Research ArticleEcological Significance of the Association betweenStomopneustes variolaris (Echinoidea) and Lumbrinerislatreilli (Polychaeta) from Visakhapatnam Coast India
Archana Ayyagari and Ramesh Babu Kondamudi
Department of Marine Living Resources Andhra University Visakhapatnam Andhra Pradesh 530 002 India
Correspondence should be addressed to Archana Ayyagari archanaayyagariyahoocom
Received 17 May 2014 Revised 7 July 2014 Accepted 27 July 2014 Published 14 August 2014
Academic Editor Evgeny Pakhomov
Copyright copy 2014 A Ayyagari and R B Kondamudi This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited
The present study reports a new association between the sea urchin Stomopneustes variolaris (Lamarck 1816) and the polychaeteLumbrineris latreilli (Audouin amp Milne Edwards 1834) based on the specimens collected intertidally at Bay of Bengal(Visakhapatnam east coast of India) Out of 60 sea urchins collected 10 (1667) were associated with the polychaete Theprevalence increased with the increasing sea urchin test diameter All polychaetes were exclusively found between the spines in theaboral region of the host This association protects the polychaete from the predators during displacement from its natural habitat
1 Introduction
Polychaetous annelids are the most abundant and cos-mopolitan marine metazoans in the benthic environment[1] Particularly in soft bottoms they dominate in termsof species abundance and biomass [2] Most of them arefree living crawling burrowing and tube-dwelling animalsbut many live in symbiosis with other marine invertebrates[3] of which the echinoderms include a higher number ofspecies harbouring polychaetes The overall association ofpolychaetes with echinoderms is 538 [4]
Polychaetes are highly vulnerable to predators includingfish and other invertebrates Some of them are soft bodiedanimals lack protective exoskeleton and have poor displace-ment capacities [5 6] To protect themselves from predatorsthey sometimes take shelter in other marine flora and faunawith this often leading to the establishment of highly specificrelationships that may lead to different kinds of symbiosisAmong the echinoderms sea urchins have physical defenses(ie test spines) and thatmakes them suitable to harbour andprotect marine organisms such as molluscs shrimps crabspolychaetes copepods and fish [7ndash9]
Stomopneustes variolaris (Lamarck 1816) is a tropicalrock boring Indo-Pacific echinoid found at the intertidal
Lumbrineris latreilli (Audouin amp Milne Edwards 1834) is afree living soft bottom dwelling burrowing polychaete thatlives in mucous lined burrows found in Visakhapatnam coast[10]The present study reports for the first time an associationbetween S variolaris and L latreilli in the intertidal regionof VisakhapatnamThe significance of this association is alsodiscussed
2 Materials and Methods
Sea urchins were hand-collected in March and April 2013from the rocky areas of the intertidal region of Visakhapat-nam 17∘1410158403010158401015840N and 83∘1610158402510158401015840 E (east coast of India) duringlow tide as part of a study on the intertidal fauna
The collected sea urchins S variolaris were transportedto the laboratory alive The spines of the sea urchinswere removed Their diameter was measured perpendicu-larly to oral-aboral axis using Vernier callipers Polychaetes(Figures 1(a) and 1(b)) associated with the sea urchins wereseparated fixed and preserved in 70 ethanol Later theirtotal length was measured from the tip prostomium to theend of pygidium using calibrated ocular micrometer understereomicroscope and also the number of segments was
Hindawi Publishing CorporationJournal of Marine BiologyVolume 2014 Article ID 640785 4 pageshttpdxdoiorg1011552014640785
counted The maxillary apparatus of each individual wasextracted after an anterodorsal incision and mounted on aslide to study the details of both maxillae and the mandiblesunder an optical microscope Parapodium was separatedfrom polychaete placed on a slide with a drop of glycerol andcoveredwith a cover slip and the chaetaewere observed underan Olympus compound microscope
3 Results
31 Description of Lumbrineris latreilli (Figure 2) Polychaetecolour is pale red or brown in live condition Body islong ranging from 60mm to 64mm (55ndash58 segments)gradually tapering towards the pygidium The prostomiumis blunt conical the length being slightly longer than widthand has no eyes and appendages Peristomium apodousconsists of two rings of equal size All the parapodia areuniramous Parapodium in the anterior segments has a shortrounded prechaetal lobe and digitiform postchaetal lobeAnterior parapodia have capillary chaetae and compoundmultidentate hooded hooks with long blades The rest ofthe parapodia have few capillary chaetae and simple hoodedhooks of similar sizes Jaw apparatus is well developed andis of the labidognatha type Maxillae II are almost as long asmaxillae I and are connected to them with a ligament Themaxilla II has four teeth maxilla III has two teeth andmaxillaIV is unidentate with pointed tooth Mandibles are compactand fused medially Aciculae are yellow in color and straight
0123456789
Prev
alen
ce (
)
Test diameter (mm)
y = 2156x minus 08
R2 = 0964
50ndash54 55ndash59 60ndash64 65ndash69
Figure 3 Relationship between the size of Stomopneustes variolarisand its infestation prevalence by Lumbrineris latreilli
32 Description of the Association Among 60 specimens ofS variolaris collected of diameter ranging from 30mm to76mm during the study period only 10 (1667) of thesea urchins were found to be associated with L latreilliEach sea urchin was found to be associated with only onepolychaete In this study it was observed that sea urchins ofdiameter in the range of 50mm to 70mm were found to beassociated with the polychaete L latreilli of average length604 plusmn 22mm The polychaete was found attached to theaboral side of the test of the sea urchin between the spinesIts presence could be noticed only when the sea urchin spineswere removedThe percentage of prevalence was more as testsize increases (119910 = 2156119909 minus 08 119877 = 0964 119875 = 002)(Figure 3)
4 Discussion
Many polychaetes including polynoids syllids and hesionidslive in either obligate or facultative association with echin-oderms [3] to derive protection from predators and foodfrom the host They often prefer the oral surface from wherethey may easily access to the food collected by the host whileothers prefer aboral surface feeding on the semi digested ordigested matter released by the host [11] Similar associationand feeding pattern was observed in another polychaeteHesione picta (Muller 1858) feeding on the undigestedmaterial released by the brittle star Ophionereis reticulata
Journal of Marine Biology 3
(Say 1825) Two of them like the amphinomid Benthoscolexcubanus (Hartman 1942) or the polynoid Gorekia crassicirris(Willey 1902) were even found inside the gut of irregular seaurchins [12]
In the present study Lumbrineris latreilli was foundattached to the test on the aboral side between the ambitusand the genital plates and accordingly the polychaete mayfeed on the undigested organic matter released by the seaurchin S variolaris
Thepresent association is between a softbottomburrowerL latreilli [13] and the rock boring sea urchin S vario-laris Both are intertidal dwellers living in different habitatsThe association of polychaete with sea urchin is due toits displacement from natural habitat during the upwelling[6 14] and dredging operations [15] Lumbrineris speciesare vulnerable to the direct effects of dredging and to thedeposition of sediments mobilized during dredging [16 17]
The principal benefit of the association however seemsto be protective as the host is shielding the polychaete frompossible predators by means of the spines Other marineorganisms reported to be associated with sea urchin areshrimps [18 19] crabs [9] and young of many fish speciesFurther the polychaete colour which is brown camouflageswith the colour of the test of the sea urchin precluding therecognition by the predators
Another plausible reasonmight be that these worms havestrong tendency to come from the soft bottom on to the algalzone for spawning as this behavior is beneficial for successfulfertilization and larval dispersal [20] During this time theymay seek shelter in sea urchins that also inhabit in this zone
5 Conclusion
Lumbrineris latreilli is a benthic dweller feeding on thesediment and its association with a rock boring sea urchinS variolaris is to tide over unfavorable circumstances likeupwelling and dredging This association protects the poly-chaete from the predators during displacement from itsnatural habitat
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Archana Ayyagari acknowledges the Department of Scienceand Technology Government of India for providing herwith the financial support The authors would like to thankDr R Rajasekaran and Dr T A Britayev for helping withthe polychaete identification The authors heartily thank allreviewers for the valuable suggestions on the paper
References
[1] M Wisshak and C Neumann ldquoA symbiotic association of aboring polychaete and an echinoid from the Late Cretaceous
of Germanyrdquo Acta Palaeontologica Polonica vol 51 no 3 pp589ndash597 2006
[2] G A Knox ldquoThe role of polychaetes in benthic soft-bottomcommunitiesrdquo in Essays on Polychaetous Annelids in Memory ofOlga Hartmann pp 507ndash604 Allan Hancock Foundation LosAngeles Calif USA 1977
[3] D Martin and T Britayev ldquoSymbiotic polychaetes review ofknown speciesrdquo Oceanography Marine Biology vol 36 pp 217ndash340 1998
[4] T A Britayey and T I Antokhina ldquoSymbiotic polychaetesfrom Nhatrang Bay Vietnamrdquo in Benthic fauna of the Bay ofNhatrang Southern Vietnam T Britayev and D S Pavlov Edsvol 2 pp 11ndash54 KMK Moscow Russia 2012
[5] T A Britayev ldquoThe symbiotic polychaetes morphology ecol-ogy and distributionrdquo in Symbiosis among Marine Animals VA Sveshnikov Ed pp 60ndash74 1989
[6] I Linero Arana and O Dıaz Dıaz ldquoPolychaeta (Annelida)associatedwithThalassia testudinum in the northeastern coastalwaters of Venezuelardquo Revista de Biologıa Tropical vol 54 no 3pp 971ndash978 2006
[7] T A Britayev O A Bratova and P Y Dgebuadze ldquoSym-biotic assemblage associated with the tropical sea urchinSalmacis bicolor (Echinoidea Temnopleuridae) in the An Thoiarchipelago Vietnamrdquo Symbiosis vol 61 pp 155ndash161 2013
[8] S E Coppard and A C Campbell ldquoOrganisms associated withdiadematid echinoids in Fijirdquo in Echinoderms Munchen Tayloramp Francis London UK 2004
[9] F E Hayes ldquoDecapod crustaceans associating with the seaurchinDiadema antillarum in the Virgin IslandsrdquoNauplius vol15 pp 81ndash85 2007
[10] A V Raman and P N Ganapati ldquoPollution effects on ecobi-ology of benthic polychaetes in Visakhapatnam Harbour (Bayof Bengal)rdquo Marine Pollution Bulletin vol 14 no 2 pp 46ndash521983
[11] J E de Assis E D A S Bezerra R J de Brito A I Gondim andM L Christoffersen ldquoAn Association between Hesione picta(Polychaeta Hesionidae) and Ophionereis reticulata (Ophi-uroideaOphionereididae) from theBrazilianCoastrdquoZoologicalStudies vol 51 no 6 pp 762ndash767 2012
[12] R H Emson C M Young and G L J Paterson ldquoA fireworm with a sheltered life studies of Benthoscolex cubanusHartman (Amphinomidae) an internal associate of the bathyalsea- urchin Archeopneustes hystrix (A Agassiz 1880)rdquo Journalof Natural History vol 27 no 5 pp 1013ndash1028 1993
[13] DA Petch ldquoSelective deposit-feeding byLumbrineris cf latreilli(Polychaeta Lumbrineridae) with a new method for assessingselectivity by deposit-feeding organismsrdquo Marine Biology vol93 no 3 pp 443ndash448 1986
[14] A Ayyagari and K Ramesh Babu ldquoSeasonal variations ofphysicochemical parameters in coastal waters of Visakhapat-nam East coast of Indiardquo Middle East Journal of ScientificResearch vol 14 no 2 pp 161ndash167 2013
[15] M Jaganadha Rao J V Ramana and M C Rao ldquoMininginitiatives for placer deposits along the east coast of India apreliminary assessment of possible impact on coastal environ-mentrdquo in Ecobiology of Polluted Waters K Arvind Ed pp 44ndash51 Daya Publishing House New Delhi India 2006
[16] D Thistle ldquoNatural physical disturbances and communities ofmarine soft bottomsrdquoMarine Ecology Progress Series vol 6 pp223ndash228 1981
4 Journal of Marine Biology
[17] S K Sarkar A Bhattacharya S Giri et al ldquoSpatiotemporalvariation in benthic polychaetes (Annelida) and relationshipswith environmental variables in a tropical estuaryrdquo WetlandsEcology and Management vol 13 no 1 pp 55ndash67 2005
[18] A J Bruce ldquoThe shrimps associated with Indo-west pacificechinoderms with the description of a new species in the genusPericlimenes coasta 1844 (Crustacea Pontoniinae)rdquoMemoirs ofthe Australian Museum vol 16 pp 191ndash216 1982
[19] P Castro ldquoThe natantian shrimps (Crustacea Decapoda) asso-ciated with invertebrates in Hawaiirdquo Pacific Science vol 25 pp395ndash403 1971
[20] A Milne-Edwards ldquoDistribution and spawning site selectionof the polychaete Lumbrineris latreilli at Asamushi NorthernJapanrdquo Bull of Marine Biological Station of Asamushi vol 17 no1 pp 17ndash28 1981
counted The maxillary apparatus of each individual wasextracted after an anterodorsal incision and mounted on aslide to study the details of both maxillae and the mandiblesunder an optical microscope Parapodium was separatedfrom polychaete placed on a slide with a drop of glycerol andcoveredwith a cover slip and the chaetaewere observed underan Olympus compound microscope
3 Results
31 Description of Lumbrineris latreilli (Figure 2) Polychaetecolour is pale red or brown in live condition Body islong ranging from 60mm to 64mm (55ndash58 segments)gradually tapering towards the pygidium The prostomiumis blunt conical the length being slightly longer than widthand has no eyes and appendages Peristomium apodousconsists of two rings of equal size All the parapodia areuniramous Parapodium in the anterior segments has a shortrounded prechaetal lobe and digitiform postchaetal lobeAnterior parapodia have capillary chaetae and compoundmultidentate hooded hooks with long blades The rest ofthe parapodia have few capillary chaetae and simple hoodedhooks of similar sizes Jaw apparatus is well developed andis of the labidognatha type Maxillae II are almost as long asmaxillae I and are connected to them with a ligament Themaxilla II has four teeth maxilla III has two teeth andmaxillaIV is unidentate with pointed tooth Mandibles are compactand fused medially Aciculae are yellow in color and straight
0123456789
Prev
alen
ce (
)
Test diameter (mm)
y = 2156x minus 08
R2 = 0964
50ndash54 55ndash59 60ndash64 65ndash69
Figure 3 Relationship between the size of Stomopneustes variolarisand its infestation prevalence by Lumbrineris latreilli
32 Description of the Association Among 60 specimens ofS variolaris collected of diameter ranging from 30mm to76mm during the study period only 10 (1667) of thesea urchins were found to be associated with L latreilliEach sea urchin was found to be associated with only onepolychaete In this study it was observed that sea urchins ofdiameter in the range of 50mm to 70mm were found to beassociated with the polychaete L latreilli of average length604 plusmn 22mm The polychaete was found attached to theaboral side of the test of the sea urchin between the spinesIts presence could be noticed only when the sea urchin spineswere removedThe percentage of prevalence was more as testsize increases (119910 = 2156119909 minus 08 119877 = 0964 119875 = 002)(Figure 3)
4 Discussion
Many polychaetes including polynoids syllids and hesionidslive in either obligate or facultative association with echin-oderms [3] to derive protection from predators and foodfrom the host They often prefer the oral surface from wherethey may easily access to the food collected by the host whileothers prefer aboral surface feeding on the semi digested ordigested matter released by the host [11] Similar associationand feeding pattern was observed in another polychaeteHesione picta (Muller 1858) feeding on the undigestedmaterial released by the brittle star Ophionereis reticulata
Journal of Marine Biology 3
(Say 1825) Two of them like the amphinomid Benthoscolexcubanus (Hartman 1942) or the polynoid Gorekia crassicirris(Willey 1902) were even found inside the gut of irregular seaurchins [12]
In the present study Lumbrineris latreilli was foundattached to the test on the aboral side between the ambitusand the genital plates and accordingly the polychaete mayfeed on the undigested organic matter released by the seaurchin S variolaris
Thepresent association is between a softbottomburrowerL latreilli [13] and the rock boring sea urchin S vario-laris Both are intertidal dwellers living in different habitatsThe association of polychaete with sea urchin is due toits displacement from natural habitat during the upwelling[6 14] and dredging operations [15] Lumbrineris speciesare vulnerable to the direct effects of dredging and to thedeposition of sediments mobilized during dredging [16 17]
The principal benefit of the association however seemsto be protective as the host is shielding the polychaete frompossible predators by means of the spines Other marineorganisms reported to be associated with sea urchin areshrimps [18 19] crabs [9] and young of many fish speciesFurther the polychaete colour which is brown camouflageswith the colour of the test of the sea urchin precluding therecognition by the predators
Another plausible reasonmight be that these worms havestrong tendency to come from the soft bottom on to the algalzone for spawning as this behavior is beneficial for successfulfertilization and larval dispersal [20] During this time theymay seek shelter in sea urchins that also inhabit in this zone
5 Conclusion
Lumbrineris latreilli is a benthic dweller feeding on thesediment and its association with a rock boring sea urchinS variolaris is to tide over unfavorable circumstances likeupwelling and dredging This association protects the poly-chaete from the predators during displacement from itsnatural habitat
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Archana Ayyagari acknowledges the Department of Scienceand Technology Government of India for providing herwith the financial support The authors would like to thankDr R Rajasekaran and Dr T A Britayev for helping withthe polychaete identification The authors heartily thank allreviewers for the valuable suggestions on the paper
References
[1] M Wisshak and C Neumann ldquoA symbiotic association of aboring polychaete and an echinoid from the Late Cretaceous
of Germanyrdquo Acta Palaeontologica Polonica vol 51 no 3 pp589ndash597 2006
[2] G A Knox ldquoThe role of polychaetes in benthic soft-bottomcommunitiesrdquo in Essays on Polychaetous Annelids in Memory ofOlga Hartmann pp 507ndash604 Allan Hancock Foundation LosAngeles Calif USA 1977
[3] D Martin and T Britayev ldquoSymbiotic polychaetes review ofknown speciesrdquo Oceanography Marine Biology vol 36 pp 217ndash340 1998
[4] T A Britayey and T I Antokhina ldquoSymbiotic polychaetesfrom Nhatrang Bay Vietnamrdquo in Benthic fauna of the Bay ofNhatrang Southern Vietnam T Britayev and D S Pavlov Edsvol 2 pp 11ndash54 KMK Moscow Russia 2012
[5] T A Britayev ldquoThe symbiotic polychaetes morphology ecol-ogy and distributionrdquo in Symbiosis among Marine Animals VA Sveshnikov Ed pp 60ndash74 1989
[6] I Linero Arana and O Dıaz Dıaz ldquoPolychaeta (Annelida)associatedwithThalassia testudinum in the northeastern coastalwaters of Venezuelardquo Revista de Biologıa Tropical vol 54 no 3pp 971ndash978 2006
[7] T A Britayev O A Bratova and P Y Dgebuadze ldquoSym-biotic assemblage associated with the tropical sea urchinSalmacis bicolor (Echinoidea Temnopleuridae) in the An Thoiarchipelago Vietnamrdquo Symbiosis vol 61 pp 155ndash161 2013
[8] S E Coppard and A C Campbell ldquoOrganisms associated withdiadematid echinoids in Fijirdquo in Echinoderms Munchen Tayloramp Francis London UK 2004
[9] F E Hayes ldquoDecapod crustaceans associating with the seaurchinDiadema antillarum in the Virgin IslandsrdquoNauplius vol15 pp 81ndash85 2007
[10] A V Raman and P N Ganapati ldquoPollution effects on ecobi-ology of benthic polychaetes in Visakhapatnam Harbour (Bayof Bengal)rdquo Marine Pollution Bulletin vol 14 no 2 pp 46ndash521983
[11] J E de Assis E D A S Bezerra R J de Brito A I Gondim andM L Christoffersen ldquoAn Association between Hesione picta(Polychaeta Hesionidae) and Ophionereis reticulata (Ophi-uroideaOphionereididae) from theBrazilianCoastrdquoZoologicalStudies vol 51 no 6 pp 762ndash767 2012
[12] R H Emson C M Young and G L J Paterson ldquoA fireworm with a sheltered life studies of Benthoscolex cubanusHartman (Amphinomidae) an internal associate of the bathyalsea- urchin Archeopneustes hystrix (A Agassiz 1880)rdquo Journalof Natural History vol 27 no 5 pp 1013ndash1028 1993
[13] DA Petch ldquoSelective deposit-feeding byLumbrineris cf latreilli(Polychaeta Lumbrineridae) with a new method for assessingselectivity by deposit-feeding organismsrdquo Marine Biology vol93 no 3 pp 443ndash448 1986
[14] A Ayyagari and K Ramesh Babu ldquoSeasonal variations ofphysicochemical parameters in coastal waters of Visakhapat-nam East coast of Indiardquo Middle East Journal of ScientificResearch vol 14 no 2 pp 161ndash167 2013
[15] M Jaganadha Rao J V Ramana and M C Rao ldquoMininginitiatives for placer deposits along the east coast of India apreliminary assessment of possible impact on coastal environ-mentrdquo in Ecobiology of Polluted Waters K Arvind Ed pp 44ndash51 Daya Publishing House New Delhi India 2006
[16] D Thistle ldquoNatural physical disturbances and communities ofmarine soft bottomsrdquoMarine Ecology Progress Series vol 6 pp223ndash228 1981
4 Journal of Marine Biology
[17] S K Sarkar A Bhattacharya S Giri et al ldquoSpatiotemporalvariation in benthic polychaetes (Annelida) and relationshipswith environmental variables in a tropical estuaryrdquo WetlandsEcology and Management vol 13 no 1 pp 55ndash67 2005
[18] A J Bruce ldquoThe shrimps associated with Indo-west pacificechinoderms with the description of a new species in the genusPericlimenes coasta 1844 (Crustacea Pontoniinae)rdquoMemoirs ofthe Australian Museum vol 16 pp 191ndash216 1982
[19] P Castro ldquoThe natantian shrimps (Crustacea Decapoda) asso-ciated with invertebrates in Hawaiirdquo Pacific Science vol 25 pp395ndash403 1971
[20] A Milne-Edwards ldquoDistribution and spawning site selectionof the polychaete Lumbrineris latreilli at Asamushi NorthernJapanrdquo Bull of Marine Biological Station of Asamushi vol 17 no1 pp 17ndash28 1981
(Say 1825) Two of them like the amphinomid Benthoscolexcubanus (Hartman 1942) or the polynoid Gorekia crassicirris(Willey 1902) were even found inside the gut of irregular seaurchins [12]
In the present study Lumbrineris latreilli was foundattached to the test on the aboral side between the ambitusand the genital plates and accordingly the polychaete mayfeed on the undigested organic matter released by the seaurchin S variolaris
Thepresent association is between a softbottomburrowerL latreilli [13] and the rock boring sea urchin S vario-laris Both are intertidal dwellers living in different habitatsThe association of polychaete with sea urchin is due toits displacement from natural habitat during the upwelling[6 14] and dredging operations [15] Lumbrineris speciesare vulnerable to the direct effects of dredging and to thedeposition of sediments mobilized during dredging [16 17]
The principal benefit of the association however seemsto be protective as the host is shielding the polychaete frompossible predators by means of the spines Other marineorganisms reported to be associated with sea urchin areshrimps [18 19] crabs [9] and young of many fish speciesFurther the polychaete colour which is brown camouflageswith the colour of the test of the sea urchin precluding therecognition by the predators
Another plausible reasonmight be that these worms havestrong tendency to come from the soft bottom on to the algalzone for spawning as this behavior is beneficial for successfulfertilization and larval dispersal [20] During this time theymay seek shelter in sea urchins that also inhabit in this zone
5 Conclusion
Lumbrineris latreilli is a benthic dweller feeding on thesediment and its association with a rock boring sea urchinS variolaris is to tide over unfavorable circumstances likeupwelling and dredging This association protects the poly-chaete from the predators during displacement from itsnatural habitat
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Archana Ayyagari acknowledges the Department of Scienceand Technology Government of India for providing herwith the financial support The authors would like to thankDr R Rajasekaran and Dr T A Britayev for helping withthe polychaete identification The authors heartily thank allreviewers for the valuable suggestions on the paper
References
[1] M Wisshak and C Neumann ldquoA symbiotic association of aboring polychaete and an echinoid from the Late Cretaceous
of Germanyrdquo Acta Palaeontologica Polonica vol 51 no 3 pp589ndash597 2006
[2] G A Knox ldquoThe role of polychaetes in benthic soft-bottomcommunitiesrdquo in Essays on Polychaetous Annelids in Memory ofOlga Hartmann pp 507ndash604 Allan Hancock Foundation LosAngeles Calif USA 1977
[3] D Martin and T Britayev ldquoSymbiotic polychaetes review ofknown speciesrdquo Oceanography Marine Biology vol 36 pp 217ndash340 1998
[4] T A Britayey and T I Antokhina ldquoSymbiotic polychaetesfrom Nhatrang Bay Vietnamrdquo in Benthic fauna of the Bay ofNhatrang Southern Vietnam T Britayev and D S Pavlov Edsvol 2 pp 11ndash54 KMK Moscow Russia 2012
[5] T A Britayev ldquoThe symbiotic polychaetes morphology ecol-ogy and distributionrdquo in Symbiosis among Marine Animals VA Sveshnikov Ed pp 60ndash74 1989
[6] I Linero Arana and O Dıaz Dıaz ldquoPolychaeta (Annelida)associatedwithThalassia testudinum in the northeastern coastalwaters of Venezuelardquo Revista de Biologıa Tropical vol 54 no 3pp 971ndash978 2006
[7] T A Britayev O A Bratova and P Y Dgebuadze ldquoSym-biotic assemblage associated with the tropical sea urchinSalmacis bicolor (Echinoidea Temnopleuridae) in the An Thoiarchipelago Vietnamrdquo Symbiosis vol 61 pp 155ndash161 2013
[8] S E Coppard and A C Campbell ldquoOrganisms associated withdiadematid echinoids in Fijirdquo in Echinoderms Munchen Tayloramp Francis London UK 2004
[9] F E Hayes ldquoDecapod crustaceans associating with the seaurchinDiadema antillarum in the Virgin IslandsrdquoNauplius vol15 pp 81ndash85 2007
[10] A V Raman and P N Ganapati ldquoPollution effects on ecobi-ology of benthic polychaetes in Visakhapatnam Harbour (Bayof Bengal)rdquo Marine Pollution Bulletin vol 14 no 2 pp 46ndash521983
[11] J E de Assis E D A S Bezerra R J de Brito A I Gondim andM L Christoffersen ldquoAn Association between Hesione picta(Polychaeta Hesionidae) and Ophionereis reticulata (Ophi-uroideaOphionereididae) from theBrazilianCoastrdquoZoologicalStudies vol 51 no 6 pp 762ndash767 2012
[12] R H Emson C M Young and G L J Paterson ldquoA fireworm with a sheltered life studies of Benthoscolex cubanusHartman (Amphinomidae) an internal associate of the bathyalsea- urchin Archeopneustes hystrix (A Agassiz 1880)rdquo Journalof Natural History vol 27 no 5 pp 1013ndash1028 1993
[13] DA Petch ldquoSelective deposit-feeding byLumbrineris cf latreilli(Polychaeta Lumbrineridae) with a new method for assessingselectivity by deposit-feeding organismsrdquo Marine Biology vol93 no 3 pp 443ndash448 1986
[14] A Ayyagari and K Ramesh Babu ldquoSeasonal variations ofphysicochemical parameters in coastal waters of Visakhapat-nam East coast of Indiardquo Middle East Journal of ScientificResearch vol 14 no 2 pp 161ndash167 2013
[15] M Jaganadha Rao J V Ramana and M C Rao ldquoMininginitiatives for placer deposits along the east coast of India apreliminary assessment of possible impact on coastal environ-mentrdquo in Ecobiology of Polluted Waters K Arvind Ed pp 44ndash51 Daya Publishing House New Delhi India 2006
[16] D Thistle ldquoNatural physical disturbances and communities ofmarine soft bottomsrdquoMarine Ecology Progress Series vol 6 pp223ndash228 1981
4 Journal of Marine Biology
[17] S K Sarkar A Bhattacharya S Giri et al ldquoSpatiotemporalvariation in benthic polychaetes (Annelida) and relationshipswith environmental variables in a tropical estuaryrdquo WetlandsEcology and Management vol 13 no 1 pp 55ndash67 2005
[18] A J Bruce ldquoThe shrimps associated with Indo-west pacificechinoderms with the description of a new species in the genusPericlimenes coasta 1844 (Crustacea Pontoniinae)rdquoMemoirs ofthe Australian Museum vol 16 pp 191ndash216 1982
[19] P Castro ldquoThe natantian shrimps (Crustacea Decapoda) asso-ciated with invertebrates in Hawaiirdquo Pacific Science vol 25 pp395ndash403 1971
[20] A Milne-Edwards ldquoDistribution and spawning site selectionof the polychaete Lumbrineris latreilli at Asamushi NorthernJapanrdquo Bull of Marine Biological Station of Asamushi vol 17 no1 pp 17ndash28 1981
[17] S K Sarkar A Bhattacharya S Giri et al ldquoSpatiotemporalvariation in benthic polychaetes (Annelida) and relationshipswith environmental variables in a tropical estuaryrdquo WetlandsEcology and Management vol 13 no 1 pp 55ndash67 2005
[18] A J Bruce ldquoThe shrimps associated with Indo-west pacificechinoderms with the description of a new species in the genusPericlimenes coasta 1844 (Crustacea Pontoniinae)rdquoMemoirs ofthe Australian Museum vol 16 pp 191ndash216 1982
[19] P Castro ldquoThe natantian shrimps (Crustacea Decapoda) asso-ciated with invertebrates in Hawaiirdquo Pacific Science vol 25 pp395ndash403 1971
[20] A Milne-Edwards ldquoDistribution and spawning site selectionof the polychaete Lumbrineris latreilli at Asamushi NorthernJapanrdquo Bull of Marine Biological Station of Asamushi vol 17 no1 pp 17ndash28 1981
