Larval nutritional mode and swimming behaviour in ciliated marine larvae

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.

Larval nutritional mode and swimming behaviour in ciliated marine larvae – CORRIGENDUM

“…The authors acknowledge that their article (Montgomery et al ., 2019) contained six conversion errors (out of the 161 records); two duplicate records were removed, and references were also updated in the supplementary file (S1).…”

Sponge larvae are not that fast, but still the fastest

“…Our own body of work has been adding to this line of inquiry, including ontogenetic behavioural shifts (Montgomery et al, 2017(Montgomery et al, , 2018, predation rates on propagules (Mercier et al, 2013) and settlement preferences of competent larvae (Mercier et al, 2000;Mercier & Hamel, 2009;Sun et al, 2010). However, the analyses in Montgomery et al (2019) were centred on the mechanistic aspects of swimming in ciliated larvae and aimed to dispel longstanding assumptions about capacities in planktotrophs vs lecithotrophs (which was made clear in the title).…”

Sponge larvae do not swim that fast: a reply to Montgomery et al. (2019)

“…Due to their reduced size, the sponge larva depends entirely on its ciliary movements to swim and at the same time when the cilia stop, the larva is stuck in the water (Maldonado, 2006). Although Montgomery et al (2019) state that the shape of the larvae of Porifera is mostly 'spheroid' (generating less 'drag') and that sponge larvae lack mineralized parts, the truth is that the majority of sponge larvae are bullet-shaped and, especially in Demospongiae, many have spicules made of silica. Therefore, the main characteristics used by Montgomery et al (2019) to explain this unexpected result do not seem to be actual and widespread characteristics of Porifera larvae.…”

“…As models to predict the dispersal of marine larvae usually consider the propagule speed, hydrographic conditions and planktonic duration, it is necessary to have in mind the different types of behaviour (Mariani et al, 2005). The absence of such a concern in their study compromises the results and the discussion of Montgomery et al (2019) and we fear that their conclusions might be propagated without proper discussion. The objective of meta-analysis studies is always to provoke discussions and to point further research topics aiming to refine the knowledge in a given field.…”

“…Montgomery et al . (2019) demonstrated through a meta-analysis that the current idea that planktotrophic larvae of marine invertebrates swim faster than their non-feeding counterparts should be challenged. They demonstrated using quantitative analysis that the ciliated lecithotrophic larvae of sessile organisms (especially sponges) swim faster than those of non-sessile animals (polychaetes and echinoderms).…”