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Reproductive System, Mating Behavior and Basic Ecology of an Extremely Rare Tropical Snail: Drymaeus Tripictus (Stylommatophora: Bulimulidae)

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Reproductive System, Mating Behavior and Basic Ecology of an Extremely Rare Tropical Snail: Drymaeus Tripictus (Stylommatophora: Bulimulidae) Reproductive system, mating behavior and basic ecology of an extremely rare tropical snail: Drymaeus tripictus (Stylommatophora: Bulimulidae) Zaidett Barrientos Laboratorio de Ecología Urbana, UNED, 2050 San José, Costa Rica; [email protected], [email protected] Received 06-IV-2015. Corrected 20-VIII-2015. Accepted 21-IX-2015. Abstract: Very little is known about the ecology and biology of Drymaeus tripictus, an extremely rare and endemic land snail species from Costa Rican highlands. I studied the ecology and reproductive biology of D. tri- pictus from April 2009 through June 2010 in an old forest, a young forest and a Cupressus lusitanica plantation in central Costa Rica. Every three months I visited each habitat and collected specimens in 20 random sampling plots (3x3 m2 each). I observed the snail’s activity and microhabitat preference in the field, and in the labora- tory I recorded high definition videos of its mating behavior and analyzed reproductive morphology with light microscopy. The snail is more abundant in the old forest (0.017 ind./m2) and prefers leaves with little epiphyllous cover (0-25 % cover, chi-square test, p <0.0001). During the dry season the snails become active between 20:00 pm and 8:00 am (chi-square = 22.65, df=3, p < 0.0001); they are inactive mainly during the afternoon (11:00 am to 16:59 pm). I found active individuals mostly on the upper side of leaves, where they feed (Chi-square =6.76, df=1, p = 0.0093). Mating is unilateral, by shell mounting, with cryptic phallus intromission and without role switching or multiple mating. Its reproductive system is morphologically similar to that of Drymaeus costari- censis. Mating behavior is as expected for snails with high-spired shells, except for the lack of role switching. The density of D. tripictus is low even when compared with other endangered bulimulids. Rev. Biol. Trop. 64 (1): 55-68. Epub 2016 March 01. Key words: land snail, reproductive anatomy, ecology, mating behavior, activity. The tree snail Drymaeus tripictus Albers, In South America about 50% of the known 1857 is an extremely rare and nearly unknown snail species belong to this family (Breure & tree snail of the family Bulimulidae. This Borrero, 2008), and in Costa Rica (Central species is closely related with Drymaeus America) it is also one of the three most diverse irazuensis (Angas, 1878) and Drymaeus gabbi families (Barrientos 2005; 2010). The genus (Angas, 1878) (Pilsbry, 1899), as suggested Drymaeus has a total of 640 reported species by the adult red outer lip. These three species that inhabit North, Central, South and Insular are endemic and restricted to the central Costa America, from sea level to 2 900 metris supra Rica highlands (Martens, 1802-1899; Pilsbry, mare (msm) (Breure, 1979; Thompson, 2011). 1899), an area impacted by urban expansion. A great contribution to the understanding of Nothing has been reported about its ecology or Drymaeus taxonomy was made by Pilsbry biology (Martens, 1802-1899; Pilsbry, 1899; (1897-1898, 1899), and more recently by Breu- Barrientos, 2010). Breure and Eskens (1981) re (Breure, 1974; 1979, Breure & Eskens, 1981; illustrated its radula and jaw, but its reproducti- Breure & Borrero, 2008; Breure & Mogollón, ve system was unknown until now. 2010; Breure & Romero, 2012; among others). Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (1): 55-68, March 2016 55 Despite its high diversity and wide dis- humid premontane forest with inceptison dys- tribution, information on Drymaeus ecology trandept soil. and biology is scarce (Breure, 1979). Most I visited the old growth and young secon- observations are brief and included within dary forests in April, July and October 2009 systematic papers. and January 2010. The cypress plantation was The Bulimulidae’s reproductive anatomy sampled in July and October 2009 and January is known for several species, including some and April 2010. Costa Rican Drymaeus species (Breure, 1974; On each sampling day I set a 200 m ran- 1979; Breure & Eskens, 1981; Beese, 2007; domly located transect (chosen with a digital Beese, Armbruster, Beier, & Baur, 2009). It is random number generator) at least 10 m away reported as being simple externally and com- from any trail to avoid edge effect and away plicated internally, and as having a short flagel- from tree gaps to avoid the effect of direct sun lum and carrefour with multiple sperm storing on litter (Camargo & Kapos, 1995). I also avoi- tubules (Solem, 1955; Van Mol, 1971; Breure, ded sampling in the same transect twice. Each 2 1974; Beese, 2007; Beese et al., 2009). Never- transect had 20 random 3x3 m plots (Digital theless, the mating behavior is not known and Appendix 2) where I collected all the snails I their mode of phallus intromission is unknown could find between 9:00 am and 2:00 pm. (Jordaens, Dillen, & Backeljau, 2009). In each plot and with the assistance of a In this paper I have described the repro- student, I collected arboreal snails with a 50x50 2 ductive system, mating behavior and mode of cm beat sheet (Digital Appendix 2) for about phallus intromission of D. tripictus, and present 7 min I gently beat branches, shrubs and seed- basic information about its daily activity, abun- lings up to 200 cm above ground and scrubbed dance, demography and shell coloration. tree trunks with a gardening glove. I also collected all leaf litter in a 50x50 cm2 subplot (Digital Appendix 2). MATERIALS AND METHODS I checked the leaf litter in the laborato- ry with magnifying glass and stereoscopic I selected three habitats with inclination microscopes. over 40° in Reserva Forestal Río Macho (Car- Empty shells can be misleading (Barrien- tago, Costa Rica): tos, 2000), so I only counted specimens collect- Old Growth Forest with well-developed ed alive, and I measured shell diameters with canopy and understory near the “El llano” a Zeiss microsteroscopic scale at 16.25X. I water dam (9º45’56.07” N - 83º51’47.11” W classified specimens as newborn when only the - 1 640 msm) (Digital Appendix 1) and Young embryonic whorls were present; juvenile when Secondary Forest (Clark, 1996) left to natural the embryonic and other whorls were present succession for about 15 years, with a poorly but periostome was not reddish or pinkish; and developed canopy, and dense understory in adult, when at least part of the periostoma was some areas and grass in others (9º45’29.52” reddish or pinkish. On each habitat I calculated N - 83º51’23.27” W - 1 684 msm) (Digital density by dividing total number of specimens appendix 1). Both are located in a tropical by total area of the sampling plots. lower montane wet forest area with ultisol I deposited specimens as vouchers to the humult soil. University of Costa Rica Zoology Museum Cupressus lusitanica Mill. 1768 plantation (MZUCR 220-01, MZUCR 220-02, MZUCR that has been without management for nearly 220-03, MZUCR 223-01, MZUCR 225-01, 40 years and therefore has a poorly developed MZUCR 227-01). understory dominated by hardwood species I observed daily cycle activity in spec- (9º47’52” N - 83º51’51” W - 1 309 msm) (Dig- imens found in the primary forest in a 2 km ital Appendix 1). Located in an area of tropical long trail during seven sampling days in the 56 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (1): 55-68, March 2016 dry season (from December 2009 through specimens only between March and April April 2010). On each sampling day I walked 2010. During this period I collected nine speci- along a trail for about an hour, and repeated mens on three different dates. the hike every three hours in a 24 hour period. On three occasions I chose two individuals In the first walk of the day, I numbered each collected the same day and I kept them alone specimen and used colour ribbons to mark in the laboratory until the next day, when I trails, plants, stems and leaves so that I could put them together in a 946 ml container. Each follow each specimen individually (Digital pair of snails was filmed with a high definition Appendix 3). Additionally I marked specimen Sony Handycam HDR XR 200 and took digital location on leaves with a felt-tipped marker to photographs to illustrate shell color variability follow their displacement (Digital Appendix in mating pairs. Intercourse was sometimes 3). In each case I took note of: hour, activity, interrupted. In those cases, I considered the behavior, part of the leaf (upper or lower side of partner that split away first responsible of the leaf), height on the plant above the ground, intercourse interruption. Some intercourse inte- coverage of visible epiphyllous and weather rruptions and separations after mating allowed (“rainy”, “cloudy with wet soil”, “cloudy with me to observe the phallus of the male-acting dry soil or sunny”, I merge sunny and cloudy partner. This allowed me to observe if phallus with dry soil categories as these two conditions intromission was unilateral or simultaneous. appeared to be similar in terms of humidity After mating I isolated each specimen and kept of microhabitat of the snail in an old growth them alive for one month. forest). I could not measure temperature and I kept each specimen in a hermetic translu- humidity. I classified time in four categories: cent plastic terrarium (10x10x11 cm3). Terraria 05:00 am-10:59 am (morning), 11:00 am-16:59 had a 1 cm thick layer of wet soil from the pm (afternoon), 17:00 pm-22:59 pm (night), Old Growth Forest. I provided food by put- 23:00 pm-04:59 am (dawn).
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