Mat ing behavior of the Atlantic bobta il squid Sepiola atlantica (Cephalopoda: Sepiolidae) M. Rodrigues, M. E. Garci, A. Guerra, J. S. Troncoso

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M. Rodrigues, M. E. Garci, A. Guerra, J. S. Troncoso. Mat ing behavior of the Atlantic bobta il squid Sepiola atlantica (Cephalopoda: Sepiolidae). Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 2009, pp.271-275. ￿hal-03253744￿

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Mating behavior of the Atlantic bobtail squid Sepiola atlantica (Cephalopoda: Sepiolidae)

M. Rodrigues 1*, M. E. Garci 2, A. Guerra 2, J. S. Troncoso 1 1 Departamento de Ecología y Biología Animal, Universidad de Vigo and Estación de Ciencias Marinas de Toralla (ECIMAT-UVIGO), 36331 Vigo, Pontevedra, Spain 2 Instituto de Investigaciones Marinas (CSIC, Vigo) * Corresponding author: [email protected]

Reproductive behavior ABSTRACT. – The mating behavioral pattern of the bobtail squid (Sepiola atlantica) was Mating Sepiola atlantica observed and described for the first time in laboratory conditions. A total of five matings were Cephalopods recorded. No courtship was noted in any of the mating events. In all the cases, the male moved quickly towards the female holding her by the middle of the ventral region of the mantle with his arms. The male, situated below the female, introduced his dorsal arms (the left dorsal arm is hectocotylized and passes the spermatophores) into the mantle cavity of the female, while grasp- ing her by the ventral region with his laterodorsal arms and by the neck with his lateroventral arms, sometimes introducing them into the female’s mantle cavity. The male showed the same pattern of coloration during the entire mating process, whereas the female changed slowly and successively her chromatic pattern. The duration of the mating varied between 68 and 80 min- utes. A comparison of the mating pattern of this species with other members of the family Sepi- olidae is made.

INTRODUCTION era Euprymna and Sepiola, “male to female neck”, seems to be a shared strategy in sepiolids (Moynihan 1983, Han- Mating in all cephalopod species consists of the male lon & Messenger 1996, Nabhitabhata et al. 2005) perhaps passing spermatophores to the female. The mating posi- linked to the position of the hectocotylus and the arrange- tion, the mode of transfer of spermatophores by the male ment of the bursa copulatrix (Norman 2000, Hoving et al. to the female and chromatic changes varies significantly 2008), a large pouch lying on the visceral mass that allows from species to species (Mangold 1987, Hanlon & Mes- the spermatangia to become attached. senger 1996). Knowledge of the mating behavior in mem- Until now, intraspecific differences in the way of copu- bers of the family Sepiolidae is scarce, perhaps due to the lating observed in other cephalopod groups (Mather 1978, nocturnal activity habits of many members of this family Hanlon & Messenger 1996 for a review) have not been (Shears 1988). Studying individual animals in small tanks noticed in any sepiolid species where this behavior has has its limitations for investigations of intraspecific rela- been studied, at least under laboratory conditions. tionships, both for the difficulty of reproducing natural Male cephalopods use various means to reduce compe- conditions in the laboratory, hindering us from determin- tition between their sperm and those of other males. One ing the “normal” mating behavior (Hanlon et al. 1997), of these is prolonged mating (Hanlon & Messenger 1996, and also for intraspecific differences, like those found in Hanlon et al. 1997). The duration of mating in sepiolids Octopus joubini (Mather 1978). varies greatly. For example, Moynihan (1983), Singley From laboratory observations, copulation was first (1983) and Hanlon et al. (1997) reported 25 minutes, reported in the family Sepiolidae for Sepiola rondeletii 45-80 minutes and 30-50 minutes for Euprymna scolopes and Rossia macrosoma by Racovitza (1894). Later it was respectively. Racovitza (1894) reported 8 minutes in described for other species of Sepiola, Sepietta and S. rondeletii, which is the only known mating time for this Euprymna (Mangold-Wirz 1963, Bergström & Summers genus. 1983, Boletzky 1983, Moynihan 1983, Singley 1983, Cephalopods have highly variable and complex life Hanlon et al. 1997, Nabhitabhata et al. 2005) but never history traits related to reproduction (Hanlon & Messen- for the bobtail squid Sepiola atlantica (d’Orbigny, 1839- ger 1996). Knowledge about the process and behavior of 1842). According to these authors, mating in sepiolids is bobtail squid species, with comparisons to other studied rather violent, completed in a short period of time and species, provides information for understanding the evo- without an initial courtship. However, Norman (2000) lution of mating behavior. Biology and ecology of the suggested the existence of courtship behavior in wild small bobtail squid S. atlantica is poorly known, and its Euprymna tasmanica. reproductive behavior has not been investigated (Guerra The copulatory position observed in species of the gen- 1986, 1992, Yau & Boyle 1996, Reid & Jereb 2005). The 272 M. Rodrigues, M. E.Garci, A. Guerra, J. S. Troncoso aim of the present study was to describe for the first time After mating occurred, the specimens were separated and the mating pattern for this species. maintained in captivity until their natural death, which occurred within a period of 2 to 30 days. Upon death, the sex was con- firmed and specimens were immediately measured: dorsal man- MATERIAL AND METHODS tle length (ML) and total length (TL) to the nearest 0.1 mm; total body weight (BW) to the nearest 0.01 g. In March 2007, ten adult specimens were obtained in two dives from the Ría of Vigo (NW Iberian Peninsula): eight indi- viduals off Area Milla (42º14’ N; 8º47’ W) and two individuals RESULTS off Toralla Island (42º12’ N; 8º47’ W). Depth of collection ranged from 5 to 6 meters and the seabed was sandy without External measurements and sex of the ten specimens seaweed. used in the study are shown in Table I. All males showed Immediately after being collected the specimens were trans- the hectocotylus as the dorsal left arm. All females ported to the Marine Station of the University of Vigo in Toralla showed a bursa copulatrix within the mantle cavity on Island. Each individual was placed in a 10.2 liters tanks (30 cm their left side. long x 18 cm wide x 19 cm deep) with an open sea water circu- In all matings observed in this study, after entering the lation system. All observations were made after ten days to specimens into the tank, they immediately went to the ensure acclimatization of the animals to captivity. After accli- bottom substrate and acquired a dark pattern. After a mean mation, specimens were paired together and transferred at the time of 47.6 min. ± 23.27 the females started swimming. same time to 20.2 liters tanks (30 cm long x 27 cm wide x 25 cm The copulatory position “male to female neck” was deep) on the same open sea water circulation system. Water tem- consistent in the five mating events observed. The subse- perature ranged between 14-17 ºC. The system received natural quent response of the male specimens to the female swim- photoperiod of 12:12 LD. The bottom of the tank was covered ming was immediate (mean 36.2 sec. ± 6.80) during all with a 2-3 cm layer of fine sand taken from the same location five mating episodes in the laboratory, four occurred dur- where the specimens were collected. Squid were fed daily ad ing daylight and one at night. libitum with mysid shrimp Siriella armata. No type of behavior that we could classify as male After consideration of small differences observed between courtship was noted in any of the mating events. The male sexes, mainly the relative size, position and coloration of the left the bottom of the tank and moved quickly toward the gonad, five couples were formed. These differences are easily female and initiated physical contact. When approached, observed through the musculature of the mantle when the chro- the female showed a general pale and translucent color- matophores are contracted. In females, the gonad is translucent ation, having only small points (non expanded chromato- orange and visible in the middle of the dorsal side of the mantle, phores) dark-brown in color, while the male showed a whereas the male gonad is in the dorsal posterior region of the cream-yellowish background with strong dark coloration mantle, opaque-white and smaller. Additionally, the posterior produced by a mosaic of expanded brown chromato- area of the female’s mantle is broadly rounded while it is more phores. Using all arms, the male initially grasped the angular in the male (cf. Singley 1983). The mating process was female in the middle ventral region of the mantle (Fig. 1a), photographed (Nikon D200 camera, lens Mikkor 60 mm), and then shifted his grasp to the female’s neck. During the filmed (Sony PD-170 with increase, 4x). The duration of the process, the male showed a different chromatic pattern mating was defined as the time elapsed from the first moment in than the female, with the chromatophores being more which the male and the female were in physical contact until expanded than those of the female, the latter producing a they separated. During observations, human interaction was general pale coloration (Fig. 1a). As a general rule, the minimized through the use of visual barriers on the experimen- male kept the same color during the mating process, tal system. whereas the female slowly and successively changed her

Table I. – Sepiola atlantica. Data of the ten specimens used in this study. Dorsal mantle length (ML) mm, total length (TL) mm, total body weight (BW) g, duration in minutes and time of individual survival after mating in days. Female Male Mating bouts Survival after mating Couples ML TL BW ML TL BW Duration Male Female 1 14.1 33.6 1.67 13.5 36.2 1.25 68 8 22 2 16.7 40.7 1.94 14.3 38.0 1.83 76 9 30 3 17.7 41.5 2.03 14.5 38.7 2.19 80 2 2 4 15.2 39.4 1.52 12.9 33.6 2.03 74 7 8 5 14.5 36.2 1.84 14.7 35.8 1.96 71 29 27

Vie Milieu, 2009, 59 (3-4) MATING BEHAVIOR OF SEPIOLA ATLANTICA 273

Fig. 1. – Copulation pattern in Sepiola atlantica: a, The male moves quickly toward the female, then holds her with his arms by the middle ventral region of the mantle. b, The male, situated below the female, introduces his pair of dorsal arms in the mantle cavity of the female. c, d, The male shows a darker color pattern than the female during the fertilization process. e, The male has a constant dark color pattern affecting the whole body; the female showing her head with contracted chromatophores and quite visible iridophores (green metallic color) around the eye-balls and the arms have a pink background. f, Before separating, the male is in a horizontal posi- tion at the bottom, while the female maintains her tilted position with the top of her mantle towards the surface of the tank. She remains gripped by the male’s arms. g, The female displays a white coloration before they separate. Scale bars: a, b, c, d, f, g, 10 mm; e, 5 mm.

chromatophoric pattern. below the female on the bottom of the tank, introduced The male then pulled the female down to the bottom of his dorsal arms carrying spermatophores in the mantle the tank, where copulation took place. The male, situated cavity of the female, while grasping her by the ventral

Vie Milieu, 2009, 59 (3-4) 274 M. Rodrigues, M. E.Garci, A. Guerra, J. S. Troncoso region with his laterodorsal arms and the neck with his in E. hyllebergi (Nabhitabhata et al. 2005). Such a scenar- lateroventral pair, sometimes introducing them into the io would allow female S. atlantica to choose whether or mantle cavity of the female. During this process the not to swim in the presence of a male (as a way of accept- female remained with her arms placed on the bottom of ing copulation). Although the male starts the physical the tank and with her posterior tip pointing upwards and contact, in our opinion it is the female who initiates mat- elevated from the bottom (Fig. 1c). The ventral arms were ing. Unfortunately, we could not uncover the cues that not used during mating. During the passing of the sper- males and females of S. atlantica respond to in order to matophores, a similar pattern of dark coloration was initiate copulation. observed in both sexes (Fig. 1b, c) with both specimens The only evidence of male courtship in the family Sep- lying down on the bottom (Fig. 1c, d). However, this color iolidae was recorded by Norman (2000) in wild E. tas- pattern changed in the female and she was observed with manica. The lack of male courtship behavior found in the contracted chromatophores on her head, prominent irido- present study could be due to the limited space in the phores (green metallic color) around the eye-balls and her experimental tanks, it may have changed S. atlantica’s arms had a pink background where some red, non expand- behavior as recorded in Sepia officinalis (Adamo et al. ed chromatophores were visible (Fig. 1e). 2000). However, from laboratory observations, absence The male was situated in a horizontal position on the of courtship, copulatory position, duration of mating and bottom of the tank before individuals separated. During spermatophore placement of S. atlantica matches with this phase, the female maintained her tilted position, with those observed in the sepiolid E. scolopes (Moynihan the top of her mantle towards the surface of the tank and 1983, Singley 1983, Hanlon et al. 1997). The mating pat- still gripped by the male’s arms (Fig. 1f). The female dis- tern also coincides with those observed in S. rondeletii played a general pale coloration with very few expanded (Racovitza 1894), Sepiola robusta (Boletzky 1983) and chromatophores, while the color pattern of the male did E. hyllebergi (Nabhitabhata et al. 2005) except for the not change significantly in relation to previous phases mating duration, which was much longer in S. atlantica (Fig. 1g). than in the other three species (68-80 minutes versus 7-10 The mean duration of mating was 73.8 min. ± 4.60 minutes). Rossia macrosoma also showed a male to (Table I). After the couple separated, if the male tried to female neck position during mating (Mangold-Wirz 1963, approach the female again she swam away. Racovitza 1894). A more detailed comparison with After mating the animals did not fast. Females survived S. atlantica is not possible because of the lack of informa- between 2 and 30 days (Table I) and males between 2 and tion on mating duration and spermatophore placement in 29 days (Table I). The females died without laying eggs. R. macrosoma. Instead of a male to female neck arrange- ment during mating, Rossia pacifica showed a male par- allel position (Brocco 1971, Summers 1985). Additional- DISCUSSION ly, in another sepiolid where mating is known, Sepietta oweniana, the mating position is “head to head” and its According to laboratory observations, males of duration is shorter than in S. atlantica (Bergstrom & Sum- Euprymna hyllebergi always started the physical contact mers 1983). with the female leaving the bottom as observed in There is still little evidence for sperm competition in S. atlantica (Nabhitabhata et al. 2005, present paper). bobtail squids although some observations strongly sup- Nabhitabhata et al. (2005) also observed that E. hylleber- port its occurrence. Thus, the long mating times observed gi males always held the females using their laterodorsal, in E. scolopes and in S. atlantica combined with the pres- lateroventral and ventral arms. However, in our observa- ence of an internal seminal receptacle, strongly suggest tions of S. atlantica, the ventral arms were used only in the possibility of sperm competition among males (Han- the first moments of grasping the female and not during lon et al. 1997). The short duration of mating observed in mating. In E. hyllebergi, mating behavior was divided by several species of bobtail squids seems to be in disagree- the authors into five stages: a) female hovers by, male ment with the existence of sperm competition, where one attention; b) male approaches female from below; c) male mating of a long duration seems to be needed. Neverthe- grasps female by mantle; d) male-grasp moves to female’s less, sperm competition is possible even when the dura- neck; e) male pulls female down to substrate (Nabhitab- tion of copulation is short, and a long mating time could hata et al. 2005). These five stages also apply in S. atlan- be linked to other processes such as mate guarding or tica. However, as mentioned above, mating in S. atlantica capacity sperm transfer (Linn et al. 2007). was different than in E. hyllebergi because the ventral Moynihan (1983) is the only author that describes the arms of the former species were not functional in the mat- color changes that occur during mating in the family Sep- ing act. iolidae when he studied the Hawaiian bobtail squid Who initiates the mating, the male or the female? In E. scolopes. Based only on the coloration pattern of Sepia the present study, the female always swam before the latimanus during mating, this author inferred that the male until he “paid attention”. This behavior was similar E. scolopes individual at the bottom was the female, while

Vie Milieu, 2009, 59 (3-4) MATING BEHAVIOR OF SEPIOLA ATLANTICA 275 the one located on top was the male. However, this Brocco SL 1971. Aspects of the biology of the sepiolid squid assumption was never investigated further. According to Rossia pacifica Berry. MA Thesis, Univ Victoria, BC Cana- this author, the first individual showed a fine reticulation da, 151 p. of dark brown marks on a cream or light yellow back- Guerra A 1986. Sepiolinae (Mollusca, Cephalopoda) de la Ría de Vigo. Iberus 6: 175-184. ground throughout and even after copulation. Additional- Guerra A 1992. Mollusca, Cephalopoda. In Ramos MA ed, ly, the animal on top slowly and successively changed its Fauna Ibèrica I, Museo Nacional de Ciencias Naturales chromatic pattern. Considering these descriptions, the CSIC, Madrid, 327 p. observation on the respective sex of the mating specimens Hanlon RT, Claes MF, Ashcraft SE, Dunlap PV 1997. Laborato- of E. scolopes by Moynihan (1983) is wrong as shown by ry culture of the Sepiolid squid Euprymna scolopes: A model Singley (1983) and Hanlon et al. (1997), where the mat- system for bacteria-animal symbiosis. Biol Bull 192: 364- ing position of both males and females of the Hawaiian 374. bobtail and the Atlantic bobtail squid are the same (‘male Hanlon RT, Messenger JB 1996. Cephalopod behavior. Cam- to female neck’), and the chromatic pattern similar. Nabh- bridge University Press, United Kingdom, 232 p. itabhata et al. (2005) reported that the color pattern of Hoving HJT, Laptikhovsky V, Piatkowski U, Önsoy B 2008. Reproduction in Hetoroteuthis dispar (Rüppell, 1844) (Mol- male E. hyllebergi during mating was a dark brown color, lusca: Cephalopoda): A sepiolid reproductive adaptation to while the female showed a pale brown coloration during an oceanic lifestyle. Mar Biol 154(2): 219-230. the mating bouts. Linn CD, Molina Y, Difatta J, Christenson TE 2007. The adap- Due to the possibility of sperm storage from a previous tive advantage of prolonged mating: A test of alternative mating (Boletzky 1983, Hanlon & Messenger 1996) we hypotheses. Anim Behav 74(3): 481-485. can not be certain that the spermatophores found in the Mangold-Wirz K 1963. Biologie des céphalopodes benthiques bursa copulatrix were transferred by the male to the et nectoniques de la mer Catalane. Vie Milieu 13(Suppl): female during the mating. However, it is known that 1-285. males transfer spermatophores with their hectocotylized Mangold K 1987. Reproduction. In Boyle PR ed, Cephalopod Life Cycles II, Academic Press London: 157-200. arms, hence, genuine mating occurred in all cases in the Mather JA 1978. Mating behavior of Octopus joubini Robson. present study. Veliger 21: 265-267. In conclusion, the information we obtained has allowed Moynihan M 1983. Notes on the behavior of Euprymna scol- us to describe for the first time the mating behavior of opes (Cephalopoda: Sepiolidae). Behavior 85: 42-57. S. atlantica. In general, our observations coincide with Nabhitabhata J, Nilaphat P, Promboon P, Jaroongpattananon C those on other sepiolid species; mating consists of five 2005. Life cycle of cultured bobtail squid, Euprymna hylle- stages, and a possible female pre-copulatory behavior was bergi Nateewathana, 1997. Phuket Mar Biol Cent Res Bull observed. Each stage triggered a display of color changes 66: 351-365. unique to this species. However, further data are needed Norman K 2000. Cephalopods: a World Guide. ConchBooks, to reach conclusions about the function of the long mating Hackenheim, 318 p. duration observed in S. atlantica. Racovitza EG 1894. Sur l’accouplement de quelques Céphalo- podes Sepiola rondeletii (Leach), Rossia macrosoma (d Ch) Acknowledgements . – The valuable help and the fruitful et Octopus vulgaris (Lam). C R Acad Sci D Nat 118: 722- discussions with A F González, S Pascual & A Roura (ECO- 724. BIOMAR, Instituto de Investigaciones Marinas, CSIC) and Reid A, Jereb P 2005. Family Sepiolidae. In Jereb P, Roper CFE F Rocha (University of Vigo) are greatly appreciated. Cristian eds, Cephalopods of the World. An Annotated and Illustrated Aldea of Department of Ecology and Animal Biology (Univer- Catalogue of Species known to date. I, Chambered Nautilus- sity of Vigo) and Foundation CEQUA (Chile) is thanked for his es and Sepioids (Nautilidae, Sepiidae, Sepiolidae, Sepiadarii- help with the software used in this manuscript. We also thank dae, Idiosepiidae and Spirulidae), FAO Species Catalogue F Read for her help with the English. The first author was sup- for Fishery Purposes, Rome: 4, 153-203. ported by a scholarship from the Secretaría Xeral de Inmigra- Shears J 1988. The use of a sand-coat in relation to feeding and ción de la Xunta de Galicia. diel activity in the sepiolid squid Euprymna scolopes. Mala- cologia 29: 121-33. Singley CT 1983. Euprymna scolopes. In Boyle PR ed, Cephalo- pod Life Cycles I, Academic Press, London: 69-74. REFERENCES Summers WC 1985. Comparative life history adaptations of some myopsid and sepiolid squids. North Atl Fish Organ Sci Adamo SA, Brown WM, King AJ, Mather DL, Mather JA, Counc Stud 9: 139-142. Shoemaker KL, Wood JB 2000. Agonistic and reproductive Yau C, Boyle PR 1996. Ecology of Sepiola atlantica (Mollusca: behaviours of the cuttlefish Sepia officinalis in a semi-natural Cephalopoda) in the shallow sublitoral. J Mar Biol Ass UK environment. J Mollus Stud 66: 417-419. 76: 733-48. Bergström B, Summers WC 1983. Sepietta oweniana. In Boyle PR ed, Cephalopod Life Cycles I, Academic Press, London: 75-91. Received March 18, 2009 Boletzky Sv 1983. Sepiola robusta. In Boyle PR ed, Cephalo- Accepted July 08, 2009 pod Life Cycles I, Academic Press, London: 31-52. Associate Editor: Sv Boletzky

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