Current Status of Indian Opisthobranch Fauna - Springer Link

Chapter 5

Current Status of Indian Opisthobranch Fauna Bhave Vishal and Apte Deepak

Abstract Opisthobranchs are fascinating molluscs with species diversifying not only in colours but also in their specificity of feeding habit and habitat. Historical studies are centred mostly on known species rich localities and are not evenly distributed along all coastal states. Opisthobranchs are among the least studied group of molluscs in India and the work carried out on the opisthobranch fauna is scanty and sparse. Though India has over 8000 km long coastline along nine coastal states and two oceanic archipelagos and have diverse habitats such as coral reefs, sandy shores, rocky patches, mangroves as well as large mud flats; yet records of Indian opisthobranchs are very less. This study revealed that 311 species are known from India distributed over 7 orders, 53 families and 141 genera. Keywords India

History Nudibranch Review Sacoglossa Cephalaspidea

5.1 Introduction Opisthobranchs are fascinating molluscs with species diversifying not only in colours but also in their specificity of feeding habit and habitat. Though India has over 8,000 km large coastline and two oceanic archipelagos with diverse habitats such as coral reefs, sandy shores, rocky patches, mangroves as well as large mud flats, records of Indian opisthobranch are very less. The study of opisthobranchs dates backs from 1850 s. Alder and Hancock in 1864, have published a

B. Vishal (&) A. Deepak Conservation Department, Bombay Natural History Society, Hornbill House, S. B. Singh Road, Bombay 400001, India e-mail: [email protected] A. Deepak e-mail: [email protected]

K. Venkataraman et al. (eds.), Ecology and Conservation of Tropical Marine Faunal Communities, DOI: 10.1007/978-3-642-38200-0_5, Springer-Verlag Berlin Heidelberg 2013

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B. Vishal and A. Deepak

comprehensive data from south-east coast of India. Subsequently, various authors have published records of opisthobranch from various coastal areas of India. The biodiversity rich areas like Gulf of Kutch (Gujarat), Gulf of Mannar and nearby island like Krusadai Island, Shingle Island and Rameshwaram were studied in the past. Two island groups, Lakshadweep and Andaman and Nicobar Islands were studied for opisthobranch fauna on few occasions. For rest of the coastal areas, studies were opportunistic or a part of general marine faunal studies. More scientific expeditions are essential to reveal true diversity of Indian opisthobranchs.

5.2 Methods All available literature was scrutinised for opisthobranchs records from India. Old articles were obtained from Biodiversity Heritage Library and some were obtained through open source and online publications. For the present study, 87 articles has been screened for presence/absence of opisthobranch records from India. We have divided the data in 4 phases from 1850–2012 which are as follows: • • • •

First phase: 1851–1900 Second phase: 1901–1950 Third phase: 1951–2000 Fourth phase: 2001–2012

ISO Codes were used as acronyms for various coastal states: GJ: Gujarat, MH: Maharashtra, GA: Goa, KA: Karnataka, KL: Kerala, TN: Tamil Nadu, AP: Andhra Pradesh, OR: Orissa, WB: West Bengal, AN: Andaman and Nicobar Island, LD: Lakshadweep Island and UNK: for data deficient but recorded from India.

5.3 Results and Discussion 5.3.1 Historical Studies Data was sourced from various publications and was segregated based on the year of publication and then it is compared with the taxonomic classification. Majority of the species recorded or described were from southern India (Tamil Nadu and Andhra Pradesh) and a few from Gujarat, Lakshadweep and Andaman and Nicobar Islands.

5.3.2 History of Indian Opisthobranchs Maximum number of species descriptions (158 species) were made in the fourth phase with 79 genera, 35 families and 6 orders (Figs. 5.1, 5.2). In the third phase, however, 135 species covering 88 genera, 41 families and six orders were

5 Current Status of Indian Opisthobranch Fauna

65

Fig. 5.1 Map of India with colours depicting number of opisthobranchs distributed across coastal states

described by various authors. Second phase covered 69 species distributed over 50 genera, 29 families and 5 orders while the first phase covered 37 species among 24 genera distributed over 14 families and 3 orders. Majority of the literatures in the first two phases 1850–1900 and 1901–1950 (mostly by British researchers), showed hand drawn colour illustrations which were good enough to recognise specimens (Alder and Hancock 1864; Bordie and Willan 1993; Ramakrishna et al. 2010). Many of the species described during these two phases are not yet been re-recorded.

Numbers

66

B. Vishal and A. Deepak 180 160 140 120 100 80 60 40 20 0

158 135

88

79

69 50 37 3

14

1851-1900

41

29

24

35

6

5

1901-1950

Order

Family

6

1951-1000

Genus

2001-2012

Species

n = 311

Fig. 5.2 Opisthobranch species with reference to taxonomic levels in four phases

5.3.3 The First and Second Phase First and second phase (1850–1900; 1901–1950) was dominated by majority of British personnel’s coming on posting to India. In the first phase, Alder and Hancock (1864) worked on the collection of Waltair Eliot from Waltair, Andhra Pradesh. Later he has published his monograph with coloured plates with description based on preserved material and few from colour drawing and notes. Melvill and Abercrombie (1893) in his publication of Bombay mollusca mentions Smaragdinella andersoni from Maharashtra coast; Farran (1905) has published mainly on Ceylonese nudibranch but few of the study areas are currently under Indian Territory like Gulf of Mannar. Eliot C.N.E. published many articles on Indian opisthobranchs (Eliot 1906a, b, 1909, 1910a, b, 1916). Eliot in 1906a, b reviewed, revised and commented on few species from the collections of Alder and Hancock (1864) from Andhra Pradesh. In 1906b, 1909, 1910a, b and 1916 he worked on specimens from various states of India; Lakshadweep (Minicoy), Gujarat, collections of Indian museum and Chilka Lake, respectively. Total of 27 species were published by Eliot from current Indian Territory. Hornell (1909 and 1949) mentioned few opisthobranchs in his book on Indian molluscs. In 1922, Annandale and Prashad published a new Saccoglossan species Stiliger pica from Chilka Lake (Sewell and Annandale 1922). Gravely F.H. an eminent British scientist published 19 species of opisthobranchs from the Krusadai Island in 1927. Later O’ Donoghue, worked on the collection of Gravely from the Gulf of Mannar and few specimens from B. Sundara Raj. He then published on 19 species which included description of 5 new species. Of these 5 species, 3 are currently valid viz. Hancockia papillata, Marionia pambanensis and Pleurophyllidia paucidentata. After 1932, few Indian researchers also started working on Indian opisthobranch fauna. Rao in (1936, 1937) published article on Kalinga ornata and a new sacoglossan species Stiliger gopalai. Winckworth (1946a, b) have worked mostly in peninsular India. In the second phase, total of 69 species were recorded out of that 15 species were described as new to science. The second phase was the rising phase for Indian opisthobranch researchers.


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5.3.4 The Third Phase In the third phase which includes time frame of 1951–2000 where most of the work was carried out by Rao (1952, 1962a, b, 1967, 1970 and 1973), Rao and Alagarswami (1960, 1961), Rao and Krishna Kumari (1973a, b, 1974, Rao et al. 1974), Rao (1965a, b, 1968) and published in various journals and total of 29 species were described including 12 new species. Most of this work was from the Gulf of Mannar and Mandapam region. Hornell (1951) published overall on Indian mollusc with opisthobranchs as a part. Satyamurti (1952) recorded 30 species from Krusadai Island. Narayanan (1968, 1969, 1970, and 1971) published 26 records from Gujarat which is one of the important studies on the Indian opithobranch. Ganapati and Sarma (1970, 1972) and Sarma (1974, 1975) published on bivalve gastropods and other algae associated opisthobranchs such as, Berthelinia limax, Ascobulla pusilla, Oxynoe viridis, Volvatella pyriformis, Berthelinia schlumbergeri, Julia burni from Indian subcontinent. New species Berthelinia ganapati and Berthelinia waltairensis were described from India by Sarma (1975). Burn (1970) published on Phyllidia (Phyllidiella) zeylanica as a rare Nudibranch from Indian waters. Rudman (1973) described two species of nudibranch from Gujarat, India; Chromodoris krishna described in 1973, was later synonymised to the Chromodoris fidelis Rudman (1985) which is now known as Goniobranchus fidelis and Sakuraeolis gujaratica described in 1980 has been recently rerecorded by the authors with several specimens from the type locality (Apte et al. 2010). Winkworth (1946a, b) described five chromodorids and a Goniodoris species from Mumbai, India out of which four Chromodorids and a Goniodoris are currently valid except Glossodoris semieon which was synonymised to Hypselodoris infucata (McDonald 2009). Salvini Plawen et al. (1973) described one new species of opisthobranch from genus Pseudovermis. Subba Rao et al. (1980), Valdes et al. (1999) described two species namely Chromodoris madapamensis and Chromodoris naiki. Wawra (1988) published records of Opisthobranchia from the Bay of Bengal in German language. Subba Rao and Dey (2000) in their ‘‘Catalogue of marine molluscs of Andaman and Nicobar Islands’’ mentioned 38 species of opisthobranchs. In this phase 27, new species and 100 range extensions were described out of total 135 (Fig. 5.3).

5.3.5 The Fourth Phase Fourth phase is from 2001 till the time of publications. In this phase comprehensive work was done by Subba Rao (2003), Subba Rao et al. (2004), Subba Rao and Sastry (2005), Jagtap et al. (2009), Apte (2009), Ganesh et al. (2009), Sreeraj

68

B. Vishal and A. Deepak 160

146

135

140

117

# Species

120

100

100 69

80 60 40

57 37

22

37

27 15

20

1

0 1851-1900

1901-1950

No.of species

1951-2000

Recorded for first time

2001-2012

New species

n = 311

Fig. 5.3 Phase-wise details of opisthobranch species; new records and new species

et al. (2010), Ramkrishna et al. (2010), Apte et al. (2010), Apte and Salahuddin (2011), Sachithananadam et al. (2011), Kamalakannan et al. (2010), Yogesh Kumar et al. (2011), Dhivya et al. (2012), Sreeraj et al. (2012a, b), Apte (2012), Sethi and Pattnaik (2012), and Srinivasulu et al. (2012). Jagtap et al. (2009) recorded a sacoglossan species Elysia bangtawaensis from the mangroves of Goa. Apte (2009) published 60 species from Lakshadweep Archipelago from which 40 were new records to India. Ramkrishna et al. (2010) was first to publish a book on opisthobranch from Andaman and Nicobar islands with several new records. Apte et al. (2010) published first part of their work on opisthobranchs of Gujarat covering 33 species including 13 new records to India. Sreeraj et al. (2010, 2012a, b) published 26 species with several range extensions from Andaman and Nicobar island. Recently, Yogesh Kumar et al. (2011) recorded 20 species from Gulf of Mannar. Kamalakannan et al. (2010) and Srinivasulu et al. (2012) recorded species of Glaucus from the eastern coast of India. Apte (2012) published a comprehensive guide to Indian marine fauna which deals with 103 opisthobranch species from India. In the fourth phase, 158 species were recorded distributed over 79 genera with 35 families in 6 orders (Fig. 5.3). Although all the four phases showed presence of Nudibranchia, the distribution of species among different suborders differs greatly. Order Doridina was predominant with most of the species. From second phase onwards, other suborders and species were recorded in substantial numbers (Fig. 5.4).

5.3.6 Indian Coastal States with Reference to Opisthobranch Diversity Compared to the size of coastline, the previous studies were concentrated in the few known biodiverse areas. Thus it will be premature to comment on the status of opisthobranch fauna in various coastal states.

# Species

5 Current Status of Indian Opisthobranch Fauna 90 80 70 60 50 40 30 20 10 0

69

77

31

29

29 19

4

9 1

9

9 2

1

1851-1900

1901-1950

Aeolidina

Dendronotida

14 6

4

1951-2000

Arminina

3

2001-2050

Doridina

n = 311

Fig. 5.4 Sub-orders of nudibranchia scattered across various phases

Most of the studies on the Indian opisthobranchs were examined in Andhra Pradesh (Alder and Hancock 1864; Eliot 1906a), Tamil Nadu (Rao KV 1952, 1962a, b, 1967, 1970, 1973; Rao and Alagarswami 1960, 1961; Rao and Krishna Kumari 1973a, b, 1974; Rao et al. 1974; Rao 1965a, b, 1968; Hornell 1949, 1951; O’ Donoghue 1932; Gravely 1927; Satyamurti 1952; Yogesh Kumar et al. 2011); Gujarat (Eliot 1909; Narayanan 1968, 1969, 1970, 1971; Apte et al. 2010); Andaman and Nicobar Islands (Ramkrishna et al. 2010; Sreeraj et al. 2010, 2012a, b) and Lakshadweep (Eliot 1906b; Apte 2009; Apte and Salahuddin 2011). Most of the work from other areas is based on few species occurred during other faunal surveys or opportunistic records. The frequently recorded species during various studies presented in Table 5.1 and Fig. 5.1 illustrates the records of opisthobranchs from various coastal states and UT’s.

Table 5.1 Frequently recorded species among Indian opisthobranchs based on literature

Species

Frequency

Bulla ampulla Bornella stellifer Jorunna funebris Phidiana militaris Aplysia dactylomela Dendrodoris nigra Dendrodoris fumata Pteraeolidia ianthina Phyllidiella zeylanica Plocamopherus ceylonicus Elysia grandifolia Dolabella auricularia Asteronotus cespitosus

11 9 9 8 7 7 7 7 7 7 7 6 6

70

B. Vishal and A. Deepak 6 5

5

5

5

5

Number

4

4

4

4

4

4

4

4

4 3

3

3 2

2

2

2 1

1

1

1

1

1

1 0

0

GJ

MH

GA

KA

KL

Order

TN

AP

OR

WB

AN

LD

UNK

Sub Order: Nudibanchia

Fig. 5.5 Number of opisthobranch orders and nudibranch sub-orders across the coastal states

5.3.7 Distribution of Orders and Sub Orders of Nudibranchia Five of the seven orders (Fig. 5.9) were recorded along Gujarat, Tamil Nadu, Andaman and Nicobar Island and Lakshadweep (Fig. 5.5). Lowest number of orders and sub-order of nudibranchia were recorded from West Bengal, Goa and Karnataka. This is primarily due to lack of systematic surveys in these areas.

5.3.8 Distribution of Opisthobranchs in Suborders of Nudibranchia Across the States Three major states (Tamil Nadu, Gujarat and Andhra Pradesh) and 2 UT’s (Andaman and Nicobar Island and Lakshadweep) showed Doridina as a dominating order (Fig. 5.6) followed by Aeolidina and Dendronotina.

56

60

Number

50 38

40

31 19

20 10 7 3 3 0

27

26

30

GJ

11 6 101

MH

000100012002

GA

KA

Aeolidina

KL

2

TN

Arminina

8 312

AP

20003001

OR

Dendronotida

WB

35

5

AN

Doridina

Fig. 5.6 Various sub-orders of nudibranchia scattered across costal Indian states

13

0000

LD

UNK

Number

5 Current Status of Indian Opisthobranch Fauna 40 35 30 25 20 15 10 5 0

71

34 30 27 21 18 8

GJ

6

MH

2

1

GA

KA

8

6

3

KL

TN

AP

OR

WB

AN

LD

UNK

Family Fig. 5.7 Number of families distributed across various states

5.3.9 Distribution of Opisthobranch Families Majority of authors worked on the Tamil Nadu opisthobranch fauna as a result of which it has highest number of opisthobranch families (Fig. 5.7). This was followed by the Andaman and Nicobar Islands, Lakshadweep, Gujarat and Andhra Pradesh with 30, 27, 21 and 18 families, respectively.

5.3.10 Distribution of Opisthobranch Genera and Species Andaman and Nicobar being closest to the coral triangle has luxuriant coral reefs, and proves to be one of the best opisthobranch habitat. It harbours 131 species which is spread over 66 genera. This is followed by Tamil Nadu with 67 genera and 102 species. Lakshadweep and Gujarat recorded 72 and 54 species among 48 and 39 genera, respectively. Whereas, Andhra Pradesh showed presence of 40 species scattered across 26 genera (Fig. 5.8). 140

131

120 102

Number

100 80

67 54

60

48 40

39

40

26 11 12

20

2

0

72

66

GJ

MH

2

GA

1

1

KA

6

7

KL

6

TN

Genus

AP

6

OR

8 10

WB

Species

Fig. 5.8 Number of genera and families distributed across various states

3

AN

LD

3

UNK

72


5.3.11 Current Status The current state of research in opisthobranch fauna suggests that opisthobranch studies are on the rise and many researchers are now trying to get involved in the taxonomy of opisthobranchs and researching in various coastal areas of India. This is primarily attributed to the All India Co-ordinated Project on Taxonomy (AICOPTAX), an initiative by Government of India under the auspicious of Ministry of Environment and Forests. There are totally 311 species recorded hereto from India of which 65 species (including 2–3 doubtful species) are described from India. Five families are dominant (Table 5.2) which covers almost 41 % of the total Indian opisthobranch fauna which includes Chromodorididae (39 species), Discodorididae (33 species), Haminoeidae (20 species), Plakobranchidae (19 species) and Phyllidiidae (17 species). Nudibranchia is diverse and large order of opisthobranchia and Indian opisthobranch are not exception for the same. 63 % of Indian opisthobranchs are under nudibranch mollusc, followed by 17 % Cephalaspidea, 12 % Saccoglossans, 4 % Anapsidea and 4 % Notaspidea. Order Umbraculida and Acochlidiacea are represented with less than 1 % due to presence of single species (Fig. 5.9). In Order Nudibranchia, Doridacean are most dominant with 66 % (127 species) followed by Aeolidacean 19 % (36 species), also by Dendrodotonids and Arminina 10 and 5 %, respectively (Fig. 5.10). Most common and widespread opisthbranchs found in India (based on more than five records) are Bulla ampulla, Bornella stellifer, Jorunna funebris, Elysia grandifolia, Phidiana militaris, Aplysia dactylomela, Dendrodoris fumata, Dendrodoris nigra, P. zeylanica, Plocamopherus ceylonicus, Pteraeolidia ianthina, Asteronotus cespitosus, Dolabella auricularia and Polybranchia orientalis. These species were recorded several times since 1850 and are also widespread from indo-pacific region (Gosliner et al. 2008).

5.3.12 Similarity Based on the Species Records and Various States The data was analysed for similarity using Bay-Curtis similarity analysis. Andaman and Nicobar Island, Lakshadweep Island, Tamil Nadu and Gujarat form a cluster predominantly due to presence of coral reefs at survey locations. Second clade is of intertidal rocky shore associated habitat especially where Kerala and Maharashtra share a few species. Andhra Pradesh showed species diversity predominantly between rocky shore and coral reef habitat (Fig. 5.11).

5 Current Status of Indian Opisthobranch Fauna Table 5.2 Species composition of top five families and their representative genera

1 2 3 4 5 6 7 8 9 10 1 2 3 4 5 6 7 8 9 10 11 12 13 14 1 2 4 5 6 1 2 3 4 1 2 3 4

73

Family and Genera

No. of species

Chromodorididae Cadlinella Ceratosoma Chromodoris Doriprismatica Felimare Glossodoris Goniobranchus Hypselodoris Mexichromis Thorunna Discodorididae Asteronotus Atagema Carminodoris Discodoris Halgerda Hoplodoris Jorunna Montereina Peltodoris Platydoris Sclerodoris Sebadoris Tayuva Thordisa Haminoeidae Atys Haminoea Limulatys Phanerophthalmus Smaragdinella Plakobranchidae Costasiella Elysia Plakobranchus Thuridilla Phyllidiidae Phyllidia Phyllidiella Phyllidiopsis Reticulidia Grand Total

39 1 1 8 1 1 5 7 13 1 1 33 2 4 1 1 5 2 2 1 2 6 2 2 1 2 20 10 7 1 1 1 19 1 12 1 5 17 7 6 3 1 128

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B. Vishal and A. Deepak Pleurobrancho morpha 12 4%

Sacoglossa, 37 12% Umbraculida, 1 0% Acochlidiacea 1 0% Anaspidea, 12 4%

Nudibranchia 194 63%

Cephalaspidea 54 17%

Fig. 5.9 Number of species and opisthobranch orders

Fig. 5.10 Number of species and nudibranch sub-orders

Aeolidina 36 19% Doridina 127 66%

Arminina 10 5%

Dendronotida 19 10%

5.3.13 Few Comments on Synonymy and Taxonomy Doris carinata Alder and Hancock (1864) is synonymised with Siraius immonda (Risbec 1928) by Bordie and Willan (1993). But there is still confusion as they lack specimens from India. According to Rudman (2000) Doris carinata and Siraius immonda differs from each other by the number and the arrangement of gills. Hypselodoris infucata is one of the most common species from the coral reef areas. Chromodoris diardii described by Kelaart in Ceylon and later recorded by Eliot in Eliot (1906a, b) (from Ceylon) and Glossodoris semeion Winkworth Winckworth (1946a, b) described from Mumbai are now synonymised to the Hypselodoris infucata Rüppell and Leuckart 1830 (McDonald 2009). Eliot in its Okhamandal Nudibranch paper described a species Janolus indica (Eliot 1909). Although, Eliot (1909) hasn’t described reproductive system.


75

Fig. 5.11 Species dominance: Blue mud/sand/rocky shore dwelling species; Red rocky shore affiliated species; yellow coral reef associated species (McAleece et al. 1997)

Externally, specimen looks quite similar to that of Janolus toyamensis Baba and Abe (1970). Recently, Baba (1986) recorded both Janolus toyamensis and Janolus indicus from Japan. So, until detailed anatomy of the species from Okha is studied; it is unable to reveal validity of the specimen J. Indicus In Ratnagiri, we got species of Atagema which is morphologically similar to Doris tristis Alder and Hancock (1864). Last mention of this species was by Satyamurti in 1952. The work on the species is under progress. There are three similar looking types of Berthellina recorded by the authors viz. Berthellina citrina, Berthellina delicata and Berthellina cf. citrina (white speculated form). The spotted form of Berthellina citrina was considered to be Berthellina minor by Narayanan (1969) which was later changed to Berthellina citrina (Narayanan 1970). We are presently retaining it as a separate species till the time we complete the anatomy and molecular phylogeny. An aeolid named Sakuraeolis gujaratica from single specimen from the Gulf of Kutch, Gujarat described Rudman (1980). Almost after 30 years of its description, authors rerecorded specimens from type locality. The species is endemic to Gulf of Kutch, Gujarat, India.

5.4 Conclusion Our knowledge on Indian opisthobranchs is yet very poor. The lack of comprehensive studies created large gaps in our knowledge on the distribution of opisthobranchs in India. More intensive surveys may improve our species inventory many folds.

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Acknowledgements We thank Dr. Bill Rudman, Dr. Richard Willan, Dr. Terry Gosliner, Dr. Nathalie Yonow, Dr. Kathe Jensen, Dr. Cynthia Towbridge, Dr. Benoit Dayrat, Dr. Gary McDonald, Mr. Vinicius Padula and Dr. Patrick Krug for their support in the form of personal communications, discussions, species validation and also for providing literature. We take opportunity to acknowledge Mr. C.R. Sreeraj for providing few ZSI publications. Ms. Amruta Prasade and Ms. Pooja Nagale helped preparing checklist and going through the manuscript. Mr. Vishwas Shinde and Rajendra Pawar provided valuable field assistance in searching for cryptic opisthobranchs during the survey. We take this opportunity to thank Ministry of Environment and Forests, Government of India for providing funding under AICOPTAX to carry out opisthobranch work along the coasts of Gujarat, Maharashtra and Lakshadweep. We thank Dr. J.R. Bhatt in particular for his continued support.

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