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Increased Population Density Depresses Activity but Does Not Influence Dispersal in the Snail Pomatias 2 Elegans

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Increased Population Density Depresses Activity but Does Not Influence Dispersal in the Snail Pomatias 2 Elegans bioRxiv preprint doi: https://doi.org/10.1101/2020.02.28.970160; this version posted March 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Increased population density depresses activity but does not influence dispersal in the snail Pomatias 2 elegans 3 Maxime Dahirel1,2, Loïc Menut1, Armelle Ansart1 4 1Univ Rennes, CNRS, ECOBIO (Ecosystèmes, biodiversité, évolution) - UMR 6553, F-35000 Rennes, 5 France 6 2INRAE, Université Côte d'Azur, CNRS, ISA, France 7 Abstract 8 Dispersal is a key trait linking ecological and evolutionary dynamics, allowing organisms to optimize 9 fitness expectations in spatially and temporally heterogeneous environments. Some organisms can 10 both actively disperse or enter a reduced activity state in response to challenging conditions, and 11 both responses may be under a trade-off. To understand how such organisms respond to changes in 12 environmental conditions, we studied the dispersal and activity behaviour in the gonochoric land 13 snail Pomatias elegans, a litter decomposer that can reach very high local densities, across a wide 14 range of ecologically relevant densities. We found that crowding up to twice the maximal recorded 15 density had no detectable effect on dispersal tendency in this species, contrary to previous results in 16 many hermaphroditic snails. Pomatias elegans is nonetheless able to detect population density; we 17 show they reduce activity rather than increase dispersal in response to crowding. We discuss these 18 results based on the ability of many land snails to enter dormancy for extended periods of time in 19 case of unfavourable conditions. We propose that dormancy (“dispersal in time”) may be more 20 advantageous in species with especially poor movement abilities, even by land mollusc standards, 21 like P. elegans. Interestingly, dispersal and activity were correlated independently of density; this 22 dispersal syndrome may reflect a dispersal-dormancy trade-off at the individual level. Additionally, 23 we found snails with heavier shells relative to their size tended to be less mobile, which may reflect 24 physical and metabolic constraints on movement and/or survival during inactivity. We finally discuss 25 how the absence of density-dependent dispersal may explain why P. elegans is often found at very 26 high local densities, and the possible consequences for ecosystem functioning and litter 27 decomposition. 28 Keywords 29 Defence, dispersal syndromes, dormancy, ecosystem functioning, gastropod, sex-biased dispersal 30 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.28.970160; this version posted March 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 31 Introduction 32 Dispersal, i.e. movement potentially leading to gene flow in space, is a key organismal trait 33 influencing and linking ecological and evolutionary dynamics in sometimes complex ways (Ronce, 34 2007; Clobert et al., 2012; Bonte & Dahirel, 2017). As the cost-benefit balance of dispersal is 35 expected to vary depending on individual phenotype and experienced conditions, dispersal is often 36 highly context- and phenotype-dependent (Bowler & Benton, 2005; Clobert et al., 2012; Baines, 37 Ferzoco & McCauley, 2019; Endriss et al., 2019). This multicausality of dispersal likely explains why 38 even well-studied environmental factors, like increased population density and competition, may 39 lead to very different dispersal responses depending on populations and species (Bowler & Benton, 40 2005; Matthysen, 2005; Kim, Torres & Drummond, 2009; Fronhofer, Kropf & Altermatt, 2015; Baines 41 et al., 2019; Harman et al., 2020). To understand the context-dependency of dispersal, it is thus 42 necessary to study a broader range of life histories and contexts, including organisms that have 43 alternative strategies to escape negative environmental conditions, such as dormancy, sometimes 44 seen as a form of “dispersal in time” (Buoro & Carlson, 2014). 45 The land winkle Pomatias elegans (Müller 1774)(Fig. 1) is a common gastropod species in forests and 46 hedgerows across Europe (Kerney & Cameron, 1999; Falkner et al., 2001; Welter-Schultes, 2012). As 47 a caenogastropod, it has separate sexes, contrary to the majority of land molluscs which are 48 hermaphrodite (Barker, 2001). Its active dispersal capacities are poorly studied but expected to be 49 very low, even by land mollusk standards (Kramarenko, 2014); average dispersal distances after 42 50 days are below 20 cm, according to one of the only (indirect) records available in the peer-reviewed 51 literature (Pfenninger, 2002). Like many other land snails, it is able to survive up to several months 52 under unfavourable conditions by entering dormancy (Falkner et al., 2001). P. elegans is often 53 distributed in a very aggregated way across landscapes, and when a population is present, local 54 densities can be highly variable, going from fewer than one to several hundred individuals.m-2 55 (Pfenninger, 2002). When it is present, P. elegans plays a key role in ecosystem functioning, by 56 decomposing litter and altering its chemical and physical characteristics (Coulis et al., 2009; De 57 Oliveira, Hättenschwiler & Tanya Handa, 2010). bioRxiv preprint doi: https://doi.org/10.1101/2020.02.28.970160; this version posted March 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 58 59 Figure 1. Pomatias elegans shell showing the measurements used in the present study (photograph: 60 Armelle Ansart). 61 We here tested the hypothesis that active dispersal and activity were density-dependent in P. 62 elegans. As in many other species, including other land molluscs (Baur, 1993; Bowler & Benton, 2005; 63 Matthysen, 2005; Dahirel et al., 2016), we expected dispersal to overall increase with population 64 density and associated competition levels. We expected dispersers to be more active than residents, 65 in agreement with general predictions about dispersal-dormancy syndromes and the pace-of-life 66 hypothesis (Cote et al., 2010; Réale et al., 2010; Buoro & Carlson, 2014). If activity merely is a 67 correlate of dispersal, or vice-versa, we would expect them to both change with density in the same 68 way. If low activity is also/instead a correlate of dormancy, we may expect the opposite response to 69 density: indeed, some previous snail studies showed depression of activity in response to density 70 (Cameron & Carter, 1979). In accordance with the phenotypic compensation hypothesis, which 71 predicts that risk-taking behaviour should be associated with morphological traits limiting 72 vulnerability to predators (e.g. Ahlgren et al., 2015), we also expected dispersers/active individuals to 73 be better defended, by having heavier shells. Finally, we accounted for sex differences, given sex- 74 biased dispersal is often observed in other taxa with separated sexes (Trochet et al., 2016). 75 Material and methods 76 We collected P. elegans snails in spring 2017 in leaf litter and at the bottom of calcareous walls 77 (Falkner et al., 2001) in Arcais, France (approximate location: 46°17'60"N, 0°41'21"W). They were 78 then kept under controlled conditions (20°C, L:D 16:8) in plastic boxes (25 × 25 × 9 cm, about 500 79 snails.m-2) with a 1 cm layer of soil and a roughly 2-3 cm thick layer of leaf litter (predominantly oaks bioRxiv preprint doi: https://doi.org/10.1101/2020.02.28.970160; this version posted March 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 80 Quercus robur and Q. petraea and beech Fagus sylvatica) collected in urban and suburban woodlots 81 and hedgerows on and close to the University of Rennes Beaulieu campus. We provided humidity by 82 watering soil and litter every 10 to 15 days. 83 Dispersal experiment 84 In June 2017, we created two-patch systems by adapting the system we developed for slugs in 85 Fronhofer et al. (2018), but with a shorter inter-patch gap and longer dispersal period to account for 86 the more limited dispersal capacities of P. elegans. We divided 32 × 12 cm2 transparent plastic boxes 87 (height: 9 cm) in two 12 × 12 cm2 patches (“release” and “arrival”) and one central 10 × 12 cm 88 matrix, using plastified cardboard walls. A 2 × 12 cm2 slot was left open in each wall to allow snails to 89 leave and enter patches. Both patches were filled with watered soil and litter as in maintenance 90 boxes (see above), with the matrix was kept dry and empty. 91 We then placed between 1 and 30 snails in each “departure” patch, and first closed the patches for 92 24 h to let the snails habituate. We then let them free to move for 4 days, and recorded which snails 93 stayed in their release patch (hereafter “residents”) and which snails dispersed to the arrival patch. 94 We tested the following group sizes: 1, 2, 3, 4, 5, 10, 15, 20, and 30 snails per box, with respectively 95 30, 20, 10, 9, 6, 4, 3, 3, and 2 replicates (total: 371 snails in 87 replicates). We chose these replicate 96 numbers to have at least 30 individuals and 2 replicates per group size.
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