Friday 7 August 2020

Lodgers on the tubes of Tube Anemones.

Benthic organisms are well adapted to the habitat conditions present in the locations where they live and estimates of abundance of these organisms are usually related to the habitat in which they are found. Moreover, some species require anchoring sites to settle and complete part of or their whole life cycles. Thus, the lack of consolidated structures on unconsolidated bottoms leads many benthic settlers to seek different suitable substrates, amongst which are artificial substrates such as ship hulls or offshore platforms, and natural substrates, such as marine invertebrate shells, Corals, and Ceriantharian (Tube Anemone) tubes. Ceriantharians (Cnidaria: Anthozoa) are tube-dwelling Animals that synthesize their tubes primarily with the use of ptychocysts, a type of cnida only found in this group, combined with small sediment fragments from the sea bottoms where the tube is built. The soft texture of ceriantharian tubes would initially appear not to be an attractive feature for the anchoring of invertebrate species that usually use rigid structures as anchoring locations. However, a few studies have reported on species able to settle on this microhabitat. In spite of it, the sampling of Ceriantharia is rather troublesome and rare, and tubes are usually overlooked and rarely collected along with polyps, contributing to lack of information about this subject.

In a paper published in the journal Biodiversity Data on 8 January 2020, Hellen Ceriello and Celine Lopes of the Instituto de Biociências at the Universidade Estadual Paulista, James Davis Reimer of the University of the Ryukyus, Torkild Bakken of the University Museum at the Norwegian University of Science and Technology, Marcelo Fukuda of the Museu de Zoologia da Universidade de São Paulo, Carlo Magenta Cunha of the Universidade Federal de São Paulo, and Sérgio Stampar, also of the Instituto de Biociências at the Universidade Estadual Paulista report on invertebrate communities inhabiting tubes of different Ceriantharian species from different locations, and discusses their main characteristics.

Ceriello et al. sampled 22 tubes of 10 species of Ceriantharia by SCUBA surveys in Argentina, Brazil, Japan, Norway, Portugal, and the United States. All material, except for Isarachnanthus nocturnus, and Ceriantheomorphe sp., was preserved along with their polyps and, before analyses, all polyps were removed from their tubes which were kept individually in labelled jars containing 70% ethanol.

The Tube Anemone, Isarachnanthus nocturnusSergio Stampar/National Science Foundation.

Each tube was analyzed separately under a stereomicroscope in a bowl with dark craft foam in the bottom and full of freshwater. All tubes were longitudinally cut with surgical carbon steel scalpels, opened, and fixed in the craft foam using acupuncture needles. Both inner and outer walls were analysed. The fauna found in or on the tubes was removed, photographed, and measured using a Zeiss AxioCam MRc5 and Zeiss AxioVision SE64 Rel 4.8 imaging software. Afterwards, the associated fauna was morphologically identified with specific taxonomic keys for each group.

A total of 58 species (8 crustaceans, 24 molluscs, 26 polychaetes) was observed in/on ceriantharian tubes. It is noteworthy that, although Crustaceans and Polychaetes in this study were alive at the time of sampling, they were not alive during tube analyzes. The results were separated by taxonomic group.

Thirghty eight Mollusc shell specimens, including Gastropoda and Bivalvia, were observed and were always found adhered to the outside of the tubes, and none had a periostracum coating, indicating that they were not alive at the time of collection.

Mollusca found on Ceriantharian tubes. (A) Schwartziella bryerea (B) Parvanachis obesa (C) Bittiolum varium (D) Cerithidea balteata (E) Chrysallida sp. (F) Liotella sp. (G) Emarginula sp. (H) Bostrycapulus odites (I) Collonista rubricincta (J) Eulima sp. (K) Microgaza rotella (L) Turbonilla sp. (M) Caecum regulare (N) Puncturella noachina (O) Basterotia elliptica (P) Ervilia nitens (Q) Macomopsis melo (R) Cumingia lamellosa (S) Musculus lateralis (T) Cardites micellus (U) Tivela sp. (V) Sphenia fragilis. Scale bars (A)-(N) 500 μm (O)–(U) 500 μm (V) 100 μm. Ceriello et al. (2020).

Ceriello et al.observed shells of Schwartziella bryerea and Turbonilla sp. adhered to the fragile tube of Arachnanthus sp., as well as amongst sediments that surrounded the tube. Shells of Cerithidea balteata, Eulima sp., Liotella sp., Emarginula sp., Chrysallida sp. and Collonista rubricincta, were found attached to the entire length of the thin and delicate tube of Isarachnanthus bandanensis. Bittiolum varium was found attached to the tubes of Isarachnanthus nocturnus. Puncturella noachins was, in part, adhered to the thin and fragile tube of Cerianthus lloydii.

On the tubes of Ceriantheomorphe brasiliensis, Ceriello et al. noted shells of Bittiolum varium, Finella dubia, Parvanachis obesa, Bostrycapulus odites, Caecum regulare, and Microgaza rotella. The tubes of Ceriantheomorphe brasiliensis usually have a high amount of overlap of filaments and, although this pattern was also observed in specimens in this study, no Mollusc shells were found between layers, and shells were only found on the outermost surfaces of the tubes.

Shells of Ervilia nitens, Chama sp., Cardites micellus, and Tivela sp. were observed adhered on the tube of Arachnanthus sp., while Ervilia nitens, Basterotia elliptica, and Musculus lateralis, were observed adhered on the tubes of Isarachnanthus nocturnus.

Shells of Sphenia fragilis, Ervilia nitens and Musculus lateralis were observed upon the tubes of Ceriantheomorphe brasiliensis, and shells of Macomopsis melo, were observed covering considerable areas of the tube of Ceriantheomorphe sp.

The only area on the tube of Ceriantheopsis americana where Ceriello et al. observed the presence of Mollusc shells, was on its slender end that was vertically inserted into the soft bottom. All specimens observed were Cumingia lamellosa, and these were found in high amounts and firmly attached to the tube.

Ceriello et al. observed 29 Peracaridans, belonging to 8 families, including 5 Amphipod species, 2 Isopod species and 1 Tanaidacean species on the tubes of three Ceriantharian species.

Crustacea and Polychaeta found in/on Ceriantharian tubes. (A) Monocorophium acherusicum (B) Idotea balthica (C) Cymadusa filosa (D) Paranthura urochroma (E) Photis sarae, female and male, respectively (F) Ampelisca burkei (G) Chondrochelia savignyi (H) Elasmopus pectenicrus (I) Nereis sp. (J) Phyllodocidae, indet. (K) Cirriformia sp. (L) Sternaspis sp. Scale bars: (A)-(H) 1000 μm (I) 2000 μm (J) 600 μm (K) 1000 μm (L) 3000 μm. Ceriello et al. (2020).

Most peracaridans were found in areas far from the Ceriantharian tentacles, thus not easily accessible to the Ceriantharian. No specimen was found inside the tubes or amongst tube layers. On the tubes of Ceriantheomorphe brasiliensis, Ceriello et al. observed the Amphipods Ampelisca burkei, Cymadusa filosa, Elasmopus pectenicrus, and Photis sarae, and the Isopod Paranthura urochroma firmly attached to the tube external wall; both Amphipods and Isopods were surrounded by ptychocyst filaments. Additionally, Ceriello et al. found Tanaidaceans of species Chondrochelia savignyi; however, those were free from ptychocyst filaments and were not firmly attached. Monocorophium acherusicum (Amphipoda) and Idotea balthica (Isopoda) were also found surrounded by ptychocyst filaments and attached to the external wall of the tube of Ceriantheopsis lineata. One specimen of Photis sarae was noted amongst Algae thalli covering the tube of Isarachnanthus nocturnus. It is noteworthy that the amphipod was not directly attached to the tube, but instead it was freely on its surface.

A total of 122 Polychaetes, including 17 families and 26 species, were found in or on tubes of six species of Ceriantharia. Some of the specimens were not possible to identify further than family or genus, as they were fragmented or in poor condition.

Ceriello et al. observed one specimen of Lysilla loveni (Terebellidae), two Cirratulids, two Paraonids and two Syllids in between layers of the tube of Botrucnidifer norvegicus. On the external wall of the tube of Ceriantheomorphe brasiliensis, Ceriello et al.found Cirratulids (Cirriformia spp.), Eunicids (Lysidice spp.), nereidids (Neanthes sp.), Syllids (Exogone spp., Myrianida sp. and Syllis prolifera), and Spionids (Aonides sp. and Dipolydora spp.), and one specimen each of Sabellidae (Branchiomma sp.), Flabelligeridae (Brada sp.), Magelonidae (Magelona sp.), Polynoidae (Malmgreniella sp.), Capitellidae (Mediomastus spp.), and Phyllodocidae. Only some specimens had ptychocyst filaments surrounding them and keeping them firmly attached to the tube. Ceriello et al. observed Dipolydora spp. amongst Algae thalli covering this tube, as well as in between folds of layers of the tube of Ceriantheomorphe brasiliensis from Guanabara Bay.

The heavy tubes of Ceriantheopsis lineata showed many perforations that were occupied by either deeply or superficially burrowed Polychaetes between some layers. Beneath layers, we observed some Spionids (Dipolydora spp.) and single specimens of Capitellid (Mediomastus spp.), Cirratulid (Cirriformia spp.), and Oenonid (Notocirrus spp.). The removal of layers also revealed empty boring holes under them. Moreover, Ceriello et al. found Syllis garciai (Syllidae) and one Phyllodocid on the tube surface, surrounded by ptychocyst filaments and mucus, respectively.

Some Parasabella sp., Lysidice spp., Cirriformia spp., and Spirobranchus sp. were found amongst algae thalli partially covering one of the tubes of Isarachnanthus nocturnus. However, they were not attached to the tube and neither had ptychocyst filaments surrounding them. Additionally, Ceriello et al. observed Notocirrus spp. on the surface of this tube.

Ceriello et al. observed one maldanid on the surface of the tube of Ceriantheomorphe sp., as well as large Nereis sp. partially burrowed, and small groups of Sternaspis sp. (3 specimens each group) both superficially anchored and deeply burrowed into tube layers.

Finally, Ceriello et al. found 36 Notocirrus spp. and two syllids on tubes of Pachycerianthus schlenzae, either burrowed between layers or attached to the surface of the tubes. In both cases, there were some specimens coated by their own mucus, but none was firmly attached to the tubes.

There have been some previous studies on the presence of marine invertebrates anchored on Ceriantharian tubes, with results suggesting that they are a suitable option as a consolidated structure for the settlement in unconsolidated bottoms. Ceriello et al.'s results not only corroborate the use of ceriantharian tubes as alternative substrates for other organisms, but also indicate a different anchoring method for species of the three phyla evaluated, Mollusca, Arthropoda (Crustacea) and Annelida (Polychaeta). Furthermore, they suggest possible benefits acquired by species on Ceriantharian tubes, discuss the use of mollusc shells in ceriantharian tube construction, and report new location records for six taxa.

Ceriello et al. did not observe whether Peracaridans and Polychaetes voluntarily settle on Ceriantharian tubes or are incorporated into the tubes by the Ceriantharians. In spite of this, their results show that most of these specimens were found in areas of the tubes where the tentacles of the Ceriantharian could not easily reach them. Thus, it is most likely that these species have actively recruited this alternative substrate than have been incorporated into it by the actions of the Ceriantharian. As Ceriello et al. could not evaluate this possibility, this hypothesis cannot be excluded.

Ptychocyst filaments are the most common material in Ceriantharian tubes. Notably, most Amphipods and Isopods firmly anchored to Ceriantharian tubes were surrounded by filaments (e.g. Ampelisca burkei, Cymadusa filosa, Idotea balthica, Monocorophium acherusicum, Paranthura urochroma, and Photis sarae), while some other specimens, such as Chondrochelia savignyi, were not. Likewise, some Polychaetes were observed surrounded by filaments (e.g. Syllis garciai) and thus firmly anchored, while others were coated by their own mucus (e.g. Phyllodocids and Notocirrus spp.) and only superficially anchored. It has been suggested that ptychocyst filaments have adhesive properties and our observations support this suggestion, as it is likely that the adhesive property of ptychocyst filaments is used by Peracaridans and Polychaetes as an anchoring method to settle on Ceriantharian tubes. Otherwise, specimens not surrounded by ptychocyst filaments must have alternative anchoring methods to keep them on tubes.

Crustaceans, Tubeworms and Ceriantharians often acquire shelter against predators in self-built-tubes which may be rigid, as in some Cirratulids, Sabellids and Serpulids. Ceriello et al. observed the Polychaetes Lysidice spp. anchored on Ceriantharian tubes. As members of this genus commonly excavate galleries or temporarily occupy empty galleries/tubes of other organisms, it is possible that Lysidice spp. use Ceriantharian tubes as alternative habitats.

Tube-dwelling Amphipods, Isopods, and Tanaidaceans usually burrow directly into the soft bottom, forming mucous tubes for habitation. For instance, the Amphipod Photis sarae was observed anchored on tubes of Isarachnanthus nocturnus and Ceriantheomorphe brasiliensis. However, this species is usually found in soft tubes built with mucus, small sediments and, sometimes, living organisms (e.g. Algae), similar to Ceriantharia. Ceriello et al. also observed other tube-dwelling Peracaridans coated by ptychocyst filaments and attached to the surface of Ceriantharian tubes, suggesting that, by using Ceriantharian tubes, Peracaridans can be sheltered, without the necessity of building their own tubes.

Mollusc shells were observed on all Ceriantharian tubes examined. However, the absence of periostracum coating these shells suggests that Ceriantharians do not shelter living Molluscs, but instead they adhere empty shells to their tubes, using them as a relevant component for the tube construction. The addition of Mollusc shells and other sediment remains as tube constituents may reinforce the tube, increasing its resistance and, thus, having an architectural role. Moreover, the external surfaces of all shells were usually very worn, indicating that they were part of the seafloor sediment rather than part of living assemblages. Although Ceriello et al.'s data do not allow them to assess how the shells were obtained during tube construction, future studies would be useful to provide such information (e.g. is there any special behavior associated with inclusion of Mollusc shells?) and to examine if it is possible that Ceriantharian tubes shelter living Molluscs.

It has been suggested that empty Mollusc shells enable the understanding of biodiversity patterns of Mollusca fauna at a specific site and can thus be used to provide data on ecological and evolutionary timescales. Accordingly, a similar role could be attributed to the accumulation of shells in Ceriantharian tubes, reflecting the species richness of living Molluscs in the surrounding habitat.

This is the first record of Microgaza rotella (Mollusca) and Brada sp. (Polychaeta) in Laje de Santos, and Photis sarae (Peracarida) in São Sebastião and Laje de Santos, São Paulo State, in southeastern Brazil. To date, Microgaza rotella had been reported as occurring from the southeastern United States to northern Brazil, and, since that there have been no other records in literature regarding this species in southeastern Brazil Microgaza rotella may occur naturally at this location (Laje de Santos) and may be rare or allochthonous (i.e. originated in a region other than where it was found) and transported by other species. Brada had been previously reported in Brazil only from Ubatuba City, while Photis sarae had only been previously reported in Rio de Janeiro State.

This is also the first record of Dipolydora in Rio de Janeiro State, and Notocirrus spp. and Syllis garciai in Espírito Santo State. Dipolydora had only been previously reported from Brazil in São Paulo, Paraná and Espírito Santo States. Notocirrus had been reported occurring in São Paulo, Rio de Janeiro, Paraná and Bahia States, while Syllis garciai had only been previously reported in São Paulo State.

It is noteworthy that Lysilla loveni (Polychaeta) was found on the tube of a Nordic Ceriantharia species, Botrucnidifer norvegicus. This Polychaete species has only rarely been found and usually as single occurrences scattered along the Norwegian coast.

Biogenic structures, such as Ceriantharian tubes, play a major role in altering community structure, thus affecting species richness and individual abundances. Tubes may affect the stability of the sea bottom and provide refugia from predation, as well as surfaces for the recruitment of benthic organisms. In fact, species abundance and richness have been observed to be greater around or on tubes than in areas without tubes. Ceriello et al. did not compare the fauna from Ceriantharian tubes to that from the surrounding sea bottoms however, their results demonstrate that Ceriantharian tubes appear to be suitable alternative substrates for numerous species, especially tubicolous and infaunal invertebrates that usually spend much energy burrowing into sediments or anchoring on fixed or mobile habitats while seeking shelter. Moreover, other than shelter, residents on and in Ceriantharian tubes may also acquire protection. Therefore, the tubes of Ceriantharia may play an important role as small-scale biodiversity hotspots.

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