Abstract
Mucus-mediated communication plays a significant role in shaping community dynamics, particularly in marine organisms found in intertidal zones with complex topography. In this study, we investigated the host preference of a flatworm Stylochoplana pusilla, which lives symbiotically with intertidal gastropods, and its responses to the host and conspecific mucus. Our line transect surveys revealed differences in flatworm prevalence among sympatric gastropods, with multiple flatworms found in a single host individual, indicating host preference. The body mucus of gastropods and flatworms was applied to one side of a Petri dish to experimentally determine whether flatworms prefer the mucus-coated side under light and dark conditions. However, contrary to our expectations, the experiments in both light and dark conditions showed that the mucus of none of the host gastropods effectively attracted flatworms, suggesting that mucus-mediated communication may not be the primary factor in establishing host preference, and other ecological factors may play a role. Nonetheless, under dark conditions, flatworms were attracted to conspecific mucus, indicating that they may engage in collective homing behaviour or conspecific aggregation to find a suitable position in the mantle cavity. Overall, our results highlight the complex ecological interactions involved in shaping symbiosis between flatworms and gastropods.
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The data used in the study are available from the corresponding author upon request.
References
Armstrong JT (1964) The population dynamics of the planarian, Dugesia tigrina. Ecology 45:361–365. https://doi.org/10.2307/1933849
Bagøien E, Kiørboe T (2005) Blind dating mate finding in planktonic copepods. I. tracking the pheromone trail of Centropages typicus. Mar Ecol Prog Ser 300:105–115. https://doi.org/10.3354/meps300105
Bakus GJ, Targett NM, Schulte B (1986) Chemical ecology of marine organisms: an overview. J Chem Ecol 12:951–987. https://doi.org/10.1007/BF01638991
Bancalà F (2009) Function of mucus secretion by lamellose ormer, Haliotis tuberculata lamellosa, in response to starfish predation. Anim Behav 78:1189–1194. https://doi.org/10.1016/j.anbehav.2009.08.008
Berry FC, Breithaupt T (2008) Development of behavioural and physiological assays to assess discrimination of male and female odours in crayfish, Pacifastacus leniusculus. Behaviour 145:1427–1446. https://doi.org/10.1163/156853908785765845
Chelazzi G, Focardi S, Deneubourg J-L (1988a) Analysis of movement patterns and orientation mechanisms in intertidal chitons and gastropods. In: Chelazzi G, Vannini M (eds) Behavioral adaptation to intertidal life. Springer, New York, pp 173–184
Chelazzi G, le Voci G, Parpagnoli D (1988b) Relative importance of airborne odours and trails in the group homing of Limacus flavus (Linnaeus) (Gastropoda, Pulmonata). J Molluscan Stud 54:173–180. https://doi.org/10.1093/mollus/54.2.173
Cook SB (1969) Experiments on homing in the limpet Siphonaria normalis. Anim Behav 17:679–682. https://doi.org/10.1016/S0003-3472(69)80012-6
Cook A (2001) Behavioural ecology: on doing the right thing, in the right place at the right time. In: Barker GM (ed) The biology of terrestrial molluscs. CABI Publishing, Wallingford, pp 447–487
Deguchi R, Sasaki H, Iwata K, Echizen M (2009) Reproduction and life cycle of the polyclad flatworm. Bull Miyagi Univ Educ 44:53–61
Fujiwara Y, Urabe J, Takeda S (2014) Host preference of a symbiotic flatworm in relation to the ecology of littoral snails. Mar Biol 161:1873–1882. https://doi.org/10.1007/s00227-014-2469-8
Fujiwara Y, Iwata T, Urabe J, Takeda S (2016) Life history traits and ecological conditions influencing the symbiotic relationship between the flatworm Stylochoplana pusilla and host snail Monodonta labio. J Mar Biol Assoc UK 96:667–672. https://doi.org/10.1017/S0025315415001009
Gonor JJ (1965) Predator-prey reactions between two marine prosobranch gastropods. Veliger 7:228–232
Haas W (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106:349–364. https://doi.org/10.1078/0944-2006-00125
Harley CDG, Denny MW, Mach KJ, Miller LP (2009) Thermal stress and morphological adaptations in limpets. Funct Ecol 23:292–301. https://doi.org/10.1111/j.1365-2435.2008.01496.x
Hay ME (2009) Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems. Ann Rev Mar Sci 1:193–212. https://doi.org/10.1146/annurev.marine.010908.163708
Hervé M, Hervé MM (2020) Package ‘RVAideMemoire.’ https://CRAN.R-project.org/package=RVAideMemoire. Accessed 23 Nov 2023
Inoue T, Hoshino H, Yamashita T, Shimoyama S, Agata K (2015) Planarian shows decision-making behaviour in response to multiple stimuli by integrative brain function. Zool Lett 1:7. https://doi.org/10.1186/s40851-014-0010-z
Iwai N, Sugiura S, Chiba S (2010) Prey-tracking behaviour in the invasive terrestrial planarian Platydemus manokwari (Platyhelminthes, Tricladida). Naturwissenschaften 97:997–1002. https://doi.org/10.1007/s00114-010-0717-4
Kato K, Okada K (1933) On Stylochoplana pusilla Bock. Doubutugaku Zasshi 45:487–490. https://doi.org/10.34435/zm002254
Kirsch DR (2022) Freshwater gastropods as an important group for studying the impact of inter- and intra-specific chemical communication on aquatic community dynamics. Aquat Ecol 56:361–375. https://doi.org/10.1007/s10452-022-09961-x
Lee J, Davidson TM, Torchin ME (2021) Variable host responses mediate host preference in marine flatworm-snail symbioses. PLoS ONE 16:e0247551. https://doi.org/10.1371/journal.pone.0247551
Lonsdale DJ, Frey MA, Snell TW (1998) The role of chemical signals in copepod reproduction. J Mar Syst 15:1–12. https://doi.org/10.1016/S0924-7963(97)00044-4
Martín J, López P (2014) Pheromones and chemical communication in lizards. In: Rheubert JL, Siegel DS, Trauth SE (eds) Reproductive biology and phylogeny of lizards and tuatara. CRC Press, Florida, pp 43–77
McFaruume ID (1980) Trail-following and trail-searching behaviour in homing of the intertidal gastropod mollusc, Onchidium verruculatum. Mar Behav Physiol 7:95–108. https://doi.org/10.1080/10236248009386974
Miyamoto S, Shimozawa A (1985) Chemotaxis in the freshwater planarian, Dugesia japonica japonica. Zool Sci 2:389–395
Morita N, Inaba K, Saito Y (2018) Post-embryonic development and genital-complex formation in three species of polyclad flatworms. Zool Sci 35:28–38. https://doi.org/10.2108/zs170114
Ng TPT, Saltin SH, Davies MS, Johannesson K, Stafford R, Williams GA (2013) Snails and their trails: the multiple functions of trail-following in gastropods. Biol Rev Camb Philos Soc 88:683–700. https://doi.org/10.1111/brv.12023
Oksanen J, Blanchet FG, Kindt R, Legendre P (2013) vegan: community ecology package. https://CRAN.R-project.org/package=vegan. Accessed 23 Nov 2023
R Core Team (2013) R: a language and environment for statistical computing. https://www.r-project.org/. Accessed 23 Nov 2023
Rice SH (1985) An anti-predator chemical defense of the marine pulmonate gastropod Trimusculus reticulatus (Sowerby). J Exp Mar Bio Ecol 93:83–89. https://doi.org/10.1016/0022-0981(85)90150-9
Rink JC (2018) Planarian regeneration: methods and protocols. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-4939-7802-1_2
Sato T, Goshima S (2007) Female choice in response to risk of sperm limitation by the stone crab, Hapalogaster dentata. Anim Behav 73:331–338. https://doi.org/10.1016/j.anbehav.2006.05.016
Takada Y (1996) Vertical migration during the life history of the intertidal gastropod Monodonta labio on a boulder shore. Mar Ecol Prog Ser 130:117–123. https://doi.org/10.3354/meps130117
Takada Y (2003) Dimorphic migration, growth, and fecundity in a seasonally split population of Littorina brevicula (Mollusca: Gastropoda) on a boulder shore. Popul Ecol 45:141–148. https://doi.org/10.1007/s10144-003-0151-y
Techawongstien K, Lirdwitayaprasit T, Pairohakul S (2022) Mucus from the pulmonate sea slug Onchidium typhae: biochemical composition and ecological implications for the intertidal community. Mar Ecol 43:e12702. https://doi.org/10.1111/maec.12702
Underwood AJ (1979) The ecology of intertidal gastropods. In: Russell FS, Yonge M (eds) Advances in marine biology. Academic Press, Cambridge, pp 111–210
Vermeij GJ (1973) Morphological patterns in high-intertidal gastropods: adaptive strategies and their limitations. Mar Biol 20:319–346. https://doi.org/10.1007/BF00354275
Vila-Farré M, Rink JC (2018) The ecology of freshwater planarians. Methods Mol Biol 1774:173–205. https://doi.org/10.1007/978-1-4939-7802-1_3
Yamazaki D, Aota T, Chiba S (2020) The genetic structure of the marine flatworm Stylochoplana pusilla (Rhabditophora: Polycladida) and its use of intertidal snails. J Mar Biol Assoc UK 100:713–717. https://doi.org/10.1017/S0025315420000570
Acknowledgements
The authors would like to thank Shun Ito and Kazuki Kimura for conducting sampling and statistical analyses. The authors would also like to thank Jotaro Urabe, Gaku Kumano, Masato Owada, and Kazuo Inaba for their helpful discussions. The authors gratefully acknowledge the members of the Chiba Laboratory, Tohoku University, and members of the Inaba Laboratory, Tsukuba University. Finally, the authors would like to thank the anonymous reviewers and the editors for the peer review.
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This study was supported by KAKENHI from the JSPS (JP21H02556, JP20J14469, and JP22J00433) and Mikimoto Fund for Marine Ecology.
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WS and OK designed this study; WS, OK, and MT conducted the fieldwork, experiments, and data analyses; SC and OK provided funding; WS, OK, and SC wrote the paper; and WS, OK, MT, and SC revised the paper.
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All applicable, national, and/or institutional guidelines for animal testing, animal care and use of animals were followed by the authors. No approval of research ethics committees was required to accomplish the goals of this study, because experimental work was conducted with an unregulated invertebrate species.
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Sakata, W., Tatani, M., Chiba, S. et al. Host preference of a symbiotic flatworm and its response to conspecific and host mucus. J Ethol 42, 53–59 (2024). https://doi.org/10.1007/s10164-023-00802-4
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DOI: https://doi.org/10.1007/s10164-023-00802-4