Notes on the head-wart found in the Southern Flatcoil snail ( cereolus)

Gia DiPanfilo, Casey Courser Malacology, Independent

 Correspondence Abstract [email protected] [email protected] The reproductive behaviors of terrestrial gastropods are often complex and vary sub- stantially between . Any similarities in these behaviors may indicate a degree of  Disciplines evolutionary relatedness between taxa and thus have the potential to be used as an aux- Zoology iliary tool when attempting to classify species. 45 adult members of the species Polygyra  Keywords cereolus were collected to study the reproductive behavior of this species and to compare Land Snails it to P. septemvolva, a species whose reproductive behavior has already been described. Polygyrid Malacology During this process, a small protuberance of tissue appearing on the forehead between Head-Wart the optic tentacles was noted. This structure visually appears homologous to what has previously been described in other terrestrial gastropods as “head-wart”, “frontal organ”,  Type of Observation and “cephalic accessory organ”. In this paper, it will simply be referred to as “head-wart”. Standalone

 Type of Link Standard Data Introduction Head-warts have been seen before in terrestrial gastropods, particularly in members of  Submitted Mar 27, 2017 the families and Bradybaenidae [1], although they have also been observed ⴑ Published Sep 14, 2017 in the genus Gymnarion [2]. Additionally, head-warts have been observed in the heli- cid snail Arianta arbustorum within a small percentage of courting individuals [3]. The appearance of this wart can vary greatly, with some species possessing warts covered in calciferous hooks [4] and others possessing subtle, smooth warts that are only visible

3 x when everted [1]. A particularly notable example is in the Japanese species peliomphala, which possesses a rough, dark-colored head-wart [5] that was found to secrete testosterone. In this species, the wart was found to have an important role in courtship, as testosterone secreted from the structure served to excite snails prior to Triple Blind Peer Review copulation [6]. However, till date, no such organ related to any snail in the family Poly- The handling editor, the re- viewers, and the authors are gyridae has ever been described. If this structure is common in this family, then this may all blinded during the review serve as further evidence [7] [8] [9] that there exists a close evolutionary relationship process. between the family and the families Camaenidae and Bradybaenidae.

Objective We aim to describe the head-wart found in and observe the behavior associated with its eversion.

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Creative Commons 4.0 This observation is dis- tributed under the terms of the Creative Commons Attribution 4.0 International License.

DOI: 10.19185/matters.201706000010 Matters (ISSN: 2297-8240) 1

| Notes on the head-wart found in the Southern Flatcoil snail (Polygyra cereolus)

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Figure Legend Figure 1. (A–D) Polygyra cereolus displaying head-wart in various stages of erection. A shows the structure a little under half way erect, B shows it almost completely erect, and C shows it fully erect. In D, the structure is beginning to retract. Swollen, spaced-out papillae are visible in this photo. (E–F) Two different angles of two separate individuals, both lacking the erect structure for comparison. Supplementary Figure. The panel on the left is a frontal angleof P. cereolus with a fully erect head-wart. The black arrow points to the convex shape of the structure. The panel on the right shows a different individual lacking an erect wart for comparison.

Results & Discussion Physical Description of the Head-Wart Microscopically, the surface of the head-wart in P. cereolus appears uniform to the sur- face of the surrounding tissue, but it can be differentiated because of the gaps that ap- pear between the papillae on the snail’s head when the structure becomes erect. This coincides with what was described in the snails fruticum and sieboldiana [1]. In each of these species, the head-wart is indistinct from the rest of the epidermis, only becoming noticeable after wart eversion, which is comparable with what was observed in P. cereolus. If the wart is homologous to those present in other species, its eversion is a result of the swelling of the body wall that is brought on by internal pressure [2]. In P. cereolus, the swelling first begins between the two optic tentacles, and it has the appearance of a small, round growth. As time passes and the growth increases in size, it eventually grows so large that the entire forehead of the snail

DOI: 10.19185/matters.201706000010 Matters (ISSN: 2297-8240) 2

| bulges out between the area of the optic tentacles and the oral tentacles. As the pro- trusion of the head-wart increases its color lightens significantly in comparison to the surrounding tissue; the head-wart adopts a translucent, grayish tint, contrasting against the typical yellow or brownish integument of this species. Associated Behavior Over the course of 2 months, the head-wart was observed for a total of 11 times. Each time, prior to wart eversion, P. cereolus was first seen resting on the side of the terrarium motionless for several hours. Subsequently, the snail’s forehead would begin to protrude outwards, very slowly over the course of approximately 15–30 min. Once the structure was fully erect, the snails would sit very still, just barely moving their optic tentacles one at a time in small, subtle circular motions. If left uninterrupted, the snails would often remain in this posture for 1–2 h, at which time the wart would slowly retractback into the head; then the snail would move on. Of the 11 total times the structure was seen, 6 times the snail was left uninterrupted for the duration of the wart’s erection, and 5 times the snail was interrupted by another snail. In 20% of the interruptions, the intruding snail ignored the snail with the erect head-wart and continued on its way. However, in the other 80% of the interruptions, courtship behavior began. Courtship in this species consists of aggressively rasping one another followed by antiparallel cir- cling. As these actions cycle, the genital pore gradually begins to swell. The swelling of the genital pore typically marks the withdrawal of the head-wart. However, in one in- stance, 2 snails went from being without everted head-warts to having fully erect ones while simultaneously having swollen genital pores. The structures continued to pro- trude until both snails fully everted their genitalia, at which time it appeared that the internal pressure needed to evert the genitalia was diverted away from the head-wart, thus causing the wart to shrink. Consumption of the mucus secreted by the snail with the swollen wart by the intruding snail prior to copulation was also a common sight. If this species releases testosterone or another sex pheromone via its head-wart as in E. peliomphala [6], it may be that the smell and consumption of the mucus serves in getting a partner initially interested in copulation.

Limitations This study does not examine the histology of the head-wart. Until that is done, itcannot be soundly confirmed that this structure is physically related to the wart described prior in other terrestrial gastropods. This study also has a small sample size. A larger sample needs to be observed to accurately determine what role the wart plays in the life of P. cereolus and if this structure is related to reproductive behavior like it is in other species.

Additional Information

Methods and Supplementary Material Please see https://sciencematters.io/articles/201706000010.

Funding Statement No funding was sought for this study.

Acknowledgements Thanks go out to John Slapcinsky for his insight and advice.

Ethics Statement Not applicable.

Citations

3 [1] Iwao Taki. “Notes on a warty growth on the head of some land 10.1093/mollus/eym030. url: snails”. In: Journal of Science and Hiroshima University and Series https://doi.org/10.1093/mollus/eym030. B and Division 1 and 3 (1935), pp. 159–183. [9] John M. C. Hutchinson and Heike Reise. “Mating behaviour [2] Eugène Binder. “Cephalic accessory sexual organ of Gymnarion: clarifies the of slug species defined by genital speciation and phylogeny (, Helicarionidae)”. In: anatomy: the Deroceras rodnae complex in the Sächsische Malacologia 9 (1969), pp. 59–64. Schweiz and elsewhere”. In: 27 (2009), pp. 183–200. [3] Tim R. Birkhead and Anders Pape Møller. “Sperm Competition [10] Leslie Hubricht. “The distributions of the native land mollusks of and Sexual Selection”. In: Elsevier Science (1998), p. 274. the eastern United States”. In: Fieldiana: Zoology 24 (1985), p. 147. [11] Robert H. Cowie. “New records of introduced land and [4] Eugène Binder. “Structure de l’organe sexuel frontal des freshwater snails in the Hawaiian islands”. In: Bishop Museum Gymnarion des Monts Nimba”. In: Revue Suisse De Zoologie 72 Occasional Papers 46 (1996), pp. 25–27. (1965), pp. 584–593. doi: 10.5962/bhl.part.75649. url: https://doi.org/10.5962/bhl.part.75649. [12] Pritpal Soorae et al. “Alien species recorded in the United Arab Emirates: an initial list of terrestrial and freshwater species”. In: [5] Naokuni Takeda and Hitomi Tsuruoka. “A sex pheromone Journal of Threatened Taxa 7.12 (Oct. 2015), pp. 7910–7921. doi: secreting gland in the terrestrial snail, Euhadra peliomphala”. In: 10.11609/jott.o4352.7910-21. url: https: Journal of Experimental Zoology 207.1 (Jan. 1979), pp. 17–25. doi: //doi.org/10.11609/jott.o4352.7910-21. 10.1002/jez.1402070103. url: https://doi.org/10.1002/jez.1402070103. [13] Robert H. Cowie et al. “The horticultural industry as a vector of alien snails and slugs: widespread invasions in Hawaii”. In: [6] Naokuni Takeda. “Hormonal control of head-wart development International Journal of Pest Management 54.4 (Oct. 2008), in the snail, Euhadra peliomphala”. In: Development 60 (1980), pp. 267–276. doi: 10.1080/09670870802403986. url: pp. 57–69. https://doi.org/10.1080/09670870802403986. [7] Christopher M. Wade, Peter B. Mordan, and Bryan Clarke. “A [14] Lindsey T. Groves and Phil Liff-Grieff. “Polygyra Cereolus phylogeny of the land snails (: Pulmonata)”. In: (Muhlfeld, 1818) (Gastropoda: Polygyridae), the Southern Flatcoil, Proceedings of the Royal Society of London B: Biological Sciences a recently introduced species in southern California”. In: The 268.1465 (Feb. 2001), pp. 413–422. doi: Festivus 44 (2012), pp. 115–123. 10.1098/rspb.2000.1372. url: [15] R. S. Kalmbacher, D. R. Minnick, and F. G. Martin. “Destruction of https://doi.org/10.1098/rspb.2000.1372. Sod-seeded Legume Seedlings by the Snail (Polygyra cereolus)”. [8] Christopher M. Wade et al. “Molecular phylogeny of the helicoid In: Agronomy Journal 71.2 (1979), pp. 365–368. doi: land snails (Pulmonata: : ), with 10.2134/agronj1979.00021962007100020034x. special emphasis on the Camaenidae”. In: Journal of Molluscan url: https://doi.org/10.2134/agronj1979. Studies 73.4 (Oct. 2007), pp. 411–415. doi: 00021962007100020034x.

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