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Trail-Following Behavior of Land Snails

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Trail-Following Behavior of Land Snails 國立中山大學生物科學系 碩士論文 Department of Biological Sciences National Sun Yat-sen University Master Thesis 陸生蝸牛的痕跡追隨行為 Trail-Following Behavior of Land Snails 研究生：梁師瑀 Shih-yu Liang 指導教授：張學文 博士 Dr. Hsueh-Wen Chang 中華民國 105 年 1 月 January 2016 摘要 費洛蒙為生物體產生的化學物質，會以不同的形式排出體外形成痕跡，並 由同種及異種間利用。而陸生腹足綱痕跡追隨的目的，大致上來說具有群聚、 交配，捕食、回巢及節省能量等功能。我利用兩種壽山常見的陸生蝸牛，分別 為雌雄同體的小菱蝸牛(Satsuma succincta)，及雌雄異體的皺大山蝸牛 (Cyclophorus friesianus) 進行追隨實驗。本研究提出三個問題：(1) 這兩種陸生 蝸牛是否也具有同種間的追隨行為，(2)追隨行為是利用何種化學物質進行追 隨，以及(3)雌雄異體的物種是否可藉由此行為作為交配策略。每次測試皆由兩 隻同種之蝸牛組成：一隻作為遺留黏液之 marker，另一隻為追隨黏液之 tracker。結果發現兩物種皆出現追隨行為，且室內與室外的結果沒有顯著差 異。小菱蝸牛同時出現黏液及以氣味追隨的行為，但以氣味作為主要的化學訊 號；皺大山蝸牛則單純以黏液追隨。在性別差異的實驗中，皺大山蝸牛在異性 間與同性間的追隨頻率雖然沒有顯著差異，但出現異性高於同性的傾向，且雄 性追隨雌性的頻率略高於其他性別配對。雖然無法支持黏液追隨可作為交配策 略，但高程度的重疊比例下，推測黏液追隨的功能可為減少移動能量的耗損達 到省能的目的。 關鍵詞：費洛蒙、痕跡追隨、同種間、交配策略、氣味、黏液 i Abstract Pheromone is produced by animals and secreted in variously ways to form trails which can be used by conspecifics or between species. The functions for trail- following in terrestrial gastropod are aggregating, mating, predating, homing and energy saving. In this study, I used two species of terrestrial gastropod, Satsuma succincta and Cyclophorus friesianus, which are abundance in Mt. Shoushan, Kaohsiung, Taiwan to test three questions: (1) Do these land snails follow the chemical trail laid by conspecifics? (2) If followed, what kind of chemical trail would they follow? (3) Whether trail-following is a mating strategy for dioecious species? Every following behavior test I used two snails, marker for leaving trail and tracker for following trail. Both of the two species showed trail-following behavior, and there were no difference between two studying areas. S. succincta had trail-following behavior both by mucus and odor, but odor was the main chemical cue for C. friesianus. In test for sexual difference on trail-following behavior, although there were no significant difference between the different and same sex groups, the frequency was higher in different sex group and female followed by male was higher than other sexual combining pairs. This test supported that mucus trail-following might be a purpose for energy saving due to the trail overlapped about half of the marker’s trail. Key words: pheromone, trail-following, conspecific, mating strategy, odor, mucus. ii Contents 中文摘要………………………………………………………………….i Abstract…………………………………………………………………..ii Contents………………………………………………………………….iii Introduction………………………………………………………………1 Materials and Methods…………………………………………………...5 Results…………………………………………………………………..10 Discussion……………………………………………………………….13 Literature Cited………………………………………………………….17 Tables……………………………………………………………………21 Figures…………………………………………………………………..24 iii Introduction Trail-following behavior, individuals following the tracks or paths previously laid by themselves or other individuals, occurs in a variety of animal taxa and likely has evolved several times (Alexy et al. 2001; Cafazzo et al. 2012; Dehnhardt et al. 2001; Ng et al. 2013). A trail can be visible like hydrodynamic trail, footprint, and mucus (Dehnhardt et al. 2001; Harmsen et al. 2010; Ng et al. 2013), or invisible like odor (Farkas and Shorey 1972). No matter the trail is visible or invisible, it contains chemical cue used to communicate with conspecifics or heterospecifics (Farkas and Shorey 1972; Harmsen et al. 2010; Davis-Berg 2011; Ng et al. 2011). Pheromones was one of the chemical cue, which could be released for communication in animals. For examples, male moth (Pectinophora gossypiella) uses olfactory cues provided by pheromone plume to identify their mates (Farkas and Shorey 1972). Gastropods utilize mucus laid by other individuals for mate-searching, predation and aggregation (Johannesson et al. 2008; Davis-Berg 2011; Ng et al. 2011; Stafford et al. 2012b). Function of trail-following in gastropod Terrestrial gastropods are well known to adopt pheromone trail-following behavior. Functions of this behavior in gastropods include facilitating aggregation, mating, homing, foraging, and energy saving (McFarlane 1980; Erlandsson and Kostylev 1995; Chapman 1998; Erlandsson 2002; Davies and Blackwell 2007; Johannesson et al. 2008; Johannesson et al. 2010; Davis-Berg 2011; Stafford et al. 2011; Ng et al. 2012). Intertidal species prefer living in groups to form aggregation, which could reduce desiccation stress or reducing predation (Coleman et al. 2004; Stafford et al. 2012a; Stafford et al. 2012b). For cross-fertilization species, trail- following may increase the chance to find an available mate. For example, male Littorina fabalis, L. ardouiniana, and L. melanostoma have the ability to track female 1 by gender-specific mucus cue, which can avoid maladaptive mating (Johannesson et al. 2010; Ng et al. 2011). Moreover, mucus following-behavior was a mechanism of reproduction barrier for L. saxatilis to different ecotypes (Johannesson et al. 2008). The terrestrial carnivorous snail, Euglandina rosea, not only can it follow the mucus laid by pray, but also distinguish conspecifics from prey by mucus (Shaheen et al. 2005; Davis-Berg 2011). Slug Limax pseudoflavus approached the home area relative to the wind direction, and was suggested to have the homing ability by tracking its odor (Cook 1980). In the study of saving energy, Davies and Blackwell (2007) suggested that movements of snails could save approximately 70% of energy cost for trail-following. It was believed that gastropods crawl on mucus laid previously could save energy on rough surface or move faster (Davies and Blackwell 2007; Davis-Berg 2011). Chemical cue in trail-following According to the respiratory, gastropod could be divided into two groups, Prosobranchia, and Pulmonata. Marine and fresh water snail species are mostly Prosobranchia while terrestrial species are mostly Pulmonata. Previous research on the mucus trail-following mainly focused on aquatic Prosobranchia (Ng et al. 2013). Little is known about the trail-following behavior of terrestrial Prosobranchia. Olfaction is the principal sensory modality for detecting and locating by the posterior tentacles in all terrestrial pulmonates for they have no auditory organs and only rudimentary eyes (Chase and Croll 1981). Previous studies supported that some land snails and slugs used odor information to track conspecific or home (Gelperin 1974; Chase et al. 1978; Lemaire and Chase 1998). Cook (1992) suggested that mucus may be subordinate to that of airborne odors, and appeared to be a low priority for trail- following in most slugs. In terrestrial slug Limax pseudoflavus, it would perform 2 mucus trail-following behavior only when the individual was isolated from airborne odors (Cook 1980). In contrast, Chase et al. (1978) documented that terrestrial pulmonate snail Achatina fulica used trail-following to find sexual mates while airborne stimuli (not trails) contain only nonsexual natural information. Nevertheless, another snail species, Otala vermiculata, did not follow the mucus left by conspecifics in the same study. So far, most terrestrial trail-following behavior studies focus on large and hermaphroditic species, and little is known about small hermaphroditic or gonochoric species (Ng et al. 2013). Concentration in chemical cue When pheromone is released from the gastropod to environment, its concentration may change due to diffusion, evaporation of water components of the mucus or change of environmental condition (e.g. rain, tide, wind and temperature). The change of concentration may influence the signal strength of the chemical and, consequently, the trail-following behavior. For example, the intertidal species Cellana grata lives on high rocky shore, where the high temperature environment (> 50°C) may rapidly breakdown the chemical in the mucus. Therefore, the short persistence time of C. grata mucus serves no post-deposition function, i.e. homing, foraging, mate-searching and anti-predator, but it was only used for locomotion and adhering (Davies and Williams 1995). In this study, I tend to the following questions about trail-following behavior of land snail: (1) Do land snails also follow the trail laid by conspecifics? (2) If followed, under morphologic difference in tentacles, what kind of chemical cue do they follow? (3) Is trail-following a mating strategy adopted by gonochoric land snail species? 3 To answer these questions, I tested and compared the trail-following behaviour of two terrestrial gastropod species with distinctively different respirational and reproductive modes, Satsuma succincta (Pulmonata, hermaphroditc) and Cyclophorus friesianus (Prosobranchia, gonochoric). Given the land snail also produced mucus while moving as other marine or intertidal species, I predicted that these two species would perform trail-following behavior as other snail species since trail-following may decrease the energy cost for the movement of the follower (or tracker) and provide benefits for aggregating or mating. If they follow the trail, I predicted the follower would move along or stayed closely to the mucus trail left by the previous individual. Given the pulmonate species was more sensitive to olfactory signals while prosobranch snails rarely used odor signals, I predicted the pulmonate species S. succincta, would follow both mucus and odor trail, while the prosobranch snail C. friesianus, would only follow the mucus trail. In other words, I predicted the follower’s trail would overlapped with the mucus trail laid by the previous individual more closely in the prosobranch species C. friesianus than in pulmonate species S. succincta. For gonochoric
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