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Research Article
Molecular data for Crenavolva species (Gastropoda, Ovulidae) reveals the synonymy of C. chiapponii
expand article infoBastian Reijnen
‡ Naturalis Biodiversity Center, Leiden, Netherlands
Open Access

Abstract

During fieldwork in Indonesia and Malaysia, eight lots containing 33 specimens belonging to the genus Crenavolva (Ovulidae) were collected. Species were initially identified as C. aureola, C. chiapponii, C. striatula and C. trailli, respectively. For C. chiapponii this is the second record. In contrast to the ecological data available from the original description of this species, it was found in shallow water on a gorgonian host coral, i.e. Acanthogorgia sp. A molecular analysis based on COI and 16S mtDNA markers, including sequence data obtained from GenBank, showed that C. chiapponii should be considered a junior synonym of C. aureola and that previously identified ovulid specimens are probably misidentified.

Keywords

Acanthogorgia, host association, molecular phylogeny, Octocorallia, 16S, COI

Introduction

The nominal taxon Crenavolva was introduced as a subgenus by Cate (1973), together with the subgenera Crenavolva, Cuspivolva and Serratovolva. In the most recent overview regarding Ovulidae these three taxa are considered genera (Lorenz and Fehse 2009). At present 18 nominal species are recognized within Crenavolva (Rosenberg 2014), most of which are considered rare (Lorenz and Fehse 2009). These species are considered rare because few specimens have been collected, probably because they occur at depths greater than standard recreational diving depth of c. 30 m and/or are only known from a limited geographical area, usually just the type locality. This also accounts for C. chiapponii Lorenz & Fehse, 2009, which is only known from Balicasag Isl., Bohol, Philippines, where specimens were trawled from 70–120 m depth and, therefore, were considered rare and confined to deeper water (Lorenz and Fehse 2009). Like almost all other ovulids, species of Crenavolva are associated with octocoral hosts (Schiaparelli et al. 2005; Reijnen 2010) belonging to several families (e.g. Melithaeidae, Ellisellidae, Subergorgiidae and Plexauridae). However, the host species are usually not collected or are disregarded and therefore unknown, which is also the case for C. chiapponii.

Molecular data (16S and COI) obtained from Crenavolva was used by Meyer (2003) to root the phylogeny of the Cypraeidae. Later, the 16S sequence data were used by Schiaparelli et al. (2005) to produce the first molecular phylogenetic reconstruction of the Ovulidae, which included two Crenavolva species: C. cf. rosewateri (Cate, 1973) and C. tokuoi Azuma, 1989. In the present study, material of four additional nominal Crenavolva species, amongst other ovulids, have been used to reconstruct a phylogeny. The newly acquired molecular data are for C. aureola (Fehse, 2002), C. chiapponii Lorenz & Fehse, 2009, C. striatula (Sowerby I, 1828) (type species), and C. trailli (Adams, 1855). In addition to this phylogenetic reconstruction, data on host species and distributional records are given for this group of rarely recorded ovulid snails.

Materials and methods

Collection and identification

During fieldwork in Indonesia (Halmahera, Ternate; Sulawesi, Lembeh Strait) and Malaysia (Borneo, Semporna and Kudat) specimens of Crenavolva species were collected by SCUBA diving (Table 1). The snails and their octocoral hosts were photographed in situ (Fig. 1) whenever possible and subsequently fixed in 80% ethanol. The holotype of C. chiapponii was studied at the Muséum national d’Histoire naturelle (MNHN) in Paris. For the identification of the other ovulid species, Cate (1973), Fehse (2002b) and Lorenz and Fehse (2009) were used. For the identification of the host species, microscopy slides of their calcareous skeletal parts (sclerites) were made by dissolving the samples in a 4% solution of household bleach. The residual sclerites were rinsed with tap water followed by demineralised water before mounting on a slide or on a stub for Scanning Electron Microscopy (SEM). Stubs with sclerites were coated with Au/Pd before SEM images were made with a JEOL 6480 LV. Identification of the octocorals to genus level was based on Stiasny (1947) and Fabricius and Alderslade (2001).

Figure 1.

A In situ image of Crenavolva aureola (Fehse, 2002) (RMNH.MOL.164209) and B C. chiapponii Lorenz & Fehse, 2009 (RMNH.MOL.164211) on Acanthogorgia sp. at Halmahera, Indonesia at 21 m and 17 m depth respectively.

Specimens used in the analyses, including locality, host, and GenBank accession data.

Collection number Species Locality (Locality code) Coordinates Date collected Host species GenBank Accession number (16S; COI) Reference
RMNH.MOL.164072 Crenavolva aureola (Fehse, 2002) Malaysia, Semporna, Si Amil Island (SEM.16) 4°19'02.1"N; 118°52'30.7"E 4-12-2010 Acanthogorgia sp. KP033143; KP033151 This publication
RMNH.MOL.164085 Crenavolva aureola (Fehse, 2002) Indonesia, Halmahera, Tidore, N of Desa Rum (TER.18) 0°44'35.8"N; 127°23'06.3"E 4-11-2009 Acanthogorgia sp. KP033144; KP033152 This publication
RMNH.MOL.164209 Crenavolva aureola (Fehse, 2002) Indonesia, Halmahera, Tanjung Ratemu (S of river)(TER.21) 0°54'24.7"N; 127°29'17.7"E 5-11-2009 Acanthogorgia sp. KP033148; KP033156 This publication
RMNH.MOL.164211 Crenavolva chiapponii Lorenz & Fehse, 2009 Indonesia, Halmahera, Tanjung Ratemu (S of river)(TER.27) 0°54'44.5"N; 127°29'09.9"E 8-11-2009 Acanthogorgia sp. KP033157 This publication
RMNH.MOL.164217 Crenavolva chiapponii Lorenz & Fehse, 2009 Indonesia, Lembeh, Tanjung Kusukusu (LEM.31) 1°27'13.8"N; 125°14'13.0"E 16-2-2012 Acanthogorgia sp. KP033149; KP033158 This publication
RMNH.MOL.164062 Primovula rosewateri (Cate, 1973) Malaysia, Semporna, Kulapuan Island 2, N side (SEM.31) 4°32'07.4"N; 118°50'18.2"E 9-12-2010 Paratelesto sp. KP033142; KP033150 This publication
RMNH.MOL.164186 Crenavolva striatula (Sowerby I, 1828) Malaysia, Sabah, S Pulau Banggi, E Molleangan Besar Island, (TMP.37) 7°05'07.2"N; 117°03'33.8"E 19-9-2012 Echinogorgia sp. KP033146; KP033154 This publication
RMNH.MOL.164144 Crenavolva trailli (Adams, 1855) Malaysia, Sabah, Kalang, (TMP.41) 6°59'48.1"N; 117°03'13.4"E 18-9-2012 Subergorgia sp. KP033145; KP033153 This publication
RMNH.MOL.164189 Crenavolva trailli (Adams, 1855) Malaysia, Sabah, Kalang, (TMP.41) 6°59'48.1"N; 117°03'13.4"E 18-9-2012 Paraplexaura sp. KP033147; KP033155 This publication
- Crenavolva cf. rosewateri (Cate, 1973) Philippines, Bohol, Balicasag Island - - - AY161394; AY161627 Meyer 2003
- Crenavolva tokuoi Azuma, 1989 Philippines, Bohol, Balicasag Island - - - AY161390; AY161623 Meyer 2003
- Primovula beckeri (Sowerby III, 1900) Indonesia, Sulawesi - - - AJ868555; - Schiaparelli et al. 2005
- Ovula ovum (Linnaeus, 1758) Indonesia, Sulawesi, Spermonde Archipelago - - - AY161399; AY161632 Meyer 2003

Barcoding Ovulidae

Specimens were barcoded for the COI barcoding region and for additional phylogenetic research also for the 16S marker. Tissue samples obtained from the foot and/or mantle were extracted with the Machery-Nagel DNA extraction kit on a KingFisher Flex. The standard COI barcoding primers by Folmer et al. (1994) and the Palumbi (1996) 16S primers were used. PCR amplification was performed on a C1000 Touch Thermal Cycler (Bio-RAD). Sequencing of the PCR products was performed at Macrogen Europe on an ABI 3730xl Automated Sequencer. Sequences were edited in Sequencher 4.10.1 and aligned with GUIDANCE (Penn et al. 2010) using the MAFFT algorithm (Katoh et al. 2005). Selecting an evolutionary model was done with jModeltest based on the Akaike Information Criterion score. MEGA 6.0.6 (Tamura et al. 2013) was used to perform Maximum Likelihood (ML) and Maximum Parsimony (MP) analyses and to calculate p-distances. Bayesian analyses were performed in MrBayes 3.2.0 (Ronquist and Huelsenbeck 2003). MrBayes was run for 4,000,000 generations with six chains. Data were sampled every 100 generations. Sequence data for Ovula ovum (Linnaeus, 1758) from GenBank was used as an outgroup. GenBank data for Crenavolva cf. rosewateri (Cate, 1973), C. tokuoi Azuma, 1989 and Primovula beckeri (Sowerby III, 1900) was also included in the phylogenetic analyses.

Results

Collecting and morphology

Eight lots, containing 33 specimens representing four nominal Crenavolva species (C. aureola, C. chiapponii, C. striatula and C. trailli) were collected in Indonesia and Malaysia (Table 1; Fig. 2). For C. chiapponii this is the first record from shallow water. The specimens were assigned to these nominal species based on shell shape (rhomboid, inflated or slender) and the colour bands on the dorsum, which in case of C. striatula were also present on the labrum. For C. aureola and C. chiapponii the absence or presence of a white dorsal band on the shell is allegedly the most obvious character to distinguish the species. After examination of the illustrations presented by Lorenz and Fehse (2009) and the newly collected material, minor morphological differences (strongly or weakly pronounced dentation, keeling angle, strongly or weakly produced funiculum, position of the widest part of the shell) do not clearly separate between C. aureola and C. chiapponii and can be considered morphological variation in a single species. The soft tissue colouration of both C. aureola and C. chiapponii is very similar (e.g. Fig. 1; Lorenz and Fehse 2009: A106, A107 p. 527). Both have a semi-transparent mantle which is entirely covered with small, irregularly placed, white dots, and both have a completely black or white foot, black tentacles with white tips, and a black siphon.

Figure 2.

Dorsal and ventral views of shells. A Holotype of Crenavolva chiapponii Lorenz & Fehse, 2009 (MNHN 21244) B C. chiapponii Lorenz & Fehse, 2009 (RMNH.MOL.164211) C C. chiapponii Lorenz & Fehse, 2009 (RMNH.MOL.164217) D C. aureola (Fehse, 2002) (RMNH.MOL.164085) E C. aureola (Fehse, 2002) (RMNH.MOL.164072) F C. aureola (Fehse, 2002) (RMNH.MOL.164209) G C. trailli (Adams, 1855) (RMNH.MOL.164144) H C. striatula (Sowerby I, 1828) (RMNH.MOL.164186) I Primovula rosewateri (Cate, 1973) (RMNH.MOL.164062). Scale bars: 5 mm.

Molecular data

Nine specimens representing five species were sequenced for COI and 16S. For one sample of C. chiapponii (RMNH.MOL.164211) the 16S marker could not be amplified. Sequences were concatenated and aligned (GUIDANCE alignment score: 0.965034) which resulted in an alignment length of 1080 base pairs per specimen including indels. Sequences obtained from GenBank are slightly shorter (~40 base pairs), these missing base pairs were coded as ‘missing data’. The program jModeltest yielded in HKY+G as most optimal evolutionary model. This evolutionary model was implemented in the Bayesian and ML analysis. The results from the different phylogenetic reconstructions were congruent, therefore only the ML tree is shown (Fig. 3).

Figure 3.

Maximum Likelihood cladogram with support values for the ML/MP/BP analyses. Numbers preceding the species names represent RMNH.MOL. collection numbers of Naturalis Biodiversity Center; species names without numbers are obtained from GenBank for which additional data can be found in Table 1.

In the phylogenetic reconstructions, specimens of Crenavolva striatula and C. tokuoi form an unresolved trichotomy with the other Crenavolva specimens. The two Primovula species cluster together and are well-supported sister species to all the Crenavolva species (with C. striatula as type species for the genus). This implies that the Crenavolva species used herein form a monophyletic group. The clustering of two C. trailli specimens is highly supported. Another well-supported clade holds three nominal species: Crenavolva aureola, C. chiapponii and C. cf. rosewateri. The pairwise p-distances between these three species are very low (16S: 0.2%; COI: 0.7%; concatenated: 0.9%). In contrast, the sequence divergence between C. trailli and the C. chiapponii / C. aureola clade is almost ten times larger (16S: 5.2%; COI: 8.7%; concatenated: 8.2%). The sequence divergence between the two C. trailli specimens (16S: 0.6%; COI: 0.8%; concatenated: 0.8%) is almost equal to that between C. aureola and C. chiapponii. With the help of the Automatic Barcode Gap Discovery tool (ABGD) (Puillandre et al. 2011), the data were analysed to identify the MOTU’s within the dataset. The results of this analysis showed that the barcode gap to identify the different species is 5–6% sequence divergence. This resulted in five groups containing the following species: 1, C. aureola, C. chiapponii, C. cf. rosewateri; 2, C. trailli; 3, C. tokuoi; 4, C. striatula; 5, P. rosewateri. One of the samples obtained from GenBank, viz. Crenavolva cf. rosewateri (= Primovula cf. rosewateri), clusters surprisingly within the clade containing C. aureola and C. chiapponii and not with the other Primovula rosewateri specimen. Instead, Primovula beckeri proves to be identical to the newly sequenced specimen of Primovula rosewateri from Malaysia.

Octocoral hosts

Almost all Ovulidae species are associated with Octocorallia hosts. By examining the sclerites and the habitus of the host corals, several new host species for ovulids of the genus Crenavolv a could be identified. An overview of previously identified host species and new records is provided in Table 2. Some of the former host identifications were published with obsolete generic names, and therefore their names in the current literature are also provided. Before C. chiapponii was synonymised, Acanthogorgia would have been a new host record. Yet, Reijnen (2010) already recorded Acanthogorgia sp. as a host for C. aureola and therefore it is not a new host record. Morphologically at least two different species of Acanthogorgia could be distinguished but these could not be identified since a revision of the family Acanthogorgiidae is lacking.

Literature overview of the octocoral hosts of selected Crenavolva species including new records. Updated names of the octocoral hosts are provided between parentheses.

Ovulid species Host genera Reference
Crenavolva aureola Euplexaura; Astromuricea (= Echinogorgia); Acanthogorgia Lorenz and Fehse 2009; Reijnen 2010
Crenavolva chiapponii (= C. aureola) Acanthogorgia this publication; Reijnen 2010
Crenavolva striatula Ellisella; Euplexaura; Echinogorgia Lorenz and Fehse 2009; Yamamoto 1973; Cumming 1997; Mase 1989;
Crenavolva trailli Echinogorgia; Anthoplexaura (= Astrogorgia); Plexauroides (= Echinogorgia); Euplexaura; Subergorgia Goh et al. 1999; Mase 1989
Primovula rosewateri Subergorgia; Dendronephthya; Stereonephthya; Paratelesto Goh et al. 1999; Lorenz and Fehse 2009; this publication
Primovula beckeri Acanthogorgia; Acabaria (= Melithaea); Unicella [sic] (= Eunicella); Lophogorgia (= Leptogorgia) Schiaparelli et al. 2005; Lorenz and Fehse 2009

Furthermore, examination of the ovulid species and their octocoral hosts revealed that in two instances individuals formerly identified as C. chiapponii and C. aureola would have co-occurred on the same host coral, in both cases Acanthogorgia sp.

Discussion

Based on the molecular data and morphological observations listed above, C. chiapponii is considered a junior synonym of C. aureola. The systematic account is therefore as follows:

Systematic part

Family Ovulidae Fleming, 1822
Genus Crenavolva Cate, 1973

Crenavolva aureola (Fehse, 2002)

Primovula aureola Fehse 2002: 37, pl. 1, fig. 1

Delonovolva formosa. — Gosliner et al. 1996: 136, fig. 469. Not Delonovolva formosa (Sowerby II in Adams and Reeve 1848) [= Cuspivolva formosa (Sowerby II in Adams and Reeve 1848)]

Primovula sp. — Coleman 2003: 51, fig. (Ovul: 121).

Crenavolva chiapponii Lorenz and Fehse 2009: 69, pl. 74, fig. 7–11.

The occurrence of C. chiapponii (= C. aureola) on Indonesian shallow water coral reefs would have represented new distribution records, both geographically and bathymetrically, before it was synonymised. However C. chiapponii proved to be a junior synonym of C. aureola and the new distribution records fall within the distribution range already known for C. aureola. Apparently, the dorsal white band and the minor morphological differences in shell shape are not indicative of species-level differences between C. aureola and C. chiapponii.

Molecular data

The species Primovula rosewateri was previously placed in the genus Crenavolva by Cate (1973) but Fehse (2002a) moved it to Primovula, primarily based on the triangular shape of the funiculum. The results of the molecular analyses (Fig. 3) support this decision. There is great genetic similarity between C. cf. rosewateri (= Primovula cf. rosewateri) obtained from GenBank, and C. aureola. However, the specimen from GenBank was collected from Balicasag Island, near Bohol, Philippines, which is the type locality of C. chiapponii. This location is approximately 85 km from Mactan Island of Cebu, Philippines which is the type locality of C. aureola. It is not unlikely that the so-called C. cf. rosewateri from GenBank (AY161394 (16S), AY161627 (COI)) was misidentified and actually represents C. aureola. Moreover, the newly sequenced specimen of P. rosewateri from Malaysia convincingly clusters with Primovula beckeri. According to Lorenz and Fehse 2009, P. beckeri has an E African distribution and was originally described from South Africa. The specimen obtained from GenBank is from Sulawesi, Indonesia (Schiaparelli et al. 2005). It is therefore unlikely that this sequence represents P. beckeri but instead is the quite similar species from the central Indo-Pacific, P. rosewateri.

Host species and distribution records

The ranges of the presently discussed species all fit within the Coral Triangle (see Hoeksema 2007) and depend on the ranges of their host species. Species of the genus Acanthogorgia are not unique hosts for just Crenavolva spp. Reijnen (2010) already mentioned Acanthogorgia spp. as a host for Dentiovula eizoi Cate & Azuma, 1973 (in Cate 1973) and D. colobica (Azuma & Cate, 1971). Acanthogorgia species and their ovulid associates are both known to occur from shallow to deep water in the Coral Triangle. In an overview of the Acanthogorgiidae by Stiasny (1947) the deepest record for an Acanthogorgia species is 4239 m, collected SE of Seram, Indonesia (Acalycigorgia densiflora = Acanthogorgia densiflora (Kükenthal & Gorzawsky, 1908). Nevertheless, Stiasny (1947) doubts the identification and compared it to congeneric species which are found in waters not exceeding 400 m depth. As a result Stiasny (1947) doubts the entire record. Therefore the deepest reliable record for an Acanthogorgia species in the Malayan Archipelago is 1254 m for Acanthogorgia multispina (Kükenthal & Gorzawsky, 1908). The deepest record for Crenavolva species is from approximately 1000 m, which is the deepest record for any ovulid species found to date (Lorenz and Fehse 2009).

Acknowledgements

Many thanks to Dr Bert W. Hoeksema who organized the Ternate and Lembeh Strait expedition together with Ir M.I. Yosephine Tuti Hermanlimianto under the umbrella of E-Win (Ekspedisi Widya Nusantara). LIPI Ternate and LIPI Bitung are acknowledged for accommodating the research at their field stations. LIPI and RISTEK granted research permits. The Semporna Marine Ecological Expedition (SMEE2010) was jointly organized by WWF-Malaysia, Universiti Malaysia Sabah’s Borneo Marine Research Institute, Naturalis Biodiversity Center and Universiti Malaya’s Institute of Biological Sciences, while research permission was granted by the Economic Planning Unit, Prime Minister’s Department, Economic Planning Unit Sabah, Sabah Parks and Department of Fisheries Sabah. The MV Celebes Explorer accommodated the research in Semporna. The 2012 Tun Mustapha Park expedition (TMP) was jointly organized by WWF-Malaysia, Universiti Malaysia Sabah (UMS), Sabah Parks and Naturalis Biodiversity Center, the Netherlands. The research permits were granted by the Economic Planning Unit, Prime Minister’s Department Malaysia and Sabah Biodiversity Centre. Both expeditions to Malaysia were co-organised by Ms Zarinah Waheed and WWF Malaysia, which was greatly appreciated. Dr Philippe Bouchet and Ms Virginie Heros were so kind to accommodate a visit to Muséum national d’Histoire naturelle (MNHN) in Paris to investigate the Ovulidae (type) collections. Dr Leendert P. van Ofwegen kindly provided help by identifying the octocoral hosts and Sancia van der Meij was a perfect dive buddy and ovulid hunter. Sequencing of the barcoding region of the ovulids was part of one of the barcoding initiatives within the Naturalis Biodiversity Center. Funding for fieldwork was provided by the Jan-Joost ter Pelkwijkfonds and A.M. Buitendijkfonds (Naturalis Biodiversity Center), Malacological Society of Australasia and the Percy Sladen Fund. I also would like to thank Prof Dr Catherine S. McFadden, an anonymous reviewer and Dr Thierry Backeljau for their constructive comments and remarks which improved the manuscript greatly.

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