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Population structure and reproductive performance in the sea anemone associated shrimp Ancylocaris brevicarpalis (Caridea: Palaemonidae)

Published online by Cambridge University Press:  08 February 2021

Sanjeevi Prakash Open the ORCID record for Sanjeevi Prakash [Opens in a new window] ,
Ampuli Muthu  and
Amit Kumar Open the ORCID record for Amit Kumar [Opens in a new window]
Sanjeevi Prakash*
Affiliation:
Centre for Climate Change Studies, Sathyabama Institute of Science and Technology, Rajiv Gandhi Salai, Chennai600 119, Tamil Nadu, India Sathyabama Marine Research Station, Sallimalai Street, Rameswaram623526, Tamil Nadu, India
Ampuli Muthu
Affiliation:
Centre for Climate Change Studies, Sathyabama Institute of Science and Technology, Rajiv Gandhi Salai, Chennai600 119, Tamil Nadu, India
Amit Kumar
Affiliation:
Centre for Climate Change Studies, Sathyabama Institute of Science and Technology, Rajiv Gandhi Salai, Chennai600 119, Tamil Nadu, India Sathyabama Marine Research Station, Sallimalai Street, Rameswaram623526, Tamil Nadu, India
*
Author for correspondence: Sanjeevi Prakash, E-mail: [email protected]
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Abstract

The peacock-tail shrimp Ancylocaris brevicarpalis Schenkel, 1902, is an obligate symbiont of sea anemones and well known for its remarkable colouration. Yet, very little information is available about its population structure and life-history traits, including reproductive parameters (fecundity, embryo volume and reproductive output). A total of 574 individuals were collected from the Gulf of Mannar, Tamil Nadu, India between February 2017 and July 2018, out of which 214 were males (37.28%), 355 were females (61.84%), and 5 (0.87%) juveniles. The highest percentage of individuals were observed in the post-monsoon season (38.10%) followed by monsoon (34.85%), pre-monsoon (15.02%), and summer seasons (12.01%). The overall sex ratio was skewed towards female individuals (0.55 male: 1 female). Fecundity was higher in females carrying early-stage embryos and embryo volume did increase, but not statistically significantly from early to late stages. The reproductive output was negatively allometric to the mean female body weight. The present study provides first-of-its-kind information on the population as well as individual-level reproductive characteristics of A. brevicarpalis.

Keywords

CarideaPalaemonidaepopulation dynamicsreproductionsymbiotic shrimp
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 101 , Issue 1 , February 2021 , pp. 109 - 116
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Alon, N and Stancyk, NE (1982) Variation in life-history patterns of the grass shrimp Palaemonetes pugio in two South Carolina estuarine systems. Marine Biology 68, 265–276.CrossRefGoogle Scholar
Anger, K and Moreira, GS (1998) Morphometric and reproductive traits of tropical caridean shrimps. Journal of Crustacean Biology 18, 823–838.CrossRefGoogle Scholar
Azofeifa-Solano, JC, Elizondo-Coto, M and Wehrtmann, I (2014) Reproductive biology of the sea anemone shrimp Periclimenes rathbunae (Caridea, Palaemonidae, Pontoniinae), from the Caribbean coast of Costa Rica. ZooKeys 457, 211.CrossRefGoogle Scholar
Baeza, JA (2006) Testing three models on the adaptive significance of protandric simultaneous hermaphroditism in a marine shrimp. Evolution 60, 1840–1850.CrossRefGoogle Scholar
Baeza, JA (2010) Molecular systematics of peppermint and cleaner shrimps: phylogeny and taxonomy of the genera Lysmata and Exhippolysmata (Crustacea: Caridea: Hippolytidae). Zoological Journal of the Linnaean Society 160, 254–265.CrossRefGoogle Scholar
Baeza, JA (2013) Molecular phylogeny of broken-back shrimps (genus Lysmata and allies): a test of the ‘Tomlinson–Ghiselin’ hypothesis explaining the evolution of hermaphroditism. Molecular Phylogenetics and Evolution 69, 46–62.CrossRefGoogle ScholarPubMed
Baeza, JA (2015) Crustaceans as symbionts: an overview of their diversity, host use and lifestyles. In Watling, L and Thiel, M (eds), The Lifestyles and Feeding Biology of the Crustacea. Oxford: Oxford University Press, pp. 163–189.Google Scholar
Baeza, JA and Bauer, RT (2004) Experimental test of socially mediated sex change in a protandric simultaneous hermaphrodite, the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae). Behavioral Ecology and Sociobiology 55, 544–550.Google Scholar
Baeza, JA and Behringer, DC (2017) Integrative taxonomy of the ornamental ‘peppermint’ shrimp market and population genetics of Lysmata boggessi, the most heavily traded species worldwide. PeerJ 5, e3786.CrossRefGoogle ScholarPubMed
Baeza, JA and Diaz-Valdes, M (2011) The symbiotic shrimp Ascidonia flavomaculata lives solitarily in the tunicate Ascidia mentula: implications for its mating system. Invertebrate Biology 130, 351–361.CrossRefGoogle Scholar
Baeza, JA and Hernaez, P (2015) Population distribution, sexual dimorphism, and reproductive parameters in the crab Pinnixa valdiviensis Rathbun, 1907 (Decapoda: Pinnotheridae), a symbiont of the ghost shrimp Callichirus garthi (Retamal, 1975) in the south eastern Pacific. Journal of Crustacean Biology 35, 68–75.CrossRefGoogle Scholar
Baeza, JA and Piantoni, C (2010) Sexual system, sex ratio, and group living in the shrimp Thor amboinensis (De Man): relevance to resource-monopolization and sex-allocation theories. Biological Bulletin 219, 151–165.CrossRefGoogle Scholar
Baeza, JA and Prakash, S (2019) An integrative taxonomic and phylogenetic approach reveals a complex of cryptic species in the ‘peppermint’ shrimp Lysmata wurdemanni sensu stricto. Zoological Journal of the Linnaean Society 184, 1018–1038.CrossRefGoogle Scholar
Baeza, JA and Thiel, M (2007) The mating system of symbiotic crustaceans: a conceptual model based on optimality and ecological constraints. In Duffy, JE and Thiel, M (eds), Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms. Oxford: Oxford University Press, pp. 250–267.Google Scholar
Baeza, JA, Hemphill, CA and Ritson-Williams, R (2015) The sexual and mating system of the shrimp Odontonia katoi (Palaemonidae, Pontoniinae), a symbiotic guest of the Ascidian Polycarpa aurata in the Coral Triangle. PLoS ONE 10, e0121120.CrossRefGoogle Scholar
Baeza, JA, Simpson, L, Ambrosio, LJ, Guéron, R and Mora, N (2016) Monogamy in a hyper symbiotic shrimp. PLoS ONE 11, e0149797.CrossRefGoogle Scholar
Baeza, JA, Barros-Alves, SP, Lucena, RA, Lima, SFB and Alves, DFR (2017) Host use pattern of the shrimp Periclimenes paivai on the scyphozoan jellyfish Lychnorhiza lucerna: probing for territoriality and inferring its mating system. Helgoland Marine Research 71, 1–10.CrossRefGoogle Scholar
Balasundaram, C and Pandian, TJ (1982) Egg loss during incubation in Macrobrachium nobili (Henderson & Mathai). Journal of Experimental Marine Biology and Ecology 59, 289–299.CrossRefGoogle Scholar
Bauer, RT (1989) Continuous reproduction and episodic recruitment in nine shrimp species inhabiting a tropical sea grass meadow. Journal of Experimental Marine Biology and Ecology 127, 175–187.CrossRefGoogle Scholar
Bauer, RT (1991) Sperm transfer and storage structures in penaeoid shrimps: a functional and phylogenetic perspective. In Bauer RT and Martin JW (eds), Crustacean Sexual Biology. New York, NY: Columbia University Press, pp. 183–207.CrossRefGoogle Scholar
Bauer, RT (2004) Remarkable Shrimps: Adaptations and Natural History of the Carideans. Norman, OK: University of Oklahoma Press.Google Scholar
Bolaños, JA, Baeza, JA, Hernandez, JE, Lira, C and López, R (2012) Population dynamics and reproductive output of the nonindigenous crab Charybdis hellerii in the southeastern Caribbean Sea. Journal of the Marine Biological Association of the United Kingdom 92, 469–474.CrossRefGoogle Scholar
Bolker BM, S, Mary, CM, Osenberg, CW, Schmitt, RJ and Holbrook, SJ (2002) Management at a different scale: marine ornamentals and local processes. Bulletin of Marine Sciences 70, 733–748.Google Scholar
Bruce, AJ (1976) A report on a small collection of shrimps from the Kenya National Marine Parks at Malindi, with notes on selected species. Zoologische Verhandelingen 145, 1–72.Google Scholar
Bruce, AJ and Svoboda, A (1983) Observations upon some pontoniine shrimps from Aqaba, Jordan. Rijksmuseum van Natuurlijke Historie 205, 1–44.Google Scholar
Calado, R (2008) Marine Ornamental Shrimps: Biology, Aquaculture and Conservation. Oxford: Wiley–Blackwell.Google Scholar
Calado, R, Lin, J, Rhyne, AL, Araujo, R and Narciso, L (2003) Marine ornamental decapods popular, pricey, and poorly studied. Journal of Crustacean Biology 23, 963–973.CrossRefGoogle Scholar
Clark, A (1993) Reproductive trade-offs in caridean shrimps. Functional Ecology 7, 411–419.CrossRefGoogle Scholar
Corey, S (1987) Comparative fecundity of four species of crayfish in Ontario. Crustaceana 52, 276–282.CrossRefGoogle Scholar
Corey, S and Reid, DM (1991) Comparative fecundity of decapod crustaceans I. The fecundity of thirty-three species of nine families of caridean shrimp. Crustaceana 60, 270–294.CrossRefGoogle Scholar
Correa, C and Thiel, M (2003) Mating systems in caridean shrimp (Decapoda: Caridea) and their evolutionary consequences for sexual dimorphism and reproductive biology. Revista Chilena de Historia Natural 76, 187–203.CrossRefGoogle Scholar
Dee, LE, Horii, SS and Thornhill, DJ (2014) Conservation and management of ornamental coral reef wildlife: successes, shortcomings, and future directions. Biological Conservation 169, 225–237.CrossRefGoogle Scholar
De Grave, S, Smith, KG, Adeler, NA, Allen, DJ, Alvarez, F, Anker, A and Page, TJ (2015 a) Dead shrimp blues: a global assessment of extinction risk in freshwater shrimps (Crustacea: Decapoda: Caridea). PLoS ONE 10, e0120198.CrossRefGoogle Scholar
De Grave, S, Fransen, CHJM and Page, TJ (2015 b) Let's be pals again: major systematic changes in Palaemonidae (Crustacea: Decapoda). PeerJ 3, e1167.CrossRefGoogle Scholar
Diaz, AC, Sousa, LG, Cuartas, EI and Petriella, AM (2003) Growth, molt and survival of Palaemonetes argentinus (Decapoda, Caridea) under different light-dark conditions. Iheringia Serie Zoologia 93, 249–254.CrossRefGoogle Scholar
Dickson, MD, Behringer, DC and Baeza, JA (2020) Life history traits and reproductive performance of the caridean shrimp Lysmata boggessi, a heavily traded invertebrate in the marine aquarium industry. PeerJ 8, e8231.CrossRefGoogle ScholarPubMed
Duffy, JE (1996) Eusociality in a coral-reef shrimp. Nature 381, 512.CrossRefGoogle Scholar
Echeverría-Sáenz, S and Wehrtmann, IS (2011) Egg production of the commercially exploited deepwater shrimp, Heterocarpus vicarius (Decapoda: Pandalidae), Pacific Costa Rica. Journal of Crustacean Biology 31, 434–440.CrossRefGoogle Scholar
ENVIS (2015) Database on Gulf of Mannar Biosphere Reserve. Environmental Information System Center. Department of Environment, Government of Tamil Nadu, Chennai.Google Scholar
Fautin, DG and Allen, GR (1992) Field Guide to Anemonefishes and their Host Sea Anemones. Perth: Western Australian Museum.Google Scholar
Fautin, DG, Guo, CC and Hwang, JS (1995) Costs and benefits of the symbiosis between the anemone shrimp Periclimenes brevicarpalis and its host Entacmaea quadricolor. Marine Ecology Progress Series 129, 77–84.CrossRefGoogle Scholar
Fernandez, M, Pardo, LM and Baeza, JA (2002) Patterns of oxygen supply in embryo masses of brachyuran crabs throughout development: the effect of oxygen availability and chemical cues in determining female brooding behavior. Marine Ecology Progress Series 245, 181–190.CrossRefGoogle Scholar
Gilpin, JA and Chadwick, NE (2017) Life-history traits and population structure of Pederson cleaner shrimps Ancylomenes pedersoni. Biological Bulletin 233, 190–205.CrossRefGoogle ScholarPubMed
Harikrishnan, M, Unnikrishnan, U, Maju, MS, Reena Greeshma, AR and Kurup, BM (2010) Size at sexual maturity, egg number and reproductive output of the snapping shrimp Alpheus euphrosyne euphrosyne De Man, 1897. Invertebrate Reproduction and Development 54, 195–202.CrossRefGoogle Scholar
Hartnoll, RG (1978) The determination of relative growth in Crustacea. Crustaceana 34, 281–293.CrossRefGoogle Scholar
Hartnoll, RG (1982) Growth. In Bliss, DE and Abele, LG (eds), The Biology of Crustacea, Vol. 2: Embryology, Morphology, and Genetics. New York, NY: Academic Press, pp. 111–196.Google Scholar
Heard, RW and Spotte, S (1991) Pontoniinae shrimps (Decapoda: Caridea: Palaemonidae) of the northwest Atlantic. II. Periclimenes patae, new species, a gorgonian associate from shallow reef areas off the Turks and Caicos Islands and Florida Keys. Proceedings of the Biological Society, Washington 104, 40–48.Google Scholar
Hines, AH (1988) Fecundity and reproductive output in two species of deep-sea crabs, Greyson fenerri and G. quinquedens (Decapoda, Brachyura). Journal of Crustacean Biology 8, 557–562.CrossRefGoogle Scholar
Hines, AH (1991) Fecundity and reproductive output in nine species of Cancer crabs (Crustacea, Brachyura, Candridae). Canadian Journal of Fishery and Aquatic Sciences 48, 267–275.CrossRefGoogle Scholar
Horka, I, De Grave, S, Fransen C, H, Petrusek, A and Duris, Z (2016) Multiple host switching events shape the evolution of symbiotic palaemonid shrimps (Crustacea: Decapoda). Scientific Reports 6, 26486.CrossRefGoogle Scholar
Kemp, S (1922) Notes on Crustacea Decapoda in the Indian Museum. XV. Pontoniinae. Records of the Indian Museum 24, 3.Google Scholar
Kim, S and Hong, S (2004) Reproductive biology of Palaemon gravieri (Decapoda: Caridea: Palaemonidae). Journal of Crustacean Biology 24(1), 121–130.CrossRefGoogle Scholar
Kuris, AM (1991) A review of patterns and causes of crustacean brood mortality. In Wenner, A and Kuris, A (eds), Crustacean Egg Production. Crustacean Issues 7. Rotterdam: AA Balkema, pp. 117–141.Google Scholar
Levitt-Barmats, Y and Shenkar, N (2018) Observations on the symbiotic relationship between the caridean shrimp Odontonia sibogae (Bruce, 1972) and its ascidian host Herdmania momus (Savigny, 1816). PLoS ONE 13, e0192045.CrossRefGoogle Scholar
Martínez-Mayén, M and Román-Contreras, R (2009) Reproduction of Periclimenes siankaanensis (Decapoda, Caridea, Palaemonidae) in Bahía de la Ascensión, Quintana Roo, México. Crustaceana 82, 27–37.Google Scholar
Nakashima, Y (1987) Reproductive strategies in a partially protandrous shrimp, Athanas kominatoensis (Decapoda: Alpheidae): sex change as the best of a bad situation for subordinates. Journal of Ethology 5, 145–159.CrossRefGoogle Scholar
Naylor, C, Adams, J and Greenwood, PJ (1988) Variation in sex determination in natural populations of a shrimp. Journal of Evolutionary Biology 1, 355–368.CrossRefGoogle Scholar
Nizinski, MS (1989) Ecological distribution, demography and behavioral observations on Periclimenes anthophilus, an atypical symbiotic cleaner shrimp. Bulletin of Marine Sciences 45, 174–188.Google Scholar
Oh, CW and Hartnoll, RG (1999) Size at sexual maturity, reproductive output, and seasonal reproduction of Philocheras trispinosus (Decapoda) in Pot Erin Bay, Isle of Man. Journal of Crustacean Biology 19, 252–259.CrossRefGoogle Scholar
Oliveira, MV, Costa-Souza, AC, Mariano, R and Almeida, AO (2018) Fecundity, embryo size and embryo loss in the estuarine shrimp Salmoneus carvachoi Anker, 2007 (Crustacea: Alpheidae) from a tidal mudflat in northeastern Brazil. Papéis Avulsos de Zoologia 58, e20185845.CrossRefGoogle Scholar
Omori, K, Yanagisawa, Y and Hori, N (1994) Life history of the caridean shrimp Periclimenes ornatus Bruce associated with a sea anemone in southwest Japan. Journal of Crustacean Biology 14, 132–145.CrossRefGoogle Scholar
Patton, WK, Patton, RJ and Barnes, A (1985) On the biology of Gnathophylloides mineri, a shrimp inhabiting the sea urchin Tripneustes ventricosus. Journal of Crustacean Biology 5, 616–626.CrossRefGoogle Scholar
Possenti, E, Sartor, P and De Ranieri, S (2007) Reproductive biology of females of Plesionika edwardsii (Brandt, 1851) (Crustacea, Decapoda, Pandalidae) in the northern Tyrrhenian Sea (western Mediterranean). Atti della Societa toscana di scienze naturali, Memorie, Serie B 114, 91–98.Google Scholar
Prakash, S and Marimuthu, N (2020) Notes on some crinoid associated crustacean decapods (Crustacea: Decapoda) from Lakshadweep Archipelago, Central Indian Ocean. Zootaxa 4766(1), 86–100.CrossRefGoogle ScholarPubMed
Prakash, S, Babu, I, Gopi, M, Ajith Kumar, TT and Balasubramanian, T (2011) Discovery of the shrimp Pycnocaris chagoae Bruce, 1972 (Decapoda: Caridea: Gnathophyllidae) in the Lakshadweep Archipelago, India. Zootaxa 2998, 66–68.CrossRefGoogle Scholar
Prakash, S, Ajith Kumar, TT and Subramoniam, T (2015) Notes on some Indo-Pacific caridean shrimps (Crustacea: Decapoda, Caridea: Palaemonidae and Gnathophyllidae) particularly from India. Zootaxa 3914, 456–466.CrossRefGoogle ScholarPubMed
Prakash, S, Ajith Kumar, TT, Bauer, R, Thiel, M and Subramoniam, T (2016) Reproductive morphology and mating behaviour in the hinge-beak shrimp Rhynchocinetes durbanensis Gordon, 1936 (Decapoda: Caridea: Rhynchocinetidae) in India. Journal of the Marine Biological Association of the United Kingdom 96, 1331–1340.CrossRefGoogle Scholar
Prakash, S, Ajith Kumar, TT, Subramoniam, T and Baeza, JA (2017 a) Sexual system and sexual dimorphism in the shrimp Periclimenes brevicarpalis (Schenkel, 1902) (Caridea: Palaemonidae), symbiotic with the sea anemone Stichodactyla haddoni (Saville-Kent, 1893) in the Gulf of Mannar, India. Journal of Crustacean Biology 37, 332–339.CrossRefGoogle Scholar
Prakash, S, Ajith Kumar, TT, Raghavan, R, Rhyne, A, Tlusty, M and Subramoniam, T (2017 b) Marine aquarium trade in India: challenges and opportunities for conservation and policy. Marine Policy 77, 120–129.CrossRefGoogle Scholar
Rajool, SCP, Akhilesh, KV, Manjebrayakath, H, Ganga, U and Pillai, NGK (2012) Shrimps of the family Pandalidae (Caridea) from Indian waters, with new distributional record of Plesionika adensameri (Balss, 1914). Journal of the Marine Biological Association, India 54, 45–49.Google Scholar
Rhyne, A, Rotjan, R, Bruckner, A and Tlusty, M (2009) Crawling to collapse: ecologically unsound ornamental invertebrate fisheries. PLoS ONE 4, e8413.CrossRefGoogle ScholarPubMed
SAC (2012) Coastal Zones of India. Ahmedabad: Space Applications Centre.Google Scholar
SAS (2015) Base SAS 9.4 Procedures Guide. Cary, NC: SAS Institute.Google Scholar
Schenkel, E (1902) Beitragzur Kenntnis der Dekapoden fauna von Celebes. Verhandlungen der Naturforschenden Gesellschaft, Basel 13, 485–585.Google Scholar
Simoes, SM, D'Incao, F, Fransozo, A, Leão Castilho, A and Costa, CR (2013) Sex ratio, growth and recruitment of the pelagic shrimp Acetes americanus on the southeastern coast of Brazil. Journal of Crustacean Biology 33, 1–9.CrossRefGoogle Scholar
Sokal, RR and Rohlf, FJ (1981) Biometry. San Francisco, CA: Freeman.Google Scholar
Spotte, S (1997) Sexual and regional variation in the morphology of the spotted anemone shrimp Periclimenes yucatanicus (Decapoda: Caridea: Palaemonidae). Journal of Crustacean Biology 17, 389–397.CrossRefGoogle Scholar
Spotte, S (1999) Possible synonymy of the western Atlantic anemone shrimps Periclimenes pedersoni and P. anthophilus based on morphology. Bulletin of Marine Sciences 65, 407–417.Google Scholar
Suzuki, K and Hayashi, KI (1977) Five caridean shrimps associated with sea anemones in central Japan. The Seto Marine Biological Laboratory 24, 193–208.Google Scholar
Tikader, BK, Daniel, A and Subbarao, NV (1986) Sea Shore Animals of Andaman and Nicobar Islands. Kolkata: Zoological Survey of India.Google Scholar
Titus, BM, Daly, M, Hamilton, N, Berumen, ML and Baeza, JA (2018) Global species delimitation and phylogeography of the circumtropical ‘sexy shrimp’ Thor amboinensis reveals a cryptic species complex and secondary contact in the Indo-West Pacific. Journal of Biogeography 45, 1275–1287.CrossRefGoogle Scholar
Turner, RL and Lawrence, JM (1979) Volume and composition of echinoderm eggs: implications for the use of egg size in life-history models. In Stancyk SE (ed.), Reproductive Ecology of Marine Invertebrates. Columbia, SC: University of South Carolina Press, pp. 25–40.Google Scholar
Unmesh, K and Prakash, S (2011) On a documentation of Haddon's carpet anemone (Stichodactyla haddoni) (Saville-Kent, 1893) (Anthozoa: Actiniaria: Stichodactylidae) and its unique symbiotic fauna from Gulf of Kutch. Bugs R All (Newsletter of the Invertebrate Conservation and Information Network of South Asia) 17, 31–34.Google Scholar
Venkataraman, K and Wafar, M (2005) Coastal and marine biodiversity in India. Indian Journal of Geo-Marine Sciences 34, 57–75.Google Scholar
Wenner, AM (1972) Sex ratio as a function of size in marine crustacean. American Naturalist 106, 321–351.CrossRefGoogle Scholar
Zar, JH (1996) Biostatistical Analysis, 3rd Edn. Englewood Cliffs, NJ: Prentice-Hall.Google Scholar
Zhang, D, Rhyne, AL and Lin, J (2007) Density-dependent effect on reproductive behaviour of Lysmata amboinensis and L. boggessi (Decapoda: Caridea: Hippolytidae). Journal of the Marine Biological Association of the United Kingdom 87, 517–522.CrossRefGoogle Scholar