. Xavier, S. López-Legentil. Development of 10 microsatellite markers for the Atlanto-Mediterranena sponge Petrosia ficiformis. Conservation Genetics Resources, 7: 895-897.
D. Martin, A. Nygren, P. Hjelmstedt, P. Drake, J. Gil. On the enigmatic symbiotic polychaete ‘Parasyllidea’ humesi Pettibone, 1961 (Hesionidae): taxonomy, phylogeny and behaviour. Zoological Journal of the Linnean Society. doi: 10.1111/zoj.12249
ABSTRACT

The hesionid genus Parasyllidea differs from Oxydromus in lacking median antennae. It was originally described to include a single species, P. humesi, known only from its original description. This was based on specimens from mangrove swamps at Pointe-Noire (Republic of Congo, West Africa), living endosymbiotically with the bivalve Tellina nymphalis. Lately, the genus included P. blacki and P. australiensis. A new population of P. humesi was recently found at the upper intertidal level of Rio San Pedro salt marsh in Cádiz Bay (eastern Atlantic, Iberian Peninsula). It was also living endosymbiotically, but with another bivalve, Scrobicularia plana. Some Iberian and Congolese specimens revealed the presence of a small papilla-like central antenna associated with the prostomial median ridge, which raised some doubts on the validity of the genus Parasyllidea. A phylogenetic analysis based on the mitochondrial COI and 16S and the nuclear 18S and 28S genes confirms Parasyllidea as a junior synonym of Oxydromus. Therefore, in this paper, P. humesi is fully re-described as Oxydromus humesi comb. nov. The worm has never been reported as free-living. Previously, the association appeared to be an obligate symbiosis, closer to parasitism, as infested hosts had lower relative biomasses than non-infested ones and the worm did not occur locally inside any other bivalve co-habiting the intertidal salt marsh. The finding of a highly infested population (> 85% in the specimens longer than 20 mm) of a new host at the lower subtidal part of Rio San Pedro mouth, the bivalve Psammotreta cumana, led us to discuss the host-specificity of O. humesi. In addition, the observation of living specimens during sampling and laboratory handling enabled detailed observations of the host-entering behaviour of the specimens living with S. plana, which are also described and illustrated. Living, uninfested specimens of P. cumana have not been obtained, preventing us from checking the host-entering behaviour in the new host. The significance of the intraspecific attacks observed in experimental conditions is also discussed.

M. Conradi, M.E. Bandera, I. Marin, D. Martin. Polychaete-parasitizing copepods from the deep-sea Kuril–Kamchatka Trench (Pacific Ocean), with the description of a new Ophelicola species and comments on the currently known annelidicolous copepods. Deep-Sea Research II 111: 147-165. doi:10.1016/j.dsr2.2014.08.018.
ABSTRACT

The annelid associated copepods, collectively called annelidicolous, were placed in 21 families. Some genera, such as Ophelicola, are considered phylogenetically isolated and are placed into the order Cyclopoida as incertae sedis. In this paper, we describe Ophelicola kurambia, the second species recorded

for the genus and the first for the Pacific Ocean. The single known specimen, a female, was found during the German–Russian deep-sea expedition KuramBio at the deep-sea Kuril–Kamchatka Trench. The new species differs from Ophelicola drachi (known from the Gulf of Biscay, Atlantic Ocean) in being attached to the host through the mandibles instead of maxillae and, specially, in the formula of the antennular armature. The study of the new species contributes to clarify the diagnosis of the genus, which clearly differs from Notomasticola (another incertae sedis genus), and resembles both the most modified clausiids (in the mandibular shape and antennular segmentation) and the clausidiids (in the shape of maxilla). However, it does not contribute to clarify the position of Ophelicola within the order Cyclopoida. The paper includes a list of the known annelidicolous copepods (excluding Monstrilloidae) and summarises the main trends shown in terms of diversity, distribution and relationships. Currently, 168 species of copepods from to 74 genera and 22 families and 7 incertae sedis (excluding Monstrilloida) are known to be involved in 235 parasitic relationships (mostly ectoparasitic) with polychaetes. Host polychaetes include 156 species belonging to 104 genera from 22 families (plus 14 unknown). About 50% of these relationships are known from European waters, mainly from shallow depths.

L. Garate, A. Blanquer, M-J. Uriz. Calcareous spherules produced by intracellular symbiotic bacteria protect the sponge Hemimycale columella from predation more than secondary metabolites. Mar Ecol Prog Ser 523:81-92. doi: 10.3354/meps11196.
ABSTRACT

Benthic sessile organisms in general, and sponges in particular, have developed an array of defense mechanisms to survive in crowded, resource and/or space-limited environments. Indeed, various defense mechanisms may converge in sponges to accomplish a defensive function in an additive or synergetic way, or to operate at different times during the sponge’s life cycle. Moreover, sponges harbor highly diverse microbial communities that contribute in several ways to the host’s success. Although some symbiotic bacteria produce chemical compounds that protect the sponge from predation, the possible deterrent function exerted by the calcareous coat of a sponge’s endosymbiotic bacterium has not, to date, been explored. Hemimycale columella is an Atlanto-Mediterranean sponge, which produces bioactive metabolites and has been reported to host an intracellular bacterium with a calcite envelope. Calcibacteria accumulate in high densities at the sponge periphery, forming a kind of sub-ectosomal cortex. They have been suggested to provide the sponge with several benefits, one of which is protection from predators. In this study, we assess the relative contribution of the endosymbiotic calcibacteria and bioactive compounds produced by H. columella to defend the sponge against sympatric predators. Deterrence experiments have revealed that the sponge combines >1 defense mechanism to dissuade a large array of potential predators; this represents an example of the evolutionary fixation of redundant mechanisms of defense. The chemicals deterred Paracentrotus lividus, Chromis chromis, Oblada melanura, and Diplodus vulgaris, but not Parablennius incognitus and Coris julis, while the spherules of the symbiotic calcibacteria significantly deterred all predators assayed.

2014

I. Burgsdorf, P.M. Erwin, S. López-Legentil, C. Cerrano, M. Haber, S. Frenk, L. Steindler. Biogeography rather than associtation with cyanobacteria structures symbiotic microbial communities in the marine sponge Petrosia ficiformis. Frontiers in Microbiology. DOI: 10.3389/fmicb.2014.00529.
ABSTRACT

The sponge Petrosia ficiformis is ubiquitous in the Mediterranean Sea and Eastern Atlantic Ocean, hosting a diverse assemblage of bacteria, including in iluminated sites, cyanobacteria. Two closely related sponge color morphs have bee described, one inside caves and at their entrance (white/pink), and one on the rocky cliffs (violet). The presence of the different morphs and their ubiquity in the Mediterranean (from North-West to South-East) provides an opportunity to examine which factors mostly affect the associated microbial communities in this species: (i) presence of phototrophic symbionts or (ii) biogeography. 16S rRNA gene tag pyrosequencing data of the microbial communities revealed taht Chloroflexi, Gammaproteobacteria, and Acidobacteria dominated the bacterial communities of all sponges analyzed. Chlorophyll a content TEM observations and DNA sequence data confirmed the presence of the cyanobacterium Synechococcus feldmannii in violet and pink norphs of P.ficiformis and their absence in white color morphs. Rather than cyanobacterial symbionts (i.e., color morphs) accounting for variability in microbial symbiont communities, a biogeographic trend was observed between  P. ficiformis collected in Israel and Italy. Analyses of partial 18S r RNA and mitochondrial cytochrome c oxidase subunit I (COX1) gene sequences revealed consitent genetic divergence betweeen the violet and pink-white morphotypes of P. ficiformis. Overall, data indicated that microbial symbiont communities were more similar in genetically distinct P. ficiformis from the same location, than genetically similar P. ficiformis from distant locations.

T.A. Britayev, J. Gil, A. Altuna, M. Calvo, D. Martin. New symbiotic associations involving polynoids (Polychaeta, Polynoidae) from Atlantic waters, with redescriptions of Parahololepidella greeffi (Augener, 1918) and Gorgoniapolynoe caeciliae (Fauvel, 1913). Memoirs of Museum Victoria 71: 27–43.
ABSTRACT

Different circumstances such as sampling methodology, sample sorting or taxa distribution among different experts often lead symbiotic associations to remain hidden and the mode of life of the involved partners are either not defined or directly reported as free living. This was apparently the case of Parahololepidella, a genus proposed by Pettibone (1969) to include Hololepidella greeffi Augener, 1918, reported as free-living from shallow waters off São Tomé and Cabo Verde Islands (W Africa). In this paper, we report for the first time the symbiotic status of P. greeffi (Augener, 1918), which lives in association with the antipatharian Tanacetipathes cf. spinescens (Gray, 1857), based on new materials collected in São Tomé Island. In addition to the originally described features, the species is characterized by a variable presence of cephalic peaks and by an irregular distribution of elytra from segment 32-33, which may be asymmetrical (within the same individual) and differ between individuals. A list of all known polychaete species associated with antipatharian corals is also provided. We also report new findings of Gorgoniapolynoe caeciliae (Fauvel, 1913) from deep waters of the Atlantic coasts of the Iberian Peninsula, living in association with the octocorals Candidella imbricata (Johnson, 1862) (first report for the Spanish waters) and Corallium niobe Bayer, 1964. The diagnosis of Gorgoniapolynoe is emended and we suggest that G. corralophila (Day, 1960) should be referred to a different genus and that G. pelagica Pettibone, 1991a should be considered as nomen dubium. The Iberian G. caeciliae fits well with the re-description by Pettibone (1991a), except for the presence of clavate papillae on dorsal cirri, which were neither mentioned nor figured in previous descriptions.

Conferences

2016

T.A. Britayev, D. Martin. Tigers into the blue: Territorial attacks in the chaetopterid associated polynoid Ophthalmonoe pettiboneae. 12th International Polychaete Conference, National Museum of Wales, Cardiff, Wales, 1-5 August. Oral communication.
M.A. Meca Jimenez, J. Gil, P. Drake, A. Nygren, D. Martin. Life history of a symbiotic Oxydromus (Annelida, Hesionidae) hosted by Scrobicularia plana in Cádiz Bay, with the description of the Iberian population as a new species based on morphometry. 12th International Polychaete Conference, National Museum of Wales, Cardiff, Wales, 1-5 August. Poster
M.J. Uriz, L. Garate, G. Agell. The meandering path to the discovering of cryptic sponge species. XIX SIEMB, 2-8 September 2016, Porto, Portugal. Oral communication.
M. Turon, L. Garate, X. Triadó-Margarit, J. Cáliz, M. J. Uriz. Sponges and their microbiomes in clean and polluted habitats. XIX SIEMB, 2-8 September 2016, Porto, Portugal. Oral communication.
Leire Garate, Andrea Blanquer, Maria J. Uriz Contrasting microbiomes in sponges with similar bacteria-mediated calcium-carbonate spherules, from temperate and tropical oceans. XIX SIEBM , 2-8 September 2016, Porto, Portugal. Oral communication.
C. Huete-Stauffer & M.J. Uriz Effects of thermal anomalies on the growth dynamics of Dysidea avara (Porifera). XIX SIEBM, 2-8 September 2016, Porto, Portugal. Oral communication.
C.Huete-Stauffer & M.J. Uriz. I like it when it’s warm! Or not? 41st CIESM Congress 12-16 September. Kiel, Germany. Oral communication.
L. Garate, A. Blanquer, M.J. Uriz. Symbiotic calcifying bacteria across sponge species and oceans. 41st CIESM Congress 12-16 September, Kiel Germany. Oral communication.
D. Cepeda, D. Martin, T.A Britayev, P. Lattig. A new species of Haplosyllis (Annelida: Syllidae) from Saudi Arabian Red Sea, with a dichotomous key of Indian Ocean species. 12th International Polychaete Conference, National Museum of Wales, Cardiff, Wales, 1-5 August. Poster.
M.J. Uriz, L. Garate, G. Agell Cryptic sponge species, much more than wrong taxonomical identification.
Cryptic sponge species, much more than wrong taxonomical identification.41st CIESM Congress 12-16 September 2016 , Kiel Germany. Oral communication.

2015

T. Molodtsova, T.A. Britayev, D. Martin & N. Budaeva. Deep-sea corals and their polychaete symbionts. 14th Deep Sea Biology Symposium, Aveiro (Portugal). 31 August – 4 September. Oral Communication.
P. Lattig, I. Muñoz, D. Martin, P. Abelló, A. Machodrom. Comparative phylogeography of two symbiotic dorvilleid polychaetes with contrasting host-crab and bathymetric patterns. International Symbiosis Society Meeting. University of Lisboa, Lisboa, 12-18 July. Oral communication.
D. Martin, & TA. Britayev. 1998-2015: Updating the quantification of symbiotic polychaetes and their hosts and relationships. International Symbiosis Society Meeting. University of Lisboa, Lisboa, 12-18 July. Poster.

2014

L. Steindler, I. Burgsdorf, PM. Erwin, S. López-Legentil, C. Cerrano, M. Haber. Biogeography rather than association with cyanobacteria structures symbiotic microbial communities in the marine sponge Petrosia ficiformis. 2nd International Symposium on Sponge Microbiology, Baltimore, Maryland, United States.
J. Sureda, G. Agell, L. Garate, M.J. Uriz. Molecular approaches to the study of a rare sponge-microbial symbiosis: cellular, taxonomical, and geographical location of calcifying bacteria. XVIII SIEMB, September 2014, Gijón.