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Occurrence of Isarachnanthus (Cnidaria: Anthozoa: Ceriantharia) at Ascension Island: a test of hypothesis

Published online by Cambridge University Press:  03 April 2014

Sérgio N. Stampar*
Affiliation:
Faculdade de Ciências e Letras, UNESP-Univ Estadual Paulista, Assis, Departamento de Ciências Biológicas, Laboratório de Biologia Aquática–LABIA, Avenida Dom Antonio, 2100, Assis, SP, 19806-900, Brazil
André C. Morandini
Affiliation:
Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, Rua do Matão, trav. 14, 101, São Paulo, SP, 05508-090, Brazil
*
Correspondence should be addressed to: S.N. Stampar, Faculdade de Ciências e Letras, UNESP-Univ Estadual Paulista, Assis, Departamento de Ciências Biológicas, Laboratório de Biologia Aquática–LABIA, Avenida Dom Antonio, 2100, Assis, SP, 19806-900, Brazil email: stampar@assis.unesp.br
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Abstract

A theory that an ancient population of Isarachnanthus from the eastern Atlantic originated the current species is discussed. Based on analysis of DNA barcoding and cnidome it was possible to identify some specimens from Ascension Island. These specimens were identified as Isarachnanthus maderensis, since the divergence of DNA barcoding was very small and the cnidome data agreed with published data. This material permitted an enhanced discussion about the origin of this population.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

INTRODUCTION

Ceriantharia taxonomy has been an issue since early studies in the 19th Century (e.g. Haime, Reference Haime1854). Many of the characters show clear phenotypic plasticity, and almost nothing is known of this variation within this species (see van Beneden, Reference van Beneden1924). Ceriantharia is a subclass within the class Anthozoa (Stampar et al., Reference Stampar, Maronna, Kitahara, Reimer and Morandini2014). The use of DNA barcoding (5′ end of mtDNA cytochrome c oxidase I (COI)) methods in this class would be virtually impossible with the traditional approaches due to the low variability of mitochondrial DNA between species (Huang et al., Reference Huang, Meier, Todd and Chou2008). However this profile is completely different in Ceriantharia compared to other class members. Mitochondrial DNA shows similar substitution rates to those found in other animal groups (e.g. Medusozoa and/or Bilaterian groups), thus the use of classical methods of DNA bar coding is quite possible (see more in Stampar et al., Reference Stampar, Maronna, Vermeij, Silveira and Morandini2012, Reference Stampar, Maronna, Kitahara, Reimer and Morandini2014).

Isarachnanthus Carlgren, 1924 is a genus of tube forming anemones within the order Ceriantharia which extend their tentacles only during the night (Stampar et al., Reference Stampar, Maronna, Vermeij, Silveira and Morandini2012). Unlike many anthozoan taxa, some ceriantharian species have larval stages with long planktonic lifespans. These planktonic forms confounded earlier researchers who classified them as a group of jellyfish that belong to the other subphylum, Medusozoa (see Rodriguez et al., Reference Rodriguez, Marques, Stampar, Morandini, Christiansen, Genzano and Mianzan2011). The genus Isarachnanthus consists of four species: I. bandanensis (Carlgren, 1924); I. maderensis (Johnson, 1861); I. nocturnus (den Hartog, 1977); and I. panamensis (Carlgren, 1924). A hypothesis about the origin of Pacific and West Atlantic species was raised by Stampar et al. (Reference Stampar, Maronna, Vermeij, Silveira and Morandini2012). The hypothesis stated that the ancestral species originated from the east coast of the Atlantic. This could be verified with the unique occurrence of the species Isarachnanthus maderensis on the coast of Africa. However, the sub-Saharan African coast still remains a large gap in information, and large expeditions have only sampled in some parts of that region (e.g. Zibrowius & Gili, Reference Zibrowius and Gili1990). We had access to some specimens of Isarachnanthus obtained from the oceanic Ascension Island (Figure 1). This record is important because it is an area with no information about Ceriantharia, and the island is under the influence of African ocean currents (see Peterson & Stramma, Reference Peterson and Stramma1991). The individuals were analysed for specific identification and the results discussed in relation to the data available from recent literature (Stampar et al., Reference Stampar, Maronna, Vermeij, Silveira and Morandini2012).

MATERIALS AND METHODS

Ascension Island is an isolated volcanic island in equatorial waters of the South Atlantic Ocean, around 1600 km from the coast of Africa and 2250 km from the coast of South America. Two specimens of Isarachnanthus were collected around the island in September 2011 (MZUSP 001947/001948 and GENBANK KJ469802/KJ46980, respectively). The two specimens were preserved in formalin, but tentacle samples were preserved in ethanol. To study the specimens we followed the methods described by Stampar et al. (Reference Stampar, Maronna, Vermeij, Silveira and Morandini2012, Reference Stampar, Maronna, Kitahara, Reimer and Morandini2014). The barcoding region (COI) was sequenced (535–639 bp) and then compared with data provided by the same authors. Kimura's two-parameter model of base substitution was used to calculate genetic distances in MEGA5 software (Tamura et al., Reference Tamura, Peterson, Peterson, Stecher, Nei and Kumar2011). The maximum likelihood phylogenetic analysis was conducted via RAxML (500 replicates) (random accelerated maximum likelihood analysis) with general time reversible model and gamma rate heterogeneity (GTR + GAMMA) (Stamatakis et al., Reference Stamatakis, Hoover and Rougemont2008). To evaluate nodal support and especially to detect if support values were positively/negatively biased, parametric (aLRT) and non-parametric (SH-aLRT) tests were applied (Anisimova & Gascuel, Reference Anisimova and Gascuel2006; Anisimova et al., Reference Anisimova, Gil, Dufayard, Dessimoz and Gascuel2011). Bootstrap values were computed on RAxML v.7.3.2 (500 pseudoreplicates, same parameters as the original phylogenetic analysis) and other statistical tests were calculated using PhyML v.3.0.1 (Guindon et al., Reference Guindon, Dufayard, Lefort, Anisimova, Hordijk and Gascuel2010; Anisimova et al., Reference Anisimova, Gil, Dufayard, Dessimoz and Gascuel2011). At the same time the measurements of cnidae were compared with those of specimens from type locations of I. maderensis and I. nocturnus (as presented by Stampar et al., Reference Stampar, Maronna, Vermeij, Silveira and Morandini2012).

RESULTS

Based on our analyses (morphology, cnidae and barcode) the specimens from Ascension Island belong to the species Isarachnanthus maderensis (Figure 1). The barcoding data show that the K2P divergence is 0.02–0.07% between specimens from Ascension Island and Madeira Island + Caribbean Sea + off Brazil (Rocas Atoll) but 9–9.6% in comparison with Brazilian + Caribbean Sea specimens of Isarachnanthus nocturnus. Maximum likelihood analyses shows that specimens from Ascension Island are grouped with other specimens of Isarachnanthus maderensis with very consistent support values (Figure 2).

Fig. 1. In situ photographs of specimens of Isarachnanthus maderensis from Ascension Island: (A, B) oral view; (C, D) side view (images: Shallow Marine Surveys Group).

Fig. 2. Phylogenetic reconstruction (maximum likelihood) of the analysed specimens of Isarachnanthus using the mitochondrial marker COI. Numbers on the branches represent the estimated values of maximum likelihood (bootstrap)/SH-aLRT/aLRT. Ascension A and B are the specimens used for the analysis.

The cnidome data from Ascension Island specimens (Table 1) also confirm the similarities with specimens from Madeira Island and off Brazil (Rocas Atoll). The measurements of cnidae capsules of Ascension Island specimens are in the same range as Isarachnanthus maderensis. Furthermore, the most relevant data are the presence of three types of microbasic b-mastigophores on the stomodeum and the column, and the presence of microbasic p-mastigophores on the column. This pattern was only observed in specimens of Isarachnanthus maderensis (see data from Stampar et al., Reference Stampar, Maronna, Vermeij, Silveira and Morandini2012).

Table 1. Cnidome of the studied specimens of Isarachnanthus maderensis from Ascension Island (N = 2 specimens × 30 cnidae).

DISCUSSION

The finding of Isarachnanthus maderensis specimens on Ascension Island provides good evidence in support of the hypothesis that the species Isarachnanthus nocturnus is restricted to the west coast of the Atlantic Ocean, with Isarachnanthus maderensis only occurring on the east coast in the South Atlantic Ocean, as proposed by Stampar et al. (Reference Stampar, Maronna, Vermeij, Silveira and Morandini2012). Isarachnanthus specimens that are driven from the African coast by the South Equatorial Current must be exclusively ‘maderensis’ species (Figure 3). Ascension Island lies exactly under the influence of the South Equatorial Current (Dunbar, Reference Dunbar1984) and probably receives a large amount of larvae derived from African coasts (McCartney et al., Reference McCartney, Keller and Lessios2000). The genus addressed in this study presents planktonic larvae that can be carried by sea currents (Rodriguez et al., Reference Rodriguez, Marques, Stampar, Morandini, Christiansen, Genzano and Mianzan2011). Unfortunately there are no data on the life cycle of this genus, except on the existence of a planktonic larva.

Fig. 3. Distribution pattern/area of Isarachnanthus maderensis in Atlantic Ocean (A).

This study highlights the importance of investigating species distribution, especially considering remote islands. Geographical records on somewhat isolated places are necessary for a better understanding of evolutionary processes, particularly in testing theories already proposed, and in the subsequent understanding of marine populations. Furthermore, this study highlighted that the use of DNA barcoding in Ceriantharia, proposed by Stampar et al. (Reference Stampar, Maronna, Vermeij, Silveira and Morandini2012, Reference Stampar, Maronna, Kitahara, Reimer and Morandini2014) is completely applicable and should be adopted by researchers.

ACKNOWLEDGEMENTS

We are grateful to the Shallow Marine Surveys Group and the South Atlantic Environmental Research Institute for organizing the expedition. We are also very grateful to the Ascension Island Government, the members of staff at the Conservation Centre and Ascension Island Dive Club for their cooperation, accommodation and hospitality. Finally we are grateful to British Forces South Atlantic Islands for their logistic support. We are also thankful to Paul Brickle and Peter Wirtz for comments on the text.

FINANCIAL SUPPORT

The funding for this work came from a grant to the Shallow Marine Surveys Group from the Darwin Initiative (EIDCF012). This work was also partly supported by grants 2012/01771 (S.N.S.), 2010/50174-7 (A.C.M.), São Paulo Research Foundation (FAPESP) and CAPES PROEX and CNPq 301039/2013-5 to A.C.M. and CNPq 481549/2102-9 to S.N.S. This study is a contribution of NP-BioMar, USP.

References

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Figure 0

Fig. 1. In situ photographs of specimens of Isarachnanthus maderensis from Ascension Island: (A, B) oral view; (C, D) side view (images: Shallow Marine Surveys Group).

Figure 1

Fig. 2. Phylogenetic reconstruction (maximum likelihood) of the analysed specimens of Isarachnanthus using the mitochondrial marker COI. Numbers on the branches represent the estimated values of maximum likelihood (bootstrap)/SH-aLRT/aLRT. Ascension A and B are the specimens used for the analysis.

Figure 2

Table 1. Cnidome of the studied specimens of Isarachnanthus maderensis from Ascension Island (N = 2 specimens × 30 cnidae).

Figure 3

Fig. 3. Distribution pattern/area of Isarachnanthus maderensis in Atlantic Ocean (A).

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