Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 April 2023 | 15(4): 23083–23090
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.7444.15.4.23083-23090
#7444 | Received 17
May 2021 | Final received 20 February 2023 | Finally accepted 22 February 2023
The giant clam commensal shrimp Anchistus miersi
(de Man, 1888) (Decapoda: Palaemonoidae)
new to Lakshadweep Sea, India
Manu Madhavan
1, Purushothaman Paramasivam
2, S. Akash 3, T.T. Ajith Kumar 4 & Kuldeep
Kumar Lal 5
1–5 ICAR – National Bureau of Fish
Genetic Resources, Canal Ring Road, P.O. Dilkusha,
Lucknow, Uttar Pradesh 226002, India.
1,4 Kerala University of Fisheries
and Ocean Studies, Kochi, Kerala 682506, India.
1 manumadhavan060@gmail.com, 2
purushothgene@gmail.com, 3 akash03jack@gmail.com
4 ttajith87@gmail.com
(corresponding author), 5 kuldeepklal@gmail.com
This article is dedicated to the
late Dr. P. Purushothaman, the second author.
Editor: V. Deepak Samuel, National Centre For
Sustainable Coastal Management, Chennai, India. Date
of publication: 26 April 2023 (online & print)
Citation: Madhavan, M., P. Paramasivam, S. Akash, T.T.A. Kumar & K.K. Lal (2023). The giant clam commensal shrimp Anchistus miersi
(de Man, 1888) (Decapoda: Palaemonoidae)
new to Lakshadweep Sea, India. Journal of Threatened Taxa 15(4): 23083–23090. https://doi.org/10.11609/jott.7444.15.4.23083-23090
Copyright: © Madhavan et al. 2023. Creative Commons Attribution 4.0 International
License. JoTT
allows unrestricted use, reproduction, and distribution of this article in any
medium by providing adequate credit to the author(s) and the source of
publication.
Funding: Funding for this study is extended by the Centre for Marine Living Resources and Ecology, MoES Govt. of India, through the project ‘Mainstreaming marine ornamental shrimp diversity for actions to enhance livelihood and gender empowerment opportunities among native Lakshadweep communities’ (MoES/CMLRE/MLRE/GIA/2002/Genl.).
Competing interests: The authors declare no competing interests.
Author details: Manu Madhavan is working as PhD, research scholar at the ICAR-National Bureau of Fish Genetic Resources. Purushothaman Paramasivam is a researcher at the ICAR-National Bureau of Fish Genetic Resources. S. Akash is working as PhD, research scholar at the ICAR-National Bureau
of Fish Genetic Resources. T.T. Ajith Kumar is working as principal scientist at the ICAR-National Bureau of Fish Genetic Resources. He known for his contribution to marine ornamental aquaculture for conservation and livelihood. Kuldeep Kumar Lal was the former director of the ICAR-National Bureau of Fish Genetic Resources and presently the director of the ICAR - Central Institute Brackishwater Aquaculture, have vast experience in conservation genetics.
Author contributions: MM—animal collection and morphological identification of the specimen. PP—species confirmation by morphological and molecular analysis and preparation of the manuscript. SK—animal collection and morphological identification of the specimen. TTAK—manuscript revision. KKL—conceptualization.
Acknowledgements: The authors are thankful to the
director, ICAR-NBFGR for the facilities and encouragement. They are grateful to
the Centre for Marine Living Resources and Ecology, MoES,
Govt. of India, for funding support. We are also extending thanks to the
Department of Fisheries, Administration of Lakshadweep, for local logistical
support.
Abstract: The genus Anchistus
Borradaile, 1898 is a colourful
shrimp from the commensal group. In this study, we are reporting a new
occurrence of Giant Clam commensal shrimp Anchistus
miersi (de Man, 1888 [in de Man, 1887–1888])
caught from Agatti Island, Lakshadweep Sea during
February 2020. The present specimens (one each matured male and female) were
collected from the mantle cavity of the Giant Clam, Tridacna maxima
(Roding, 1798) in the coral lagoon at a depth of 4 m. Anchistus
miersi is morphologically very similar to Anchistus demani, which
is easily distinguished by the presence of a strong antennal spine and
conspicuous accessory spinules in the third─fifth pereopods and presence of small blue spots all
over the body. The molecular analysis confirms that, the morphological
identification of the present Indian specimens displays an intraspecific
genetic divergence of 0.3─1.2%. Besides,
the remarkable taxonomic features and colour
patterns, distributional ranges are also attested with the report of the
species from the present area.
Keywords: Agatti
Island, distributional range, giant clam association, Lakshadweep,
morphology.
Introduction
The shrimp
fauna of Indian waters was studied majorly in the zones of western and eastern
coasts. The insight knowledge on the caridean shrimps from Lakshadweep waters
is still very narrow with the current status. Recently, a few surveys have
exposed new distributional coral-associated carideans (Baby et al. 2016;
Bharathi et al. 2019; Madhavan et al. 2019; Akash et
al. 2020; Prakash & Marimuthu 2020).
In general,
some of the palaemonid shrimps are endo-commensal species, enticing and
fascinating in their colour patterns. These shrimps
inhabit mantle cavities and gastric regions of host organisms such as sponges,
bivalves, and tunicates (Kemp 1922; Johnson & Liang 1966; Bruce 1977; De
Grave 1999). The genus Anchistus Borradaile, 1898 is one such taxa and has been symbolized
as a commensal group, usually associated with bivalves (mostly in the subfamily
Tridacninae) (Bruce 1972, 2000; Jayachandran 2001).
In the symbiotic relationship, the giant clam gain benefits from the shrimps
with cleaning service, which helps to maintain the health of its tissues.
Simultaneously, the shrimps get benefits from the giant clams like safety from
predator, stable environment, as well as access to food. This symbiotic
relationship was dynamic and can change over time. For example, a cleaner shrimp
may become a parasite, if it begins feeding on the giant clam’s tissues rather
than just its parasites.
Typically,
this genus covers seven species which are distributed in the Indo-Pacific
regions at shallow water depths (Jayachandran 2001; De Grave & Fransen 2011). Four species are reported from the Indian
waters notably in Andaman and Nicobar Islands; Anchistus
custos (Forskål, 1775),
A. demani Kemp, 1922, A. miersi
(de Man, 1888 [in de Man, 1887–1888]), and Anchistus
pectinis Kemp, 1925 (Samuel et al. 2016). The
morphological features of Anchistus are
distinguished from other groups of palaemonid shrimps by the presence of their
movable spine in the lateral border of uropods,
rostrum downwards, laterally compressed and extended to the distal end of eyes.
Also, the distolateral spine of antennal scaphocerite
is not overreaching the distal margin and has a convex structure in the inner
margin of the dactylus of 3rd pereopods.
During the
recent survey undertaken at Lakshadweep waters, a pair of Anchistus
specimens were collected at shallow depth lagoon regions of Agatti
Island. These specimens were carefully examined and have been identified as A.
miersi, which is a new distributional record to
the Lakshadweep Sea. The authors also provided taxonomic notes on morphological
and molecular features, habitat, and coloration of this species in a unique
manner.
Materials and methods
Sampling
A pair of
A. miersi specimens were caught out from
the mantle cavity of the Giant clam, T. maxima (Roding, 1798) from the
lagoon area of Agatti island at the depth of 4 m
(10.8533N & 72.1872E; Image 1). The specimens were picked up using a hand
net during snorkeling in the reef region of the lagoon. The specimens were
transferred alive to the Germplasm Resource Centre of the ICAR - National
Bureau of Fish Genetic Resources (NBFGR) located at Agatti,
Lakshadweep, India for further analysis. After transportation, the colouration of the species was captured with a camera
(Canon G1X), followed by maintaining the specimens in live condition. However,
mortality was noticed on the second day, it might be happened due to the
absence of host organisms. Further, the dead specimens were preserved in 95% of
ethanol for detailed morphological examination.
Morphology
The
preserved specimens were taken to the Peninsular and Marine Fish Genetic
Resources (PMFGR) Centre of the ICAR-NBFGR, Kochi, India for further studies.
Careful examination with a stereo zoom microscope (0.5–8X) with Nikon SMZ1270
digital camera has been carried out. A compound microscope, Leica ICC50 was
used for observation of dactylus and mouth structures. The illustrative images
for morphological characteristics were drawn using the GNU Image Manipulation
Program (Version 2.10.12) and edited with Adobe Photoshop CS2. The
morphological identification and diagnosis were carried out by following the
literature of Holthuis (1952), Bruce (1973), and
Jayachandran (2001). The examined material was deposited in the National Fish
Museum and Repository of the ICAR-NBFGR, Lucknow, India. The measurement of
carapace length (CL) was taken from the posterior orbit angle to the posterior
margin of the cephalothorax with Vernier caliper (0.1 mm accuracy). The measure
of CL is considered as a standard length for both individuals.
DNA
barcoding
The partial
sequences of barcoding gene mitochondrial cytochrome c oxidase I (COI) data
were generated for this species adopting Akash et al. (2020). BioEdit software v. 5.0.9 (Thompson et al. 1994) was used
to align and correct the sequence data. The corrected sequences were blasted in
Blastn (https://blast.ncbi.nlm.nih.gov/Blast.cgi) of
NCBI to find out similarity ranges. 12 COI sequences of Anchistus
species were retrieved from NCBI (https://www.ncbi.nlm.nih.gov/) and were
used in this analysis. MEGA X software was used to estimate the pairwise
genetic distances and reconstruct the Maximum Likelihood (ML) tree (Kumar et
al. 2018) with the implementation of 1,000 replications.
Taxonomic
Status
Order Decapoda Latreille, 1802
Infraorder Caridea Dana, 1852
Superfamily
Palaemonoidea Rafinesque, 1815
Family Palaemonidae Rafinesque, 1815
Genus Anchistus Borradaile,
1898
Species Anchistus miersi
(de Man, 1888 [in de Man, 1887–1888]) (Images. 2, 3 & 4)
Harpilius miersi De Man,
1888 : 274, Plate 17, figs 6–10 [type locality : Elpninstone
Island. Mergui Archipelago. Burma].
A. miersi. – Holthuis. 1952 :
110–111, Fig 45. – Bruce, 1973 : 136, Fig. 1c–e. – Monod, 1976 : 24–26, figs
29–36. De Grave, 1999: 132–133.
Material
examined
NBFGR/PALAMIE.01,
female (CL: 3.0 mm, ID no: DBTLD224) and 1 male (CL 2.5 mm, ID no: DBTLD186),
coral reef lagoon at Agatti Island, Lakshadweep,
Arabian Sea, Indian Ocean (10.8533N & 72.1872E), 4 m depth, associated with
T. maxima, temperature 28.20 C, Salinity 35 ppt, February
2020.
Diagnosis
Carapace
(Image 2) glabrous and more or less dorsally convex with a strong antennal
tooth. Rostrum Fig 1A) short and directed downwards, slightly reaching the
distal end of second antennular peduncle; terminal end rounded and bearing 2–3
teeth on the upper border, ventral of the terminal end rounded with few plumose
setae. Abdomen tergites dorsally rounded and somewhat compressed. The posteroventral angle of the 4th & 5th
somite rounded, 6th somite bearing a strong tooth in postero-ventrally. The nature of the telson smooth and
thin, about 1.6 times as long as 6th abdominal somites,
and bears two pairs of dorsolateral spines; terminal end rounded and bears with
small 4 pairs of posterior-distal spines (Figure 1B). Uropod rounded
posteriorly and bearing with a movable tooth in the lateral side, slightly
exceeded in the distal end of telson. Basal antennular peduncle (Figure 1C)
with anterolateral tooth, second and third segments short. Stylocerite
acute distally and exceeding to middle of the first antennular segment; both
flagella almost equal, upper antennular flagellum fused with 13 segments and
free ramus with 11 segmented, which has few hairy setae in distally. The
antennal scale (Figure 1D) with a strong anterolateral spine, and distinctly
exceeded distal end with few long plumose setae. Third maxilliped with
well-developed exopod; the antepenultimate segment about 1.5 times as long as
the penultimate segment with few lateral setae, ultimate segment short and
fringed with numerous setae. The first pereopod slender, merus
slightly longer than carpus. The ventral side of the carpus with few long setae
and fingers with nine groups of setae present dorsally. Second pereopods (Image
2) symmetrical, carpus short, and triangle-shaped with palm stout, dactylus
curved hook like structure at anteriorly and proximally with strong tooth and
few small teeth; female pereopods somewhat similar in length, dactylus about
0.5 lengths of palm, whereas in male, major dactylus is about 0.5 in the length
of the palm and minor dactylus is 0.64 length of the palm. Pereopods III–VI
(Figure 1E–J) similar in size; propodus have few long
setae at the distal end, their dactylus short and hook liked structure with a
microscopic tooth in flexor margin. The third and fourth pereopods stout and
similar in structures, merus about 2.3 times as long
as carpus; propodus subequal to merus,
about 7.3 lengths of dactylus. Fifth pereopods slightly compressed, merus about 1.9 times as long as carpus, propodus about 1.1 times as long as merus,
2.1 times as long as carpus, and 8.5 times of dactylus.
Colouration in life
The body
and appendages are commonly translucent with scattered small blue spots (Image
3). Rostrum with few blue dots, antennal scale, and antennular peduncle with
blue spots, but flagellum is transparent. The second pereopods are translucent
with lined blue dots dorsally. The third─fifth
pereopods are transparent without any marks. Eyes are translucent with small
dark blue dots in eyestalk, cornea with dark black with translucent. The ovary
is greenish.
Habitat and
Distribution
The present
species was caught from the mantle cavity of the Giant clam, T. maxima (Röding, 1798) (Image 4) in the lagoon region of Agatti island (10.8533N & 72.1872E), Lakshadweep at the
depth of 4 m. A. miersi is widely distributed
in Indo-Pacific regions, ranging from the Red Sea, eastern Africa to the
Gambier Archipelago through Maldive and Chagos Islands, Seychelles; Zanzibar, Kenya, Tanganyika,
Madagascar, Andaman Islands, and the Philippines. In common, this species is
associated with the Tridacna clam (subfamily Tridacninae).
However, it also occurred within bivalve of the genera Hippopus,
Pinna, Magnavicula, and Meleagrina
(Bruce 1978; Chace & Bruce 1993; De grave 1999; Neo et al. 2014).
Remarks
The present
Indian specimens were agreed well with previous descriptions of De Man (1888)
and Kemp (1922) with their key characteristics of Jayachandran (2001) with
carapace and architecture of rostrum, presence of antennal spines, dactylus
dentation of second pereopods, and its colour
patterns. The general appearance of the Indian materials is similar with
earlier finding, but a female individual is bigger than the male. Also, some
remarkable differences were noticed in the present organisms, upper antennular
flagellum fused with 13 segments and free ramus segmented with 11 articles
(where de Man mentioned few segments fused in basally), the antepenultimate
segment of third maxilliped is broader much than the penultimate segment.
Dactylus of ambulatory pereopods with hook-like distal end with a microscopic
tooth in flexor margin, fifth pereopod slightly compressed and longer than
third and fourth pereopods. However, minute spinules
or granules were not able to observe on the anterior border on the dactylus,
where Fujino (1975) described the minute granules
with the help of scanning electron microscopy.
The present
individuals of A. miersi had an appealing colour pattern in their overall body with transparent and
small dark blue spots, which also agree well with the previous descriptions of
Bruce (1976) and Neo et al. (2014). However, he has noticed two different colour spots (red and blue) over the body and appendages.
Commonly, Anchistus shrimps live as pairs in
the host animals, especially bivalves (Bruce 1975; Fujino
1975). This colour variation is caused due to sexual
dimorphism and based on their dwelling habitats (Bruce 1976). De Grave (1999)
reported red dots and transparent colour in both the
animals obtained from the Hansa Bay associated with Magnavicula
penguin at the depth of 19 m. Neo et al. (2015) also noticed red dots in
the male organism, wherein female blue dots were noticed, which were associated
with a fluted giant clam, Tridacna squamosa from Singapore waters. In
the present study, both the sex had dark blue spots in the body, which were
associated with Giant clam, T. maxima from Agatti
Island, Lakshadweep. In morphological and colour
patterns wise, A. miersi is closely related to
A. demani. However, A. miersi
differed by the presence of a strong antennal spine (vs absent in A. demani), very minute and conspicuous accessory spinules in the third-fifth pereopods (vs inconspicuous and
blunt in A. demani). The colour
patterns also differed between these two species, small blue spots over the
body for A. miersi and comparatively bigger in
size of blue spots for A. demani individuals
(Kemp 1922; Jayachandran 2001).
DNA
Barcoding
The COI DNA
barcoding has been commonly applied for revealing cryptic species complex,
taxonomic ambiguities, delineating species boundaries of crustaceans (Hebert et
al. 2003; Schwentner et al. 2013; Chan et al. 2017).
The present study generated two COI sequences for Indian materials of A. miersi with greater than 650 bp
(Accession No: MW897781 & MW897782). The NCBI has only 12 COI sequences of
the Anchistus species, which have been
retrieved and used for the present analysis where, two sequences are from A.
australis, four from A. miersi,
and another four from A. custoides. It should
also be noted that the sequences of A. demani (KP759379
& KC706757) are not used for the present analysis due to the close
homogeneity with the sequences of A. miersi. It
reveals that misidentified sequences are there in NCBI for A. demani (KP759379 from Madagascar and KC706757 from
French Polynesia), which have >99.5% sequences similarity with the present
Indian materials of A. miersi. Overall, the
present study reveals that the intraspecific genetic divergence for A. miersi is 0.3─1.2 % and the highest interspecific
divergences were showed between these three species which ranged from 9.7─23.9%
(Table 1). On the other hand, a sequence of A. custoides
(MH287043) showed the greatest intraspecific divergences with the Malaysian
materials (Fransen & Reijnen
2012) which has to be restudied with integrative approaches in the future.
Additionally, the phylogenetic tree constructed with the Maximum Likelihood
analysis for available sequences among the Anchistus
species is represented in Figure 2. The A. miersi sequences
from India formed a clade with the other sequences of A. miersi which were retrieved from NCBI and it
confirms the morphological identification of the present Indian materials.
Overall,
the present study reports new occurrence of small commensal shrimp associated
with Giant clam, T. maxima (Roding 1798) in the lagoon regions of Agatti Island, Lakshadweep at the depth of 4 m, which
distribution extended Andaman Sea─Lakshadweep Sea
towards. Additionally, taxonomic, habitat details are represented discussed in
detail. The present report is also strengthening the caridean fauna of the
Lakshadweep waters.
Table 1. Pairwise genetic
distances for Anchistus species using COI gene
sequence data.
|
Species |
1 |
2 |
3 |
4 |
5 |
6 |
7 |
8 |
9 |
10 |
11 |
12 |
1 |
Anchistus miersi JX185707 |
|
|
|
|
|
|
|
|
|
|
|
|
2 |
Anchistus miersi JX185706 |
0.008 |
|
|
|
|
|
|
|
|
|
|
|
3 |
Anchistus miersi JX185705 |
0.008 |
0.003 |
|
|
|
|
|
|
|
|
|
|
4 |
Anchistus miersi JX185704 |
0.012 |
0.007 |
0.003 |
|
|
|
|
|
|
|
|
|
5 |
Anchistus miersi DBTLD224 |
0.007 |
0.008 |
0.008 |
0.012 |
|
|
|
|
|
|
|
|
6 |
Anchistus miersi DBTLD186 |
0.007 |
0.008 |
0.008 |
0.012 |
0.000 |
|
|
|
|
|
|
|
7 |
Anchistus custoides JX185712 |
0.221 |
0.227 |
0.230 |
0.237 |
0.221 |
0.221 |
|
|
|
|
|
|
8 |
Anchistus custoides JX185711 |
0.217 |
0.224 |
0.227 |
0.233 |
0.217 |
0.217 |
0.002 |
|
|
|
|
|
9 |
Anchistus custoides JX185710 |
0.221 |
0.227 |
0.230 |
0.237 |
0.221 |
0.221 |
0.003 |
0.002 |
|
|
|
|
10 |
Anchistus australis JX185709 |
0.097 |
0.097 |
0.101 |
0.106 |
0.101 |
0.101 |
0.239 |
0.239 |
0.242 |
|
|
|
11 |
Anchistus australis JX185708 |
0.099 |
0.099 |
0.104 |
0.108 |
0.104 |
0.104 |
0.229 |
0.229 |
0.232 |
0.005 |
|
|
12 |
Anchistus custoides MH287043 |
0.201 |
0.196 |
0.199 |
0.204 |
0.196 |
0.196 |
0.125 |
0.122 |
0.120 |
0.227 |
0.224 |
|
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