Abstract
Like many other benthic infaunal invertebrates, spionid polychaetes often lose portions of their bodies to predators, which affects their activities. Feeding palp loss and tail loss have been studied in several spionids, but the capacity for anterior tissue regeneration has not been compared in different species. The present study examines anterior tissue regeneration in two species, Dipolydora quadrilobata (Jacobi 1883) and Pygospio elegans Claparède 1863, in two laboratory experiments. Tissue removal treatments included removal of palps only, removal of anterior tissue through the first setiger, anterior tissue through the fifth setiger, all anterior tissue through half of the gill-bearing setigers, and all anterior tissue through the last gill-bearing setiger. Regeneration was monitored by capturing images of the worms and digitizing the area of regenerated anterior tissue or counting the number of segments that grew over time. Worms of both species regenerated anterior tissue regardless of the amount removed. Morphogenesis during regeneration followed a similar pattern in these two species regardless of the amount of anterior tissue lost, progressing from wound healing to formation of a recognizable prostomium and peristomium (“head”) by 6 days post-ablation. Palp and setal growth, addition of segments, and formation of nuchal organs and the ciliated food groove followed so that worms appeared to have re-grown “normal,” but smaller, “heads” and palps by 9–12 days following ablation. Over the course of 16 days, worms that lost more segments regenerated less tissue relative to their initial intact size and did so more slowly. There was no significant palp growth during the first 3 days following ablation. Rate of segment addition was directly related to the degree of tissue loss in D. quadrilobata. P. elegans added segments at similar rates whether 50 or 70% of the original segments was removed.




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Abeloos M (1950) Regeneration et region cephalique chez l’annelide P. ciliata. C R Soc Biol 144:1527–1528
Aller RC (1982) The effects of macrobenthos on chemical properties of marine sediment and overlying water. In: McCall PL, Tevesz MJS (eds) Animal-sediment relations. Plenum, New York, pp 53–102
Ansell AD, Harvey R, Gunther CP (1999) Recovery from siphon damage in Donax vittatus (da Costa) (Bivalvia: Donacidae). J Mollus Stud 65:223–232
Berrill NJ (1952) Regeneration and budding in worms. Bio Rev Camb Philos Soc 27:401–438
Blake JA, Arnofsky PL (1999) Reproduction and larval development of the spioniform Polychaeta with application to systematics and phylogeny. Hydrobiologia 402:57–106
Bolam SG, Fernandes TF (2003) Dense aggregations of Pygospio elegans (Claparède): effect on macrofaunal community structure and sediments. J Sea Res 49:171–185
Bowmer R, Keegan BF (1983) Field survey of the occurrence and significance of regeneration in Amphiura filiformis (Echniodermata: Ophiuroidea) from Galway Bay, west coast of Ireland. Mar Biol 74:65–71
Clavier J (1984) Production due to regeneration by Euclymene oerstedi (Claparède) (Polychaeta: Maldanidae) in the maritime basin of the Rance (Northern Britanny). J Exp Mar Biol Ecol 75:97–106
Clements LAJ (1985) Post-autotomy feeding behavior of Micropholis gracillima (Stimpson): Implications for regeneration. In: Proceedings of the international echinoderm conference, Galway, Ireland, vol 5, pp 609–615
Coen LD, Heck KLJ (1991) The interaction effects of siphon nipping and habitat on bivalve (Mercenaria mercenaria [L.]) growth in a subtropical segrass (Halodule wrightii Aschers) meadow. J Exp Mar Biol Ecol 145:1–13
Cummings VJ, Pridmore RD, Thrush SF, Hewitt JE (1996) Effect of the spionid polychaete Boccardia syrtis on the distribution and survival of juvenile Macomona liliana (Bivalvia: Tellinacea). Mar Biol 126:91–98
Dauer DM, Maybury CA, Ewing RM (1981) Feeding behavior and general ecology of several spionid polychaetes from the Chesapeake Bay. J Exp Mar Biol Ecol 54:21–38
De Vlas J (1979a) Annual food intake by plaice and flounder in a tidal flat area in the Dutch Wadden Sea, with special reference to consumption of regenerating parts of macrobenthic prey. Neth J Sea Res 13:117–153
De Vlas J (1979b) Secondary production by tail regeneration in a tidal flat population of lugworms (Arenicola marina), cropped by flatfish. Neth J Sea Res 13:362–393
De Vlas J (1985) Secondary production by siphon regeneration in a tidal flat population of Macoma balthica. Neth J Sea Res 19:147–164
Edwards R, Steele JH (1968) The ecology of 0-group plaice and common dabs at Loch Ewe. I. Population and food. J Exp Mar Biol Ecol 2:215–238
Fauchald K (1977) The polychaetes worms. Definitions and keys to the orders, families and genera. Nat Hist Mus Los Angeles Cty Sci Ser 28:1–190
Gibson GD, Harvey JM (2000) Morphogenesis during asexual reproduction in Pygospio elegans Claparède (Annelida, Polychaeta). Biol Bull 199:41–49
Harvell D (1984) Why nudibranchs are partial preadators: intracolonial variation in bryozoan palatability. Ecology 65:716–724
Harvell D, Suchanek TH (1987) Partial predation on tropical gorgonians by Cyphoma gibbosum (Gastropoda). Mar Ecol Prog Ser 38:37–44
Hentschel BT, Harper NS (2006) Effects of simulated sublethal predation on the growth and regeneration rates of a spionid polychaete in laboratory flumes. Mar Biol 149:1175–1183. DOI 10.1007/S00227-006-0274-8
Hyman LH (1940) Aspects of regeneration in annelids. Am Nat 74:513–527
Jumars PA, Self RLF, Nowell ARM (1982) Mechanisms of particle selection by tentaculate deposit-feeders. J Exp Mar Biol Ecol 64:47–70
Kamermans P, Huitema HJ (1994) Shrimp (Crangon crangon L.) browsing upon siphon tips inhibits feeding and growth in the bivalve Macoma balthica (L.). J Exp Mar Biol Ecol 175:59–75
Kihslinger RL, Woodin SA (2000) Food patches and a surface deposit feeding spionid polychaete. Mar Ecol Prog Ser 201:233–239
Lindsay SM, Woodin SA (1992) The effect of palp loss on feeding behavior of two spionid polychaetes: changes in exposure. Biol Bull 183:440–447
Lindsay SM, Woodin SA (1995) Tissue loss induces switching of feeding mode in spionid polychaetes. Mar Ecol Prog Ser 125:159–169
Lindsay SM, Woodin SA (1996) Quantifying sediment disturbance by browsed spionid polychaetes: implications for competitive and adult-larval interactions. J Exp Mar Biol Ecol 196:97–112
Lindsay SM, Jackson JL, He SQ, Forest DL (2004) Losing heads and making connections: anterior regeneration in spionid polychaetes. Integr Comp Biol 44:593 (abstract)
Luckenbach MW (1987) Effects of adult infauna on new recruits: implications for the role of biogenic refuges. J Exp Mar Biol Ecol 105:197–206
Luckenbach MW, Huggett DV, Zobrist EC (1988) Sediment transport, biotic modifications, and selection of grain size in a surface deposit-feeder. Estuaries 11:134–139
Mikkelsen PS, Virnstein RW (1982) An illustrated glossary of polychaetes terms. Harb Branch Found Tech Rep 46:1–92
Peterson CH, Quammen ML (1982) Siphon nipping: its importance to small fishes and its impact on growth of the bivalve Protothaca staminea (Conrad). J Exp Mar Biol Ecol 63:249–268
Peterson CH, Skilleter GA (1994) Control of foraging behavior of individuals within an ecosystem context: the clam, Macoma balthica, flow environment, and siphon-cropping fishes. Oecologia 100:256–267
Pleijel F (1983) On feeding of Pholoe minuta (Fabricius, 1780) (Polychaeta: Sigalonidae). Sarsia 68:21–23
Sayles LP (1932) External features of regeneration in Clymenella torquata. J Exp Zool 62:237–258
Stancyk SE, Golde HM, Pape-Lindstrom PA, Dobson WE (1994) Born to lose. I. Measures of tissue loss and regeneration by the brittlestar Microphiopholis gracillima Echinodermata: Ophiuroidea). Mar Biol 118:451–462
Stehlik LL, Meise CJ (2000) Diet of winter flounder in a New Jersey estuary: ontogenetic change and spatial variation. Estuaries 23:381–391
Stock M (1965) Anterior regeneration in Spionidae. MS thesis, University of Connecticut, Storrs, CT
Taghon GL, Nowell ARM, Jumars PA (1980) Induction of suspension feeding in spionid polychaetes by high particulate fluxes. Science 210:562–564
Tamaki A (1985) Inhibition of larval recruitment of Armandia sp. (Polychaete: Opheliidae) by established adults of Pseudopolydora paucibranchiata (Okuda) (Polychaeta: Spionidae) on an intertidal sand flat. J Exp Mar Biol Ecol 87:67–82
Theil M, Watling L (1998) Effects of green algal mats on infaunal colonization of a New England mud flat—long-lasting but highly localized effects. Hydrobiologia 375–376:177–189
Thrush SF, Whitlach RB, Pridmore RD, Hewitt JE, Cummings VJ, Wilkinson MR (1996) Scale-dependent recolonization: the role of sediment stability in a dynamic sandflat habitat. Ecology 77:2472–2487
Virnstein RW (1977) The importance of predation by crabs and fishes on benthic infauna in Chesapeake Bay. Ecology 58:1199–1217
Wilson WH Jr (1984) An experimental analysis of spatial competition in a dense infaunal communtiy: the importance of relative effects. Est Coast Shelf Sci 18:673–684
Woodin SA (1982) Browsing: important in marine sedimentary environments? spionid polychaete examples. J Exp Mar Biol Ecol 60:35–45
Woodin SA (1984) Effects of browsing predators: activity changes in infauna following tissue loss. Biol Bull 166:558–573
Zajac RN (1985) The effects of sublethal predation on reproduction in the spionid polychaete Polydora ligni Webster. J Exp Mar Biol Ecol 88:1–19
Zajac RN (1995) Sublethal predation on Polydora cornuta (Polychaeta: Spionidae): patterns of tissue loss in a field population, predator functional response and potential demographic inputs. Mar Biol 123:531–541
Acknowledgments
Portions of this work were submitted by JLJ to fulfill the requirements of an Honors Thesis in the School of Marine Sciences at the University of Maine. We thank Dr. Kevin Eckelbarger and the staff of the Darling Marine Center for facilitating our work there. Dr. Jill Fegley provided helpful statistical advice. Toni Lombardi capably assisted with image analysis. Comments by Marlene Tsie and two anonymous reviewers improved the manuscript. JLJ and SQH were supported in part by the Maine Research Internships for Teachers and Students (MERITS) program. Financial support was provided by NSF grant OCE-0221229 to SML.
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Communicated by J.P. Grassle, New Brunswick
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Lindsay, S.M., Jackson, J.L. & He, S.Q. Anterior regeneration in the spionid polychaetes Dipolydora quadrilobata and Pygospio elegans . Mar Biol 150, 1161–1172 (2007). https://doi.org/10.1007/s00227-006-0431-0
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DOI: https://doi.org/10.1007/s00227-006-0431-0


