Do syntopic host species harbour similar symbiotic communities? The case of Chaetopterus spp. (Annelida: Chaetopteridae)

PeerJ, Feb 2017

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.

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Do syntopic host species harbour similar symbiotic communities? The case of Chaetopterus spp. (Annelida: Chaetopteridae)

Do syntopic host species harbour similar symbiotic communities? The case of Chaetopterus spp. (Annelida: Chaetopteridae) Temir A. Britayev1 , Elena Mekhova1 , Yury Deart1 and Daniel Martin2 1 Severtzov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russian Federation 2 Department of Marine Ecology, Centre d’Estudis Avançats de Blanes (CEAB–CSIC), Blanes, Catalunya, Spain ABSTRACT Submitted 10 October 2016 Accepted 21 December 2016 Published 2 February 2017 Corresponding author Daniel Martin, Academic editor James Reimer Additional Information and Declarations can be found on page 19 DOI 10.7717/peerj.2930 Copyright 2017 Britayev et al. 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. Distributed under Creative Commons CC-BY 4.0 Subjects Biodiversity, Ecology, Marine Biology, Zoology OPEN ACCESS Tergipedidae, Competition, South China Sea, Vietnam Keywords Symbiotic community structure, Polychaeta, Carapidae, Porcellanidae, Pinnotheridae, How to cite this article Britayev et al. (2017), Do syntopic host species harbour similar symbiotic communities? The case of Chaetopterus spp. (Annelida: Chaetopteridae). PeerJ 5:e2930; DOI 10.7717/peerj.2930 INTRODUCTION During the last few decades, significant efforts have been undertaken to study the species composition and structure of marine symbiotic communities associated with different hosts taxa such as scleractinian corals (Hoeksema, Van der Meij & Fransen, 2012; Stella, Jones & Pratchett, 2010), echiurans (Anker et al., 2005), hermit crabs (Williams & McDermott, 2004) and echinoderms (Barel & Kramers, 1977). Despite this being an interesting aspect of marine ecosystems’ functioning and the need to fill in existing gaps in related knowledge, the current focus of scientific interests have shifted to ecological and evolutionary aspects of the establishment of symbiotic communities (Baeza, 2015; Duffy, 2002; Thiel & Baeza, 2001). Accordingly, host characteristics (morphological, ecological and physiological) have been considered as some of the most important parameters driving these processes (e.g., Abele & Patton, 1976; Deheyn, Lyskin & Eeckahaut, 2006; Goto & Kato, 2011). The coexistence of potential hosts that are taxonomically closely related (thus sharing similar morphological and physiological characteristics) may facilitate host switching, leading to the infestation of different host species by the same species of symbiont, as reported for example in freshwater fish (Poulin, 1998). Accordingly, we may expect the composition of symbiotic communities established on closely related hosts to be similar. Hence, sympatric coral species belonging to the same family harbour symbiotic communities more similar than those belonging to different families (Stella, Jones & Pratchett, 2010), while the symbiotic communities associated with two starfish hosts from the same family living in the same area have nearly identical species composition (Antokhina, Savinkin & Britayev, 2012). There seems to be a correlation between increasing taxonomic proximity between hosts and a higher similarity in species composition of the respective symbiotic communities. In other words, we could expect that closely related (i.e., belonging to the same genus) host species sharing the same habitat would harbour very similar (or even identical) symbiotic communities. Therefore, the current study investigated the symbiotic communities associated with two species of Chaetopterus in Nhatrang Bay (Vietnam), to assess whether this hypothesis may apply to this particular situation. These two species of Chaetopterus appeared to be excellent subjects for the intended comparison due to their highly similar morphology. In fact, the genus has long been regarded as monospecific and, to date, the morphological identification of species is still considered as rather complex (Britayev & Martin, 2016; Nishi, Hickman Jr & Bailey-Brock, 2009; Petersen, 1984a; Petersen, 1984b). Moreover, these two species share the same habitat and, thus the influence of environmental parameters can be excluded as influential factors on the associated symbiotic communities. The genus Chaetopterus (Annelida: Chaetopteridae) includes relatively large animals (up to 20–25 cm in length) living in roughly U-shaped tubes embedded into soft sediments or attached to hard surfaces in shallow waters of temperate and tropical seas (Britayev & Martin, 2016). Morphologically, they are highly adapted for feeding on plankton using complex mucus-net based mechanisms (Enders, 1909). They are also well known as hosts harbouring numerous symbiotic associates (often including complex communities) inside their parchment-like tubes. These tubes provide well-protec (...truncated)


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Temir A. Britayev, Elena Mekhova, Yury Deart, Daniel Martin. Do syntopic host species harbour similar symbiotic communities? The case of Chaetopterus spp. (Annelida: Chaetopteridae), PeerJ, 2017, pp. e2930, Issue 5, DOI: 10.7717/peerj.2930