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Sponge larvae are not that fast, but still the fastest

Reply to: ‘Sponge larvae do not swim that fast’

Published online by Cambridge University Press:  07 January 2020

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. Phillips, 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

Type
Letter to the Editor
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

We would like to thank Lanna & Riesgo (Reference Lanna and Riesgo2019) for their commentary on our recent publication on larval nutritional mode and swimming behaviour in ciliated marine larvae. They raised interesting points regarding the specificities of sponge larval behaviour, and we appreciated their addition of new records to the dataset. However, we wish to reiterate that the main objective of our original paper (Montgomery et al., Reference Montgomery, Hamel and Mercier2019) was to highlight general patterns of larval swimming capacity among a broad suite of taxa exhibiting different nutritional modes and adult motility levels. Some simplifications and generalizations were required to identify these broad patterns. For instance, rather than studying whether the larvae of different species swam on a continuous basis or not, we focused on their swimming capacity, i.e. maximum achievable speeds. We agree that specific larval behaviours (including but not limited to intermittent vs steady swimming) are pertinent to dispersal studies, not only for sponges but for all taxa (Robins et al., Reference Robins, Neill, Giménez, Jenkins and Malham2013; Nanninga & Berumen, Reference Nanninga and Berumen2014). Our own body of work has been adding to this line of inquiry, including ontogenetic behavioural shifts (Montgomery et al., Reference Montgomery, Hamel and Mercier2017, Reference Montgomery, Hamel and Mercier2018), predation rates on propagules (Mercier et al., Reference Mercier, Doncaster and Hamel2013) and settlement preferences of competent larvae (Mercier et al., Reference Mercier, Battaglene and Hamel2000; Mercier & Hamel, Reference Mercier and Hamel2009; Sun et al., Reference Sun, Hamel and Mercier2010). However, the analyses in Montgomery et al. (Reference Montgomery, Hamel and Mercier2019) were centred on the mechanistic aspects of swimming in ciliated larvae and aimed to dispel long-standing assumptions about capacities in planktotrophs vs lecithotrophs (which was made clear in the title).

We have taken this opportunity to re-examine the original dataset in light of the conversion errors identified by Lanna & Riesgo (Reference Lanna and Riesgo2019), in addition to recalculating the relevant statistics using the new records they provided (Table 1). A total of six conversion errors were identified and corrected (out of the 161 records), two duplicate records were removed, and references were also updated in the supplementary file (S1). The main findings of our original paper remain unchanged with these corrections and adjusted statistics (Figures 1–4). Overall, lecithotrophic propagules swim faster than planktotrophic propagules (ANOVA P = 0.003); two clusters are identified from the hierarchical cluster analyses (FAMD, HCPC P < 0.001); species with sessile or sedentary adults have larvae that swim faster than larvae from motile adults (ANOVA, P < 0.001); and lecithotrophic larvae demonstrate a greater capacity for faster swimming speeds at a given size than planktotrophic larvae (ANCOVA P < 0.001). Moreover, Porifera larvae still display the fastest mean swimming speed (5.78 mm s−1; Figure 1), although they are now statistically in a similar range as Bryozoa (3.30 mm s−1) and Cnidaria (3.05 mm s−1) and significantly faster than Annelida, Mollusca and Echinodermata larvae based on the adjusted values (Table 1, Tukey HSD P = 0.8 (Bryozoa), 0.2 (Cnidaria) and <0.01 (all others)).

Fig. 1. Mean propagule swimming speed (mm s−1 ± SE) varies among phyla and larval nutritional modes. Phylum Cnidaria and Porifera only have one bar as these taxa only have one larval nutritional mode. Error bars are present where more than one record per phylum and category were available. See Table S1 for raw data.

Fig. 2. Mean propagule swimming speed (mm s−1 ± SE) of specific life stages varies with nutritional mode. Taxa and life stages presented here had both planktotrophic and lecithotrophic representatives in the dataset. Error bars are present where more than one record per phylum and category were available. See Table S1 for raw data.

Fig. 3. Mean propagule swimming speed (mm s−1 ± SE) varies with taxa and level of adult mobility. Sessile adults are incapable of movement, sedentary adults have the capacity to move but do so rarely and motile adults move readily and often. Error bars are present where more than one record per category were available. See Table S1 for raw data.

Fig. 4. Larval swimming speed (mm s−1) vs propagule body size (μm) in lecithotrophic and planktotrophic larvae of various phyla (Porifera, Cnidaria, Mollusca, Annelida, Echinodermata, Bryozoa) on log10 scales. Log scales were used to examine scaling relationships across a wide range of propagule sizes and speeds. Points represent mean values for individual species. Symbols depicting the various phyla are either solid/open to indicate the lecithotrophic/planktotrophic larval feeding mode (except for Porifera, which is fully lecithotrophic and identified with +). N = 125 total records. The solid lines show regression results. Planktotrophs: y = −0.33x + 0.54, R 2 = 0.04; Lecithotrophs: y = − 0.03x + 0.31, R 2 = <0.01.

Table 1. Updated mean length and swimming speed summarized across the two larval nutritional modes and six phyla featured in the dataset (Supplementary material S1)

Supplementary material

The supplementary material for this article can be found at https://doi.org/10.1017/S0025315419001139.

References

Lanna, E and Riesgo, A (2019) Sponge larvae do not swim that fast. Journal of the Marine Biology Association of the United KingdomGoogle Scholar
Mercier, A and Hamel, J-F (2009) Reproductive periodicity and host-specific settlement and growth of a deep-water symbiotic sea anemone. Canadian Journal of Zoology 87, 967980.CrossRefGoogle Scholar
Mercier, A, Battaglene, SC and Hamel, J-F (2000) Settlement preferences and early migration of the tropical sea cucumber Holothuria scabra. Journal of Experimental Marine Biology and Ecology 249, 89110.CrossRefGoogle ScholarPubMed
Mercier, A, Doncaster, EJ and Hamel, J-F (2013) Contrasting predation rates on planktotrophic and lecithotrophic propagules by marine benthic invertebrates. Journal of Experimental Marine Biology and Ecology 449, 100110.CrossRefGoogle 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.CrossRefGoogle 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, 6372.CrossRefGoogle Scholar
Montgomery, EM, Hamel, J-F and Mercier, A (2019) Larval nutritional mode and swimming behaviour in ciliated marine larvae. Journal of the Marine Biological Association of the United Kingdom 99, 10271032.CrossRefGoogle Scholar
Nanninga, GB and Berumen, ML (2014) The role of individual variation in marine larval dispersal. Frontiers in Marine Science 1, 71.CrossRefGoogle Scholar
Robins, PE, Neill, SP, Giménez, L, Jenkins, SR and Malham, SK (2013) Physical and biological controls on larval dispersal and connectivity in a highly energetic shelf sea. Limnology and Oceanography 58, 505524.CrossRefGoogle Scholar
Sun, Z, Hamel, J-F and Mercier, A (2010) Planulation periodicity, settlement preferences and growth of two deep-sea octocorals from the northwest Atlantic. Marine Ecology Progress Series 410, 7187.CrossRefGoogle Scholar
Figure 0

Fig. 1. Mean propagule swimming speed (mm s−1 ± SE) varies among phyla and larval nutritional modes. Phylum Cnidaria and Porifera only have one bar as these taxa only have one larval nutritional mode. Error bars are present where more than one record per phylum and category were available. See Table S1 for raw data.

Figure 1

Fig. 2. Mean propagule swimming speed (mm s−1 ± SE) of specific life stages varies with nutritional mode. Taxa and life stages presented here had both planktotrophic and lecithotrophic representatives in the dataset. Error bars are present where more than one record per phylum and category were available. See Table S1 for raw data.

Figure 2

Fig. 3. Mean propagule swimming speed (mm s−1 ± SE) varies with taxa and level of adult mobility. Sessile adults are incapable of movement, sedentary adults have the capacity to move but do so rarely and motile adults move readily and often. Error bars are present where more than one record per category were available. See Table S1 for raw data.

Figure 3

Fig. 4. Larval swimming speed (mm s−1) vs propagule body size (μm) in lecithotrophic and planktotrophic larvae of various phyla (Porifera, Cnidaria, Mollusca, Annelida, Echinodermata, Bryozoa) on log10 scales. Log scales were used to examine scaling relationships across a wide range of propagule sizes and speeds. Points represent mean values for individual species. Symbols depicting the various phyla are either solid/open to indicate the lecithotrophic/planktotrophic larval feeding mode (except for Porifera, which is fully lecithotrophic and identified with +). N = 125 total records. The solid lines show regression results. Planktotrophs: y = −0.33x + 0.54, R2 = 0.04; Lecithotrophs: y = − 0.03x + 0.31, R2 = <0.01.

Figure 4

Table 1. Updated mean length and swimming speed summarized across the two larval nutritional modes and six phyla featured in the dataset (Supplementary material S1)

Supplementary material: File

Montgomery et al. supplementary material

Table S1

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