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Larval nutritional mode and swimming behaviour in ciliated marine larvae

Published online by Cambridge University Press:  27 December 2018

E. M. Montgomery ,
J.-F. Hamel  and
A. Mercier
E. M. Montgomery*
Affiliation:
Department of Ocean Sciences, Memorial University, St. John's, Newfoundland and Labrador, A1C 5S7, Canada
J.-F. Hamel
Affiliation:
Society for Exploration and Valuing of the Environment (SEVE), Portugal Cove–St. Philips, Newfoundland and Labrador, A1M 2B7, Canada
A. Mercier
Affiliation:
Department of Ocean Sciences, Memorial University, St. John's, Newfoundland and Labrador, A1C 5S7, Canada
*
Author for correspondence: E. M. Montgomery, E-mail: e.montgomery@mun.ca
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Abstract

Swimming propagules (embryos and larvae) are a critical component of the life histories of benthic marine animals. Larvae that feed (planktotrophic) have been assumed to swim faster, disperse farther and have more complex behavioural patterns than non-feeding (lecithotrophic) larvae. However, a number of recent studies challenge these early assumptions, suggesting a need to revisit them more formally. The current review presents a quantitative analysis of swimming speed and body size in planktotrophic and lecithotrophic propagules across five major marine phyla (Porifera, Cnidaria, Annelida, Mollusca and Echinodermata). Results of the comparative study showed that swimming speed differences among ciliated propagules can be driven by taxonomy, adult mobility (motile vs sessile) and/or larval nutritional mode. On a phylogenetic level, distinct patterns emerge across phyla and life stages, whereby planktotrophic propagules swim faster in some of them, and lecithotrophic propagules swim faster in others. Interestingly, adults with sessile and sedentary lifestyles produce propagules that swam faster than the propagules produced by motile adults. Understanding similarities and differences among marine propagules associated with different reproductive strategies and adult lifestyles are significant from ecological, evolutionary and applied perspectives. Patterns of swimming can directly impact the dispersal/recruitment potential with incidence on the design of larval rearing methods and marine protected areas.

Keywords

Ciliated larvaelarval sizelecithotrophylocomotionphylogeny
Type
Review
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 5 , August 2019 , pp. 1027 - 1032
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

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References

Butman, CA, Grassle, JP and Buskey, EJ (1988) Horizontal swimming and gravitational sinking of Capitella sp. I (Annelida: Polychaeta) larvae: implications for settlement. Ophelia 29, 43–57.Google Scholar
Carrier, T, Heyland, A and Reitzel, A (2017) Evolutionary Ecology of Marine Invertebrate Larvae. Oxford: Oxford University Press.Google Scholar
Chia, F-S, Buckland, J and Young, CM (1984) Locomotion of marine invertebrate larvae – a review. Canadian Journal of Zoology 62, 1205–1222.Google Scholar
Costello, MJ, Claus, S, Dekeyzer, S, Vandepitte, L, Tuama, ÉÓ, Lear, D and Tyler-Walters, H (2015) Biological and ecological traits of marine species. PeerJ 3, e1201.Google Scholar
Emlet, RB (1991) Functional constraints on the evolution of larval forms of marine invertebrates: experimental and comparative evidence. American Zoologist 31, 707–725.Google Scholar
Emlet, RB (1994) Body form and patterns of ciliation in nonfeeding larvae of echinoderms – functional solutions to swimming in the plankton. American Zoologist 34, 570–585.Google Scholar
Emlet, RB and Hoegh-Guldberg, O (1997) Effects of egg size on postlarval performance: experimental evidence from a sea urchin. Evolution 51, 141–152.Google Scholar
Ereskovsky, AV (2010) The Comparative Embryology of Sponges. New York, NY: Springer Science & Business Media.Google Scholar
Grünbaum, D and Strathmann, RR (2003) Form, performance, and trade-offs in swimming and stability of armed larvae. Journal of Marine Research 61, 659–691.Google Scholar
Harii, S, Kayanne, H, Takigawa, H, Hayashibara, T and Yamamoto, M (2002) Larval survivorship, competency periods and settlement of two brooding corals, Heliopora coerulea and Pocillopora damicornis. Marine Biology 141, 39–46.Google Scholar
Hayward, PJ (1985) Ctenostome bryozoans: keys and notes for the identification of the species. In Kermack, D and Barnes, R (eds), Synopses of the British Fauna, vol. 33. London: Brill Archive, p. 147.Google Scholar
Koehl, M and Reidenbach, MA (2007) Swimming by microscopic organisms in ambient water flow. Experiments in Fluids 43, 755–768.Google Scholar
Krug, PJ and Zimmer, RK (2000) Developmental dimorphism and expression of chemosensory-mediated behavior: habitat selection by a specialist marine herbivore. Journal of Experimental Biology 203, 1741–1754.Google Scholar
Krug, PJ and Zimmer, RK (2004) Developmental dimorphism: consequences for larval behavior and dispersal potential in a marine gastropod. Biological Bulletin 207, 233–246.Google Scholar
Leys, SP, Cronin, TW, Degnan, BM and Marshall, JN (2002) Spectral sensitivity in a sponge larva. Journal of Comparative Physiology A 188, 199–202.Google Scholar
Maldonado, M (2006) The ecology of the sponge larva. Canadian Journal of Zoology 84, 175–194.Google Scholar
Meidel, SK, Scheibling, RE and Metaxas, A (1999) Relative importance of parental and larval nutrition on larval development and metamorphosis of the sea urchin Strongylocentrotus droebachiensis. Journal of Experimental Marine Biology and Ecology 240, 161–178.Google Scholar
Mercier, A and Hamel, J-F (2008) Depth-related shift in life history strategies of a brooding and broadcasting deep-sea asteroid. Marine Biology 156, 205–223.Google Scholar
Mercier, A, Sewell, MA and Hamel, J-F (2013) Pelagic propagule duration and developmental mode: reassessment of a fading link. Global Ecology and Biogeography 22, 517–530.Google Scholar
Mileikovsky, SA (1973) Speed of active movement of pelagic larvae of marine bottom invertebrates and their ability to regulate their vertical position. Marine Biology 23, 11–17.Google Scholar
Montgomery, EM, Hamel, J-F and Mercier, A (2017) Ontogenetic shifts in swimming capacity of echinoderm propagules: a comparison of species with planktotrophic and lecithotrophic larvae. Marine Biology 164, 43.Google Scholar
Montgomery, EM, Hamel, J-F and Mercier, A (2018) Ontogenetic variation in photosensitivity of developing echinoderm propagules. Journal of Experimental Marine Biology and Ecology 500, 63–72.Google Scholar
Mundy, CN and Babcock, RC (1998) Role of light intensity and spectral quality in coral settlement: implication for depth-dependent settlement? Journal of Experimental Marine Biology and Ecology 223, 235–255.Google Scholar
Podolsky, RD and Emlet, RB (1993) Separating the effects of temperature and viscosity on swimming and water movement by sand dollar larvae (Dendraster excentricus). Journal of Experimental Biology 176, 207–222.Google Scholar
Poulin, É, Boletzky, S and Féral, J-P (2001) Combined ecological factors permit classification of developmental patterns in benthic marine invertebrates: a discussion note. Journal of Experimental Marine Biology and Ecology 257, 109–115.Google Scholar
Raimondi, PT and Morse, AN (2000) The consequences of complex larval behavior in a coral. Ecology 81, 3193–3211.Google Scholar
Schwarz, JA, Weis, VM and Potts, DC (2002) Feeding behavior and acquisition of zooxanthellae by planula larvae of the sea anemone Anthopleura elegantissima. Marine Biology 140, 471–478.Google Scholar
Strathmann, RR (1971) The feeding behaviour of planktotrophic echinoderm larvae: mechanisms, regulation, and rates of suspension feeding. Journal of Experimental Marine Biology and Ecology 6, 109–160.Google Scholar
Strathmann, RR and Grünbaum, D (2006) Good eaters, poor swimmers: compromises in larval form. Integrative and Comparative Biology 46, 312–322.Google Scholar
Wendt, DE (2000) Energetics of larval swimming and metamorphosis in four species of Bugula (Bryozoa). Biological Bulletin 198, 346–356.Google Scholar
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