TAXONOMIC STATUS OF OYSTERS

51

Oysters are members of the family Ostreacea; class Bivalvia, in the phylum

Mollusca. Under the current systematic schema, most commercially important species

are classified in three major genera: Ostrea, Saccostrea, and Crassostrea and a

number of minor genera (Carriker and Gaffney, 1996).

Fig.3.1: Morphological structure of Saccostrea cucullata shells of Mandovi - Zuari Estuary, Goa

Fig.3.2: Phenoplastic nature of Saccostrea cucullata in Chorao Island and Nerul Creek of

Mandovi - Zuari Estuary, Goa, India

52

Oyster species are a challenging group for taxonomists and phylogeneticists.

Several studies based on morphology and geographic range information have

attempted to identify characters and traits that can be used for identification and

resolving relationships among species (Stenzel 1971; Bernard 1983; Harry 1985; Brock

1990), but this process has proven problematic. For example, shell morphology, which

is commonly used as a primary distinguishing feature, is phenoplastic and greatly

affected by habitat (Tack et al., 1992). Oysters are notorious for the complex taxonomic

problems they present and the profound nomenclatural confusion regarding species

identities. The basis of early oyster taxonomy, such as the work of Cox (1883), Saville-

Kent (1893) and Iredale (1924), is entirely conchological. Later, many authors, e.g.,

Hirase (1930), Elsey (1935), Nelson (1938) and Thomson (1952), studied the anatomy

of the internal tissues, such as the gill ostia, heart, adductor muscle, mantle, pallio-

branchial fusion, promyal chamber and rectum and confirmed their generic importance

in oyster nomenclature. The malacological characters of taxonomic usefulness are,

however, limited and have been almost completely ignored by most systematists

(Thomson, 1954). In recent years several researchers have developed molecular

markers and identification keys to help resolve some of the questions surrounding

oyster identifications and taxonomic relationships. Comparative features of three Oyster

genera from Glude (1971), Ahmed (1975) and Stenzel (1971) are listed in Table 3.1

(Source: Angell, 1986).

53

Table 3.1: Comparative features of three Oyster genera based on conchological and malacological characters

Characteristics Ostrea Crassotrea Saccostrea

Chromata Present Absent Present

Promyal Chamber Absent Present Present

Umbonal Cavity Absent Moderate Deep

Sexual

Development

Protandrous

hermaphrodite Dioecious Dioecious

Spawning Mode Larviparous Oviparous Oviparous

Turbidity Tolerance Low High Moderate

Salinity Preference Stenohaline Euryhaline Stenohaline

Shape Sub circular, Flat Somewhat Elongated

and cupped

Cornucopia or

Rudistiform

Shell Margins Crenulated in some

speciesNot Crenulated Crenulated

Valves Equal Upper Valve Smaller Upper Valve

Smaller

Size Small to Moderate May be Large Small to Moderate

Range All Tropical Seas

All Tropical Seas

except Polynesia and

Melanesia

Indo-Pacific

Variations in the shape of the oyster shells are likely within the same species

from the same area due to overcrowding, orientation, substratum and ecological

conditions (Quayle and Newkirk, 1989). Such variations cause great difficulties in the

identification of oysters, leading to disagreements among researchers. Oyster shell

morphology is typically plastic and creates difficulties in classification (Gaffney and

Allen, 1993). Table 3.2 presents the taxonomic status of Saccostrea cucullata.

54

Table 3.2: Taxonomic status of Saccostrea cucullata

NAME YEAR DESCRIPTION

Oliver 1922 Saccostrea is a mono-specific genus and reports S. cucullata

in the Red Sea.

Thomson 1954 Regarded the Australian rock oyster "commercialis", which

had been earlier named as "cucullata"

Thomson 1954 Claimed S. tuberculata is very close to S. cucullata

Stenzel 1971

Believed that Saccostrea cucullata (Born, 1778) should be

regarded as the 'monotypic species" or "super species" of the

genus Saccostrea.

Some of the species named in the genera Crassostrea, e.g.,

C. commercialis and Saccostrea, e.g., S. cucullata, according

to Stenzel (1971) and Ahmed (1975), are, in fact,

synonymous.

This view has relegated (demote) many oysters that grow on

rocks and mangroves in the Indo-Pacific area, such as S.

commercialis (Iredale and Roughley, 1933), S. echinata

(Quoy and Gaimard, 1835), S. glomerata (Gould, 1850) and

S. mordax (Gould,1850), to either component species of S.

cucullata or merely its geographic ecomorphs, or variants.

Glude 1971 Proposed that S. cucullata should be considered an

ecomorph of S. mordax

Dinamani 1976

Concluded that revision of the taxonomic status of such a

multitude of oyster species could only be attempted after

more detailed studies of all the "species" of the S. cucullata

group distributed around the world had been undertaken.

Buroker et al. 1979

Saccostrea manila was identified as a sibling species of S.

malabonensis using genetic markers identified by protein

electrophoresis & Electrophoretic analysis.

Phillips 1979 The local rock oyster, S. cucullata, has been misidentified as

S. glomerata in his heavy metal investigations of the species.

Torigoe 1981

Reported the occurrence of S. glomerata, S. mordax, S.

kegaki (Torigoe & Inaba, 1981) and S. echinata in Japanese

waters.

Morris 1985 Proposed that the spinose S. kegaki (Torigoe and Inaba,

1981) from Japan (Torigoe and Inaba1981) is also included

55

as a probable synonym of S. cucullata.

Quayle and

Newkirk1989

Studied variations in the shape of the oyster shells are likely

within the same species from the same area due to

overcrowding, orientation, substratum and ecological

conditions.

O’Foighil et al. 1995

Developed a number of molecular markers to distinguish

among various species of oysters. Ostrea, Crassostrea and

Saccostrea species. Molecular markers have been variously

used to examine phylogenetic relationships, elucidate genetic

diversity, and develop molecular genetic identification tools.

Used mitochondrial markers such as 16S rRNA.

Carriker and

Gaffney1996

The genera of the Ostreidae have been reviewed by many

authors. Three major genera: Ostrea, Saccostrea, and

Crassostrea and a number of minor genera

Visootiviseth et al 1998

These oysters can be differentiated at the genus level using

the chromata. Oysters having that morphologic characteristic

are regarded as members of less economically important

Oysters genera Saccostrea or Striostrea, whereas those that

do not have chromata are Crassostrea oysters

O’Foighil et al. 1998 Used mitochondrial markers such as the cytochrome oxidase

subunit I

Yoosukh and

Duangdee1999

These oysters can be differentiated at the genus level using

the chromata. Oysters having that morphologic characteristic

are regarded as members of less economically important

Oysters genera Saccostrea or Striostrea, whereas those that

do not have chromata are Crassostrea oysters

Hedgecock et al. 1999 Used nuclear markers such as the first internal transcribed

spacer (ITS-1)

Wang et al. 2004

More recently, studies have also used nuclear markers

regions of the nuclear rRNA gene family, or some

combination of mitochondrial and nuclear markers. The most

commonly used techniques to reveal genetic variation in

these markers are sequencing.

Lam and Morton 2006

The morphologies of Saccostrea cucullata, Saccostrea

glomerata, Saccostrea kegaki, and Saccostrea commercialis,

are so variable and overlapping that is not always possible to

tell them apart by eye. The differentiation of Saccostrea

56

Saccostrea cucullata was first described by the Czech mineralogist, metallurgist,

and malacologist Ignaz von Born in 1778. They are commonly called the Natal rock

oysters and are mainly seen in the Indo-pacific oceans. One of the widely accepted

scientific classifications for Saccostrea cucullata is as follows in Table 3.3.

Table 3.3: Scientific classification of Saccostrea cucullata

Saccostrea cucullata (Born, 1778)

Kingdom Animalia

Phylum Mollusca

Class Bivalvia

Order Ostreoida

Family Ostreidae

Genus Saccostrea

Species S. cucullata

Scientists aim to describe a single 'tree of life' that reflects the evolutionary

relationships of living things. However, evolutionary relationships are a matter of

ongoing discovery, and there are different opinions about how living things should be

glomerata (Sydney Rock Oyster) from Saccostrea cucullata is

so problematic by the external characteristics at times even

for experts that oysters like this are frequently given both

names, S. glomerata cucculata.

In species of Saccostrea such as cucullata, glomerata, and

kegaki which are all morphologically similar to each other with

an oval, deeply cupped left valve and a smaller, relatively flat

right valve with slightly plicate, raised margins, even the

phylogenetic results using some molecular markers cannot

differentiate them. Only mitochondrial 16S rDNA gene

sequence data accurately identifies S. cucullata

57

grouped and named. Encyclopedia of Life (EOL) (http://eol.org/) reflects these

differences by supporting several different scientific 'classifications'. Some species have

been named more than once. Such duplicates are listed under synonyms. EOL also

provides support for common names which may vary across regions as well as

languages. There are nearly 20 different classifications available at present for

Saccostrea cucullata and a few are mentioned below in Table 3.4 (Source:

http://eol.org/pages/449497/names)

Table 3.4: Different classifications available at present for Saccostrea cucullata

Recognized By Rank Classification

Species 2000 & ITIS

Catalogue of Life: April 2013

(http://www.

catalogueoflife.org/)

Species

58

Inventaire National du

Patrimoine Naturel

(http://inpn.mnhn.fr)

Species

BOLDS resource for

species-level taxa

Barcode of Life Data

Systems (BOLD)

(http://www.

boldsystems.org)

Environments

http://environments-

eol.blogspot.com/

59

BioLib.cz Import

(http://www.biolib.cz/en/)

Integrated Taxonomic

Information System (ITIS)

(http://www.itis.gov/)

Species

BOLDS images II

Barcode of Life Data

Systems (BOLD)

(http://www.

boldsystems.org)

Species

60

Inventaire National du

Patrimoine Naturel

(http://inpn.mnhn.fr)

Species

Inventaire National du

Patrimoine Naturel

(http://inpn.mnhn.fr)

Species

61

Inventaire National du

Patrimoine Naturel

(http://inpn.mnhn.fr)

Species

Inventaire National du

Patrimoine Naturel

(http://inpn.mnhn.fr)

Species

62

Mineralogy

OBIS depth range resource

Ocean Biogeographic

Information System (OBIS)

(http://www.iobis.org/)

NCBI Taxonomy

view in classification

(http://www.ncbi.nlm.nih.gov)

Species

63

Wikipedia

(http://www.wikipedia.org/)

Paleobiology Database

view in classification

(http://www.paleodb. org/)

Species

64

India Biodiversity Portal

Species Data

(http://indiabiodiversity.org/)

Species

Taxonomic Hierarchy of

COL-China 2012

view in classification

Species

World Register of Marine

Species (WoRMS)

view in classification

(http://www.

marinespecies.org/)

Species

65

The names in the table below presents an overview of the relationships of this

group to other groups in the tree of life, based on the classification hierarchies provided

by EOL classification partners. "Parents" are more inclusive group’s one level higher up

in the hierarchy. "Children" are the subgroups of the current group. The three related

names of Saccostrea cucullata are mentioned below in Table 3.5.

(Source: http://eol.org/pages/449497/names/related_names).

Table 3.5: Related names for Saccostrea cucullata used by different groups

Parents Sources

Saccostrea Dolfuss &

Dautzenberg 1920 Paleobiology Database

Saccostrea Dollfus &

Dautzenberg 1920

WORMS Species Information (Marine Species)

Integrated Taxonomic Information System (ITIS)

Saccostrea NCBI Taxonomy

Species 2000 & ITIS Catalogue of Life: April 2013

Taxonomic Hierarchy of COL-China 2012

Sometimes taxonomists create new names for groups that already have a name.

They may do this because they are unaware of the original name, or they may think the

organism before them belongs to a different group when in fact it does not. If two or

more names are found to apply to the same group, they are considered synonyms. In

66

most cases, the first name takes priority and is considered to be the valid or accepted

name. However, there can be exceptions, and it's not always easy to determine which

of a series of synonyms should be considered valid or accepted. Here we list the

synonyms provided to EOL by our classification partners. We also include other

versions of the name that most likely refer to the same group, for example, misspellings

in the literature or different variations of the authorship associated with the name.

Saccostrea cucullata has 22 synonyms which are mentioned below in Table 3.6

(Source: http://eol.org/pages/449497/names/synonyms)

Frequent synonyms / misidentifications:

Table 3.6: Frequent synonyms or misidentifications of Saccostrea cucullata by different

sources

Paleobiology Database

Name Relationship

*Saccostrea cucullata (Born 1778) Preferred

Ostrea cucullata Born, 1778 Valid

Lopha (Lopha) cucullata (Born 1778)

Ostrea (Lopha) cucullata (Born 1778)

Crassostrea cucullata (Born, 1778)

Gryphaea cucullata (Born 1778)

NCBI Taxonomy

Name Relationship

*Saccostrea cucullata Preferred

Crassostrea cucullata Synonym

Saccostrea cucculata Misspelling

Saccostrea cuccullata

Saccostrea cucullata (Born 1778) Authority

Species 2000 & ITIS Catalogue of Life: April 2013

Name Relationship

*Saccostrea cucullata (Born 1778) Preferred

Ostrea turbinata Lamarck, 1819

Ostrea forskali Gmelin, 1791

Ostrea saccellus Dujardin, 1835

Ostrea forskahlii Gmelin, 1791

67

Ostrea stellata Gmelin, 1791

Ostrea purpurea Lightfoot, 1786

Ostrea gibbosa Lamarck, 1819

Crassostrea cucullata (Born, 1778)

Dioeciostrea subtropica Orton, 1928

Saccostrea cuccullata [sic]

Saccostrea forskhalii (Gmelin, 1791)

Ostrea cornucopiae Gmelin, 1791

Ostrea cucullata Born, 1778

Food and Agriculture Organization of the United Nations (FAO)

(Source: ftp://ftp.fao.org/docrep/fao/009/w7191e/w7191e20.pdf)

FAO names: En - Hooded oyster; Fr - Huître-capuchon; Sp - Ostión capuchón.

Name Relationship

Crassostrea cuccullata (Born, 1778)

Ostrea cornucopiae (Chemnitz, 1785) (Invalid name)

O. cornucopiaeformis (Saville-Kent, 1893)

O. echinata (Quoy and Gaimard, 1835)

O. forskaelii (Chemnitz, 1785) (Invalid name)

O. forskalli (Gmelin, 1791)

O. glomerata (Gould, 1850)

O. malabonensis (Faustino, 1832)

O. mordax (Gould, 1850)

O. spinosa (Deshayes, 1836)

Saxostrea amasa (Iredale, 1939)

S. commercialis (Iredale and Roughley, 1933)

S. gravida (Iredale, 1939)

*Marks the preferred name from each source.

Many people know organisms only by the common names, or "vernacular"

names. Unlike scientific names, common names are almost always different for

speakers of different languages. They may also vary regionally within a language. The

table below shows some of the common names provided to EOL for this organism from

a variety of providers, including EOL curators. Currently we can only set one preferred

common name per language on a given EOL page, but all the names should be

searchable. Saccostrea cucullata has 7 common names in English which are mentioned

in Table 3.7.

(Source: http://eol.org/pages/449497/names/common_names)

68

Table 3.7: Common names of Saccostrea cucullata

Name Sources Status

Common rock oyster Hans-Martin Braun Trusted

Forsskål’s Oyster Hans-Martin Braun Trusted

* Hooded Oyster Hans-Martin Braun Trusted

Milky Oyster Hans-Martin Braun Trusted

Natal rock oyster Hans-Martin Braun Trusted

small rock oyster NCBI Taxonomy Trusted

Sydney cupped oyster uBio Unknown

*Marks the preferred name from each source.

Oyster species are a challenging group for taxonomists and phylogeneticists.

They are notorious for the complex taxonomic problems they present and the profound

nomenclatural confusion regarding species identities. Because of shell plasticity, the

taxonomy of Saccostrea has been problematic.

Species of Saccostrea are common oysters on Indo-Pacific rocky shores. The

taxonomy of this genus is unclear because of morphological plasticity among its

constituent species. Variations in the shape of the oyster shells are likely within the

same species from the same area due to overcrowding, orientation, substratum and

ecological conditions. Such variations cause great difficulties in the identification of

oysters, leading to disagreements among researchers. The taxonomic status of

Saccostrea genus rock oysters along the coastlines of India is unclear and poorly

known because of the morphological plasticity among its constituent species. Species of

Saccostrea from these localities have been identified solely on the basis of shell

morphology and anatomy. The malacological characters of taxonomic usefulness are,

however, limited and have been almost completely ignored by most systematists. In

recent years several researchers have developed molecular markers and identification

keys to help resolve some of the questions surrounding oyster identifications and

taxonomic relationships.