A new aestivation strategy for land molluscs: hanging upside down like bats
PDF
HTML
EPUB

Supplementary Files

Video 01 Hanging
Video 02 Unhanging
Video 03 Shell rotation
Video 04 Foot twisting
Video 05 Grooming
Video 06 Feeding
Video 07 Defecating

Keywords

aestivation
defensive behavior
caudal gland
grooming

How to Cite

Barrientos, Z. (2020). A new aestivation strategy for land molluscs: hanging upside down like bats. UNED Research Journal, 12(1), e2802. https://doi.org/10.22458/urj.v12i1.2802

Abstract

Introduction: Many land molluscs survival strategies are still poorly understood or have not been even reported, especially in the Neotropics. Methods: I collected 25 adult Tikoconus (Tikoconus) costarricanus from Reserva Forestal Río Macho, Costa Rica. I kept the specimens for 8 days in terrariums to film their behavior. Objective: To analyse the behavior of T. costarricanus, with emphasis on its strategies to survive drought and probably also predation. Results: This snail has at least three unusual behaviors that probably help them reduce dehydration and may be escape from enemies and avoid diseases: hanging upside down like bats, falling and grooming. During aestivation, they compress the body and hang upside down from leaves, like bats hang from perches. They attach to the underside of leaves with mucus from a caudal gland. Disengagement is done with vigorous shell rotations and foot twisting in contorting sequences, and can be done as reaction to direct sunlight, and probably to avoid predators and parasites. They groom their own shell, shell lappets and foot, an unusual behavior among land snails. This species feeds mainly on epiphyllous mosses, algae and lichens, occasionally adding arthropod eggs and carrion. Egg laying is similar to other euconulids and valloniid snails. Conclusions: Aestivating hanging upside down is a drought avoiding trait described here for the first time and is also a new function for the caudal gland mucus. Leaf detaching is done by a contortion sequence of shell rotations and foot twisting; its complexity and duration varies according to the leaf side where the snail is located.
https://doi.org/10.22458/urj.v12i1.2802
PDF
HTML
EPUB

References

Arad, Z., Goldenberg, S., & Heller, J. (1989). Resistance to desiccation and distribution patterns in the land snail Sphincterochila. Journal of Zoology, 218(3), 353-364. DOI: 10.1111/j.1469-7998.1989.tb02549.x

Arad, Z. (1990). Resistance to desiccation and distribution patterns in bush‐dwelling land snails. Journal of Zoology, 221(1), 113-124. DOI: 10.1111/j.1469-7998.1990.tb03780.x

Arad, Z., Mizrahi, T., Goldenberg, S., & Heller, J. (2010). Natural annual cycle of heat shock protein expression in land snails: desert versus Mediterranean species of Sphincterochila. Journal of Experimental Biology, 213(20), 3487-3495. DOI: 10.1242/jeb.047670

Asami, T. (1993). Interspecific differences in desiccation tolerance of juvenile land snails. Functional Ecology, 7(5) 571-577. DOI: 10.2307/2390133

Barrientos, Z. (1998). Life history of the terrestrial snail Ovachlamys fulgens (Stylommatophora: Helicarionidae) under laboratory conditions. Revista Biología Tropical, 46(2), 369-384. Retrieved from https://revistas.ucr.ac.cr/index.php/rbt/article/view/19628/19714

Barrientos, Z. (2005). Moluscos terrestres de los páramos de Costa Rica. In M. Kappelle & S.P. Horn (eds.), Páramos de Costa Rica (pp. 501– 512). Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio)

Barrientos, Z. (2012). Dynamics of leaf litter humidity, depth and quantity: two restoration strategies failed to mimic ground microhabitat conditions of a low montane and premontane forest in Costa Rica. Revista de Biología Tropical, 60(3), 1041-1053. Retrieved from https://revistas.ucr.ac.cr/index.php/rbt/article/view/18582/22978

Barrientos, Z. (2016). Reproductive system, mating behavior and basic ecology of an extremely rare tropical snail: Drymaeus tripictus (Stylommatophora: Bulimulidae). Revista de Biología Tropical, 64(1), 55-68. Retrieved from https://www.scielo.sa.cr/pdf/rbt/v64n1/0034-7744-rbt-64-01-00055.pdf

Barrientos, Z. (2019a). A new genus of semislugs (Stylommatophora, Euconulidae) from Costa Rica and a review of the genus Velifera (Stylommatophora, Euconulidae). Revista Biología Tropical, 67(6), 1313-1358. DOI: 10.15517/RBT.V67I6.36105

Barrientos, Z. (2019b). Demography of the land snail Tikoconus (Tikoconus) costaricanus (Stylommatophora: Euconulidae) in tropical low montane and premontane forests, Costa Rica. Revista Biología Tropical, 67(6), 1449-1460. DOI: 10.15517/RBT.V67I6.36201

Barr, R. A. (1927). Memoirs: Some Notes on the Mucous and Skin Glands of Arion ater. Journal of Cell Science, 2(283), 503-525. Retrieved from https://jcs.biologists.org/content/joces/s2-71/283/503.full.pdf

Binney, W. G. (1879). On the jaw and lingual dentition of certain Costa Rica Land Shells collected by Dr. William M. Gabb. Annals of the New York Academy of Sciences, 1(9), 257-262, Pl.XI.

Breure, A. S. (2011). Dangling shells and dangerous spiders: malacophagy and mimicry in terrestrial gastropods. Folia conchyliologica, 7, 7-13. Retrieved from https://www.researchgate.net/publication/254879625_Dangling_shells_and_dangerous_spiders_malacophagy_and_mimicry_in_terrestrial_gastropods

Callaghan, C. J. (1992). Biology of epiphyll feeding butterflies in a Nigerian cola forest. Journal of the Lepidopterists' Society, 46(3), 203–214. Retrieved from http://images.peabody.yale.edu/lepsoc/jls/1990s/1992/1992-46(3)203-Callaghan.pdf

Cook, A. (2001). Behavioural Ecology: On Doing the Right Thing, in the Right Place at tha Right Time. In: Barker, G.M. (ed). The biology of terrestrial mollusks (pp. 447-488.). New York, USA: CABI publishing.

Dimitriadis, V. K. (2001). Structure and Function of the Digestive System in Stylommatophora. In: Barker, G.M. (ed). The biology of terrestrial mollusks (pp. 237-257). New York, USA: CABI publishing.

Dourson, D. C. (2008). The feeding behavior and diet of an endemic West Virginia land snail, Triodopsis platysayoides. American Malacological Bulletin, 26(1/2), 153-160. DOI: 10.4003/006.026.0215

Elves, M. W. (1961). The histology of the foot of Discus rotundatus, and the locomotion of gastropod Mollusca. Journal of Molluscan Studies, 34(6), 346-355. DOI: 10.1093/oxfordjournals.mollus.a064880

Emberton, K. C. (1994). Morphology and aestivation behaviour in some Madagascan acavid land snails. Biological Journal of the Linnean Society, 53(2), 175-187. DOI: 10.1111/j.1095-8312.1994.tb01008.x

Giokas, S., Pafilis, P., & Valakos, E. (2005). Ecological and physiological adaptations of the land snail Albinaria caerulea (Pulmonata: Clausiliidae). Journal of Molluscan Studies, 71(1), 15-23. Retrieved from https://academic.oup.com/mollus/article/71/1/15/997866

Gould, J., Valdez, J. W., & Upton, R. (2019). Adhesive defence mucus secretions in the red triangle slug (Triboniophorus graeffei) can incapacitate adult frogs. Ethology, 125(8), 587-591. DOI:10.1111/eth.12875

Gugler, C. W. (1963). The eggs and egg-laying habits of some Midwestern land snails. Transactions of the Kansas Academy of Science (1903-), 66(2), 195-201. DOI: 10.2307/3626560

Hyman, L. H. (1967). The Invertebrates: Mollusca 1 (Vol VI). New York, USA: McGraw-Hill.

Karlin, E. J., & Bacon, C. (1961). Courtship, mating, and egg-laying behavior in the Limacidae (Mollusca). Transactions of the American Microscopical Society, 80(4), 399-406. DOI: 10.2307/3223598

Kuźnik-Kowalska, E., Proćków, M., Pląskowska, E., & Pokryszko, B. M. (2018). Egg Grooming in Vallonia Snails—Anti-Parasite Defence or Trophic Behaviour? Polish Journal of Ecology, 66(1), 64-70. DOI: 10.3161/15052249PJE2018.66.1.007

Le Ferrand, H., & Morii, Y. (2020). Structure–behaviour correlations between two genetically closely related snail species. Royal Society Open Science, 7(1), 191471. DOI: 10.1098/rsos.191471

Luchtel, D. L., & Deyrup-Olsen, I. (2001). Body wall: form and function. In: Barker, G. M. (ed). The biology of terrestrial mollusks (pp. 147-178). New York, USA: CABI publishing.

Moreno-Rueda, G., Ruiz-Ruiz, A., Collantes-Martín, E., & Arrébola, J. R. (2009). Relative importance of humidity and temperature on microhabitat use by land snails in arid versus humid environments. p. 331-343. In: Fernández–Bernal, A. & De la Rosa, M.A. (Eds). Arid Environments and wind erosion. Nueva York, USA: Nova Science Publishers.

Morii, Y., Prozorova, L., & Chiba, S. (2016). Parallel evolution of passive and active defence in land snails. Scientific reports, 6, 35600. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5105203/

Naranjo-García, E. (2003). Moluscos continentales de México: terrestres. Revista de Biología Tropical, 51 (Suppl. 3), 483-493. Retrieved from https://revistas.ucr.ac.cr/index.php/rbt/article/view/26396/26584

Newell, P.F., & Machin, J. (1976). Water regulation in aestivating snails. Cell and tissue research, 173(3), 417-421.

Pomeroy, D. E. (1968). Dormancy in the land snail, Helicella virgata (Pulminata: Helicidae). Australian Journal of Zoology, 16(5), 857-869. DOI: 10.1071/zo9680857

Prior, D. J. (1985). Water‐regulatory behaviour in terrestrial gastropods. Biological Reviews, 60(3), 403-424. DOI: 10.1111/j.1469-185X.1985.tb00423.x

Ng, T. H., & Tan, S. K. (2011). Observations of land snails feeding on the eggs of Pomacea canaliculata (Lamarck, 1822)(Mollusca: Gastropoda). Nature in Singapore, 4, 79-83. Retrieved from https://lkcnhm.nus.edu.sg/app/uploads/2017/06/2011nis079-083.pdf

Rahman, M.S., & Raut, S.K. (2010). Factors inducing aestivation of the giant African land snail Achatina fulica Bowdich (Gastropoda: Achatinidae). Proceedings of the Zoological Society, 63(1), 45-52.

Reber, A., Purcell, J., Buechel, S., Buri, P., and Chapuisat, M. (2011). The expression and impact of antifungal grooming in ants. Journal of evolutionary biology, 24(5), 954-964. DOI: 10.1111/j.1420-9101.2011.02230.x

Rollo, C.D., & Wellington, W.G. (1979). Intra- and inter-specific agonistic behavior among terrestrial slugs (Pulmonata: Stylommatophora). Canadian journal of Zoology, 57, 846-855. DOI: 10.1139/z79-104

South, A. (2012). Terrestrial slugs: biology, ecology and control. Berlin, Germany: Springer Science & Business Media.

Sparks, J. (1967). Allogrooming in Primates: a Review. In: Morris D. (ed.). Primate ethology. pp. 148-175. Aldine, Chicago, USA: Aldine Transaction. Retrieved from https://psycnet.apa.org/record/2006-01577-004

Speiser, B. (2001). Food and feeding behaviour. In: Barker, G. M. (ed). The biology of terrestrial mollusks (pp. 259-288). New York, USA: CABI publishing.

Vermeij, G. J. (2015). Gastropod skeletal defences: land, freshwater, and sea compared. Vita Malacologica, 13, 1-25. Retrieved from https://www.repository.naturalis.nl/document/621888

Wahl, M. (1997). Increased drag reduces growth of snails: comparison of flume and in situ experiments. Marine Ecology Progress Series, 151, 291-293. Retrieved from https://www.int-res.com/articles/meps/151/m151p291.pdf

Wiktor, A. & Stawarczyk, T. (2011). An unusual mode of locomotion of an Ecuadorean slug Belocaulus sp. (Mollusca: Gastropoda: Vaginulidae). Folia Malacologica, 19(4), 277–278. DOI: 10.2478/v10125-011-0007-6

Wilson, S. N., Sindi, S. S., Brooks, H. Z., Hohn, M. E., Price, C. R., Radunskaya, A. E., ... & Fefferman, N. H. (2020). How Emergent Social Patterns in Allogrooming Combat Parasitic Infections. Frontiers in Ecology and Evolution, 8, 54. DOI: 10.3389/fevo.2020.00054

Withers, P., Pedler, S., & Guppy, M. (1997). Physiological adjustments during aestivation by the Australian land snail Rhagada tescorum (Mollusca: Pulmonata: Camaenidae). Australian Journal of Zoology, 45(6), 599-611.

Wondrak, G. (2012). Monotypic gland-cell regions on the body surface of two species of Arion: ultrastructure and lectin-binding properties. Journal of Molluscan Studies, 78(4), 364-376. DOI: 10.1093/mollus/eys024

Yeargan, K. V. (1994). Biology of bolas spiders. Annual review of entomology, 39(1), 81-99. Retrieved from http://www.annualreviews.org/doi/abs/10.1146/annurev.en.39.010194.000501

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.