Population Dynamics and Mantle Autotomy of the Figsnail Ficus ...

Zoological Studies 38(1): 1-6 (1999)Population Dynamics and Mantle Autotomy of the Figsnail Ficus ficus(Gastropoda: Mesogastropoda: Ficidae)Li-Lian Liu* and Sheau-Ping WangInstitute of Marine Biology, National Sun Yat-sen University, Kaohsiung, Taiwan 804, R.o.C.Fax: 886-7-5255100. E-mail: lilian@mail.nsysu.edu.tw(Accepted September 11, 1998)Li-Lian Liu and Sheau-Ping Wang (1999) Population dynamics and mantle autotomy of the figs nail Ficusficus (Gastropoda: Mesogastropoda: Ficidae). Zoological Studies 38(1): 1-6. Ficus ficus, a member of theMesogastropoda, exhibits a special behavior of mantle autotomy as a defensive mechanism. This study wasconducted to characterize the population dynamics of F. ficus and the occurrence of autotomic behavior in thefield. Monthly collections of F. ficus were made between May 1992 and June 1993. A total of 2186 individualswere sampled with shell lengths ranging from 28 to 95 mm. Small individuals with shell lengths < 35 mm werefound only between July and September 1992. Seasonal variation in the abundance of figsnails was observed:while few figsnails (less than 75 individuals) were collected from May to July, abundant snails were obtainedfrom November to February. Sexual dimorphism in shell length (male < female) was also found. Sex ratiosvaried from 0.3 to 2.3 in favor of females between March and September. The male-biased sex ratiosobserved between October and February indicate that egg-laying migration might exist. The autotomic tissueweighed from 0.03 to 8.86 g and comprised 0% to 34% of the total body weight. A negative correlationbetween the percentage of autotomic tissue and shell length was observed (y = 30.88 - 0.27x; R 2 = 0.35;P < 0.01). Figsnails with newly regenerated tissue (indication of recent occurrence of defensive autotomy)comprised < 1% of the total samples, with 0 to 3 individuals appearing in each monthly collection. The resultsindicate that autotomized figsnails might be more vulnerable to predation than are intact snails, or that theoccurrence of defensive autotomy in natural environments might be low.Key words:Ficus ficus, Figsnail, Population dynamics, Autotomy.Figsnails (Mesogastropoda: Ficidae) arecommonly found in the warm seas of the world(Feinberg 1979), yet little is known about thebiology of this relatively small family. Based onprevious studies, it is known that figsnails aremedium to large in size, lack an operculum, andhave a radula of the taenioglossan type. As far aswe are aware, there are 12 species in this family:Ficus ventricosa (Sowerby), F. gracilis (Sowerby),F. subintermedia (Orbigny), F. variegata Roding, F.carolae Clench, F. communis Roding, F. filosa(Sowerby), F. eospila (Peron-Lesueur), F. howelliClench and Farfante, F. atlanticus Clench andAguayo, F. investigatoris E.A. Smith (Abbott andDance 1983), and F. ficus Linnaeus (Lai 1987).Four species, i.e., F. ficus, F. gracilis, F. subintermedia,and F. filosa, have been recorded (Lai1987) from Taiwan with F. ficus the most commonspecies.Among the 12 species of Ficus, F. subintermediaand F. ficus are the best known. In F.subintermedia, Arakawa and Hayashi (1972)reported sexual dimorphism of the shell (female>male) and propodium (edges of propodium blunt infemale and hook-shaped in male). In F. ficus,Wang (1993a) observed that copulation and egglayingoften occurred at night to early morning inthe laboratory during the period of November toFebruary, and undigested polychaetes (Onuphissp. and Oiopatra sp.) were found in the stomach.Liu and Wang (1996) reported that F. ficus understress sheds a certain part of its mantle on the side*To whom correspondence and reprint requests should be addressed.

2 Zoological Studies 38(1): 1-6 (1999)of the inner lip as a special defensive mechanism.Regeneration of the autotomic tissue occurred inthe following week and reached a normal sizewithin 2 mo. The newly regenerated tissue is thin,membrane-like, and shows color changes fromtransparent white to white. Moreover, defensiveautotomy can not be induced in figsnails with newlyregenerated thin membrane-like tissues. Thus,based on the appearance and the size of theautotomic tissue, recently autotomized snails canbe easily recognized in the field.Figsnails can be caught in sandy or muddysubtidal habitats by bottom trawling (Lai 1987). InTaiwan, they are a common edible shellfish withlow economic value due to the toughness of theautotomic tissue. In general, people eat figsnailsafter removing the autotomic tissue. The figsnail isa bycatch of the shrimp fishery off the west coastof Taiwan and in the Taiwan Strait. Since they canbe caught in large numbers and the newlyregenerated tissue can be identified by size andappearance, we thought it feasible to study them,especially since mantle autotomy in mesogastropodsis uncommon. Therefore, studies onthe population dynamics and mantle autotomy of F.ficus were initiated.MATERIALS AND METHODSMonthly collections of F. ficus were madebetween May 1992 and June 1993 on the 5th, 6th,or 7th day of the month by bottom trawling off thecoast of Kaohsiung (120 01TE, 22°38'N). Trawlingwas made by fishing boat at depths of 30 to 40 mfor 40 min through a distance of about 30 km.During trawling, the autotomic behavior of F. ficusmight have been induced. Such autotomizedsnails could be recognized as those lackingautotomic tissue and by a wound mark on themantle. Based on the condition of autotomy, thecollected figsnails were sorted into autotomized(without autotomic tissue, i.e., portion of mantlehad been cast off during trawling) and intact (withautotomic tissue) groups. After the status ofautotomy was recorded, figsnails were separatedaccording to their sex: males are those with a vasdeferens and penis, and females are those with afemale opening and albumen gland. Then, shelllength, total body weight (after removal of shell),and autotomic tissue weight (if present) wererecorded. The percentage of autotomic tissuerelative to total body weight was determined as(autotomic tissue weight/total body weight) x 100%.I-tests were used to determine the sex ratioand the difference of shell length between the 2sexes (SAS 1985). The relationship between shelllength and percentage of autotomic tissue wasevaluated by linear regression analysis, andcovariance analysis was used to test for adifference between slopes of males and females.RESULTSA total of 2186 individuals was collected fromMay 1992 to June 1993. Autotomized figsnails,apparently induced by trawling, numbered 1574comprising 72% of the total samples, with the restbeing 612 intact individuals. A positive relationshipbetween shell length and body weight was found inF. ficus when autotomic tissue was excluded (y =1.900 - 0.106x + 0.001x 2 + 6.386E-5x 3 ; R 2 = 0.90;P < 0.01, N = 2186).The analyses of monthly size frequencyhistograms from May 1992 to June 1993 showedthat shell length of F. ficus ranged from 28 to 95mm (Fig. 1). Small individuals with shell lengths of< 35 mm were found only from July to September.Seasonal variation in abundance was alsoobserved: more than 200 figsnails were collectedfrom November to February, and fewer than 75individuals were collected from May to July.Sexual dimorphism in shell length, with femalesbeing significantly larger than males, was alsoobserved (Fig. 1; Table 1).Sex ratios deviating from 1:1 were common(Table 1), with female to male ratios ranging from0.3 to 2.3. In general, more females than maleswere found from March to September, with femaleto male ratios ranging from 0.9 to 2.3. However,from October to February, ratios changed to 0.3 to0.8 in favor of males.In the intact group (N = 612), the weight ofautotomic tissue ranged from 0.03 to 8.86 g, and itcomprised 0% to 34% of total body weight (Fig. 2).A distributional gap of between 2% to 5% wasobserved. Figsnails with autotomic tissue at < 1%of the total weight were recognized as havingrecently autotomized in the field. The autotomictissue was semitransparent white and small. Atotal of 19 figsnails occurred in monthly numbers ofo to 3.Because the newly regenerated autotomictissue was small, the tissue contributed very little(almost 0%) to total body weight. However, thismay have influenced the data analysis of therelationships between shell length and body

OL.-~e_aJ O"_'_....La ~---......~Liu and Wang - Population Dynamics and Autotomy of Ficus 314126 10a5 85- 6(j)u: 4214126 10May 1992N=49OL.-~~L.LO------"""~--'---~July 1992N = 73a5 8::Jrr 6~ 4 f2'OL.-' La.J......-LIILRJ ~50 r40 f6 Ia5 30::J~ 20u..101401206100c(j)::J 80cr~60u.. 402060506 40c~ 30cr(j) 20u:10oL.-~"~Aug, 1992N=216O~~-OLII----......~_L_..J"'___'_Sept. 1992N= 364Oct. 1992N= 166100 [80 l6 Ia5 60 r::Jcr 40 ~~ IJan, 1993N= 226Feb,1993N=318Mar, 1993N=93Apr. 1993N= 1721~ L,~ L~,20Iu.. 2:L ---. e----.~~120 r>. 100 f~ 80 r::J 60 rrr ,~ 40 fu..20 Io ~,~_=__' l. _2520>,oa5 15::J~ 10u.. 5o Lc __~~,_L.U50 -40>.oa5 30::Jg 20u:6 15c(j)5- 10~u.. 5~~,J~~~May 1993N=6680>.oa5 60::Jg 40u:10020L..._~Nov, 1992N=21510Ow-~---'--'WA..----..------~~~8>.oc 6(j)::Jg 4u:2June 1993N= 17100>. 80oa5 600~~---L.aJ..-a..._~~~Dec, 1992N= 211O~~~""'~~~'30 40 50 60 70 80 90 100Shell length (mm)::Jg 40u:200~~---"----....l.AJ--~~~30 40 50 60 70 80 90 100Shell length (mm)Fig. 1. Size-frequency histograms of Ficus ficus, Filled histograms: female; open histograms: male,

4 Zoological Studies 38( 1): 1-6 (1999)weight, and between shell length and percentageof autotomic tissue. Therefore, these 19 individualswere excluded in the following calculations,leaving 593 individuals (286 females and 307males) for further consideration. A positive relationshipbetween shell length and body weightwas found, i.e., y = 1.037x - 0.018x 2 + 1.722E-4x 3- 19.329; R 2 = 0.90; P < 0.01. The percentage ofautotomic tissue in males and females variedmonthly, but no trend could be determined (Fig. 3).Negative correlations between the percentage ofautotomic tissue and shell length were found inboth males and females. By covariance analysis,slopes of males and females showed no differences(p > 0.05). Therefore, males and femaleswere pooled to calculate the regression equation.A negative correlation between the percentage ofautotomic tissue and shell length was obtained,i.e., y =30.88 - 0.27x; R 2 =0.35; P < 0.01 (Fig. 4).DISCUSSIONAn unbalanced sex ratio in favor of females,following the seasonal cycle of copulation andspawning, has been reported for many gastropods,such as Buccinum undatum, Urosalpinx cinerea,and Eupleura caudata (Cole 1942, MacKenzie1961, Martel et al. 1986). A general migrationtowards the rocky substrata in shallower water foregg-laying and a return to the deeper soft substratafor food such as bivalves have been observed inB. undatum (Martel et al. 1986). It is assumed thatsuch migration serves to locate sites for eitherfavorable larval development or minimizingpredation. Thus, the varied sex ratios for F. ficusin our monthly samples (Table 1) would indicatethat egg-laying migration may exist. According toWang (1993a), the peaks of copulation and egglayingin F. ficus are from November to JanuaryTable 1.Mean shell length and sex ratio of Ficus ficusMonth N Sex Shell length (mm) i-test Sex ratio i-test(mean ± std) significance (F/M) significanceMay 92 34 F 54.9 ± 5.315 M 47.2 ± 3.5July 92 46 F 58.7 ± 11.027 M 51.8 ±6.5Aug. 92 133 F 61.9 ±8.383 M 51.6 ± 5.9Sept. 92 213 F 60.0 ± 11.9151 M 52.6 ± 6.2Oct. 92 59 F 60.9 ± 10.2107 M 54.0 ± 5.3Nov. 92 52 F 54.5 ± 6.3163 M 50.1 ± 3.8Dec. 92 62 F 56.5 ± 7.4149 M 52.3 ± 4.2Jan. 93 88 F 58.5 ± 8.1138 M 52.9 ± 4.3Feb. 93 138 F 63.6 ± 8.7180 M 54.9 ± 4.5Mar. 93 52 F 59.8 ± 8.141 M 52.7 ± 6.3Apr. 93 102 F 64.2 ± 8.970 M 52.1 ± 5.1May 93 45 F 63.4 ± 8.221 M 53.0 ± 4.7June 93 8 F 50.5 ± 2.39 M 50.0 ± 4.1F: female; M: male.p < 0.01 2.3 P < 0.05p < 0.01 1.7 p » 0.05p < 0.01 1.6 P < 0.01p < 0.01 1.4 P < 0.01p < 0.01 0.6 P < 0.01p < 0.01 0.3 P < 0.01p < 0.01 0.4 P < 0.01p < 0.01 0.6 P < 0.01p < 0.01 0.8 P < 0.05p < 0.01 1.3 p » 0.05p < 0.01 1.5 p < 0.05p < 0.01 2.1 P < 0.01p » 0.05 0.9 p » 0.05

Liu and Wang - Population Dynamics and Autotomy of Ficus 5and January to February, respectively. Laid eggcapsules are translucent-white and rectangular,about 0.5 to 1 cm long without a stalk (Fig. 5).Thus, our collection of fewer females during thereproductive season (October to February) wouldsignify that a copulated female F. ficus mightmigrate to sites with hard substrata to deposit itsegg capsules for firm attachment. Although few F.ficus individuals were observed between May andJuly (Fig. 1; Table 1), no explanation for thisphenomenon is available.Furthermore, figsnails smaller than 28 mmwere not collected in our sampling site. Similarly,bottom trawlings near our sampling site at depthsof 10 to 30 m did not reveal small individuals either(H.Y. Chen pers. comm., L.S. Feng pers. comm.).Certainly the habitat of juvenile figsnails must differfrom that of adults. However, it is unknown100 -whether the juvenile stays remains at the spawningground.We found a low incidence of figsnails (19individuals; see Fig. 2) with newly regeneratedtissue (indication of recent defensive autotomy inthe field) in our samples. According to the study byLiu and Wang (1996), the mantle tissue of F. ficusincreases in size and acts as a protective coverwhen the animal is under stress. If the stress isrelaxed, the mantle tissue is restored to its originalcondition. Otherwise, shedding of the autotomictissue occurs. In other words, if predatory pressureis not long-lasting and/or severe enough, defensiveautotomy may not be induced. Therefore, the lownumber of figsnails with newly regenerated tissuesmay indicate that predatory stress did not reach thelevel which evokes defensive autotomy during ourstudy period. If stress had induced defensiveautotomy, then many of the autotomized figsnailswould have died since they are more vulnerable topredation than intact snails. Another possibility isthat predation pressure of F. ficus might be low in80 -y = 30.88 - 0.27x; Ff = 0.35. P < 0.01N = 593a~ 40E ::>z._________o 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36Autotomic tissue (%)':11___.I,Fig. 2. Frequency histograms of the percentage of autotomictissue weight relative to total body weight in Ficus ficus.30i25 C. MaleN=59325~~ 20(lJ::>U'JU'J~ 15E.9~ 10

6 Zoological Studies 38(1): 1-6 (1999)natural environments. Although predation of F.ficus in the field is unknown, puffer fish and boxcrabs are known to attack live figsnails in thelaboratory (pers. observation). As puffer fish andbox crabs are rarely seen in the sampling area, itcan be concluded that predation pressure may below. Inasmuch as a complete regeneration of theautotomized tissue takes about 2 mo (Wang1993b), a possibility of rapid regeneration in oursamples is ruled outA negative correlation between the percentageof regenerated autotomic tissue and shell length inF. ficus (Fig. 4) indicates age-specific differences inthe growth of autotomic tissue. Older figsnails maynot expend as much energy for regenerating tissueas do younger snails. Older snails may allocate alarger portion of their energy for either reproductionor other somatic growth. However, further studiesare needed to test this hypothesisAcknowledgments: The authors would like tothank Mr. Y.W. Chiu for sample collection. Thisstudy was sponsored by the National ScienceCouncil of the Republic of China (NSC83-0209 司 B ­110-007).REFERENCESAbbott RT, SP Dance. 1983. Compendium of seashells. FLAmerican Malacologists , 411 ppArakawa KY, S Hayashi. 1972. On sexual dimorphism of figshell, Ficus subintθrm θdia. Venus 31: 63-71Cole HA. 1942. The American whelk ting 悔 , Urosalpinx ciner,θa(Say), on British oyster beds. J. Mar. BioI. Ass. UK 25:477-508Feinberg HS. 1979. Simon & Schuster's Guide to shells. NewYork: Simon and Schuste 人 512 ppLai KY. 1987. Marine gastropods of Taiwan (2). Taipei: TaiwanMuseum , 116 pp. (in Chinese).Liu LL, SP Wang. 1996. Mantle autotomy of Ficus ficus(Gastropoda: Ficidae). J. Mollus. Stud. 62: 390-392MacKenzie CL Jr. 1961. Growth and reproduction of the oysterdrill, Eupl,θura caudata in York River, Virginia. Ecology 42:317-338Martel A, DH Larrivee, JH Himmelman. 1986. Behavior andtiming of copulation and egg-laying in the neogastropodBuccinum undatum L. J. Exp. Mar. BioI. Ecol. 96: 2742.SAS. 1985. SAS User's Guide: statistics. 5th ed. NC: SASInstituteWang SP. 1993a. Reproduction of the Ficus ficus in Taiwan. JTaiwan Museum 39: 46-49. (in Chinese)Wang SP. 1993b. Autotomy in Ficus ficus. Master's thesis,National Sun Yat-sen University, Kaohsiung , Taiwan. 53pp. (in Chinese).花 球 批 把 螺 ( Ficus ficus) 之 族 群 動 態 與 自 割 研 究劉 莉 蓮 1 王 曉 萍 1花 球 批 把 螺 ( 月 'c u s ficus) 是 腹 足 綱 中 腹 足 目 的 員 , 具 有 自 劃 外 套 膜 的 防 禦 機 制 。 本 研 究 之 日 的 在 探 討 花 球批 把 螺 之 族 群 動 態 及 防 禦 性 自 割 在 野 外 之 變 化 們 自 1 9 9 2 年 5 月 至 1 9 9 3 年 6 月 , 每 個 月 收 集 高 雄 附 近 海 域 底 拖 之花 球 批 耙 螺 共 採 集 2 1 86 個 樣 品 , 殼 長 範 圍 介 能 2 8 - 9 5 mm 之 間 , 其 中 殼 長 小 監 35 mm 之 小 型 個 體 僅 在 7 至 9 月間 出 現 。 批 把 螺 豐 度 呈 現 季 節 性 變 化 , 其 中 1 1 至 2 月 數 量 較 多 , 在 5 至 7 月 間 族 群 數 量 較 其 它 月 份 低 , 個 體 數少 於 75 隻 。 雌 性 個 體 的 平 均 殼 長 大 民 雄 性 個 體 , 殼 長 有 性 雙 型 的 現 象 n 雌 雄 性 比 介 於 0 . 3 - 2.3 之 間 , 其 中 3 至9 月 間 雌 性 個 體 較 多 , 10 至 2 月 間 雄 性 個 體 較 多 , 顯 示 花 球 批 把 螺 可 能 有 產 卵 遷 移 行 為 c 花 球 批 把 螺 自 割 組 織的 重 量 介 民 0 . 0 3 - 8 . 8 6 9 之 間 , 占 個 體 總 重 的 0%-34% 們 殼 長 和 自 割 組 織 占 個 體 總 重 百 分 比 有 顯 著 的 負 相 閱(y = 30.88 - 0.27x; R 2 = 0.35; P < 0.01) 。 只 有 少 位 1% 之 樣 且 有 新 生 的 再 生 自 割 組 織 ( 顯 示 近 期 在 野 外 曾 有 防禦 性 自 害 。 發 生 ) , 在 每 個 月 樣 品 中 只 有 0 -3 重 個 體 。 本 結 果 顯 示 真 新 主 自 割 組 織 之 批 相 螺 可 能 較 易 遭 到 捕 食 或在 自 然 環 境 下 防 禦 性 自 割 可 能 很 少 發 生 。關 鍵 詞 : 花 球 批 吧 螺 , 批 + 巴 螺 , 族 群 動 態 , 自 割 。1 團 立 中 山 大 學 海 洋 生 物 研 究 所