Mating Behavior of Abdopus Aculeatus (D’Orbigny 1834) (Cephalopoda: Octopodidae) in the Wild

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Mating Behavior of Abdopus Aculeatus (D’Orbigny 1834) (Cephalopoda: Octopodidae) in the Wild Mar Biol DOI 10.1007/s00227-008-0930-2 RESEARCH ARTICLE Mating behavior of Abdopus aculeatus (d’Orbigny 1834) (Cephalopoda: Octopodidae) in the wild Christine L. HuVard · Roy L. Caldwell · Farnis Boneka Received: 1 March 2007 / Accepted: 8 February 2008 © Springer-Verlag 2008 Abstract The mating system of Abdopus aculeatus incor- than did #T, while $GA spent more than twice as much time porates sneaker matings, mate guarding, sex-speciWc body per day in copula than did other females. Sneaker copula- patterns, frequent copulations, and male–male competition tions lasted longer than those by males adopting other tactics. for mates, making it more similar to that of aggregating deca- Mate-guarding was an eVective and important tactic used by pod cephalopods than any previously known octopus social males to temporarily monopolize mating with apparently system. Large male–female A. aculeatus occupy ‘Adjacent’ non-selective females. Males demonstrated clear pre-copula- (GA) dens and copulate frequently in mate-guarding situa- tory mate choice by guarding and mating repeatedly with tions over successive days. Nearby individuals copulate in large females (typically $GA). While foraging alone away ‘Temporary guarding’ (GT) and ‘Transient’ (T; non-guard- from the den, #G procured ‘Transient’ copulations with ing) situations, the latter of which can involve ‘Sneaker’ (S) unguarded females. However, mate-guarding reduced the mating. In a focal animal study of these octopuses in the wild amount of time #G were alone and may impede their ability (Sulawesi, Indonesia) we addressed the hypotheses that they to seek out new mates. Low-copulation rates by $T, the demonstrate: (1) precopulatory mate choice, (2) diVerential smallest female tactic on average, may reXect this trade-oV copulation rates by individuals employing diVerent mating between mate preference and mate-searching by males, or tactics, and (3) distant sex identiWcation. We quantiWed daily non-receptivity of some females. A male-typical body pat- copulation rates of A. aculeatus of reproductive size as well tern (black and white stripes) appeared to facilitate distant as aspects of copulation duration, display, mate-competition, sex identiWcation. Although mating and aggression were and mate rejection. Mating tactic correlated with daily copu- often initiated before contact between individuals, same-sex W lation rates. #GA spent signi cantly more time copulating copulations and intense male–female aggression were rare. By contrast frequent male–female copulations and intense Communicated by P. Kraufvelin. male–male aggression were consistent behavioral compo- nents of mating in A. aculeatus at these sites. Because the Electronic supplementary material The online version of this behavioral and ecological characters conducive to this com- article (doi:10.1007/s00227-008-0930-2) contains supplementary plex system are not exclusive to A. aculeatus, it is possible material, which is available to authorized users. that other octopuses exhibit some or all of these behaviors. C. L. HuVard · R. L. Caldwell Department of Integrative Biology, University of California, Berkeley, CA 94720-3140, USA Introduction C. L. HuVard (&) Monterey Bay Aquarium Research Institute, 7700 Sandholdt Aided by a well-developed nervous system (Young 1971; Road, Moss Landing, CA 95039-9644, USA Williamson and Chrachri 2004) shallow-water octopodids e-mail: [email protected] (hereafter referred to as ‘octopuses’) can be highly visual animals capable of learning and problem-solving (Hochner F. Boneka Department of Fisheries and Marine Science, et al. 2006). By contrast, one of the most important acts Universitas Sam Ratulangi, Manado, North Sulawesi, Indonesia of an octopus’s life, mating, has been generalized as 123 Mar Biol opportunistic, indiscriminate, and almost completely devoid have not been performed in ways that would address these of complex behavior (Hanlon and Messenger 1996). Despite topics speciWcally. These limited and isolated observations the visual nature of these animals and the presence of sexu- exemplify the need for detailed in situ comparisons of the ally dimorphic traits in many species, conclusive evidence mating behaviors by multiple individuals. for the use of courtship and distant sex identiWcation has Abdopus aculeatus (d’Orbigny 1834) is a diurnal inter- not been presented [Wells and Wells 1972; Voight 1991; tidal species that may demonstrate the most complex mat- Cheng 1996; Cheng and Caldwell 2000; we consider court- ing behaviors observed thus far for any octopus species. ship to be “behaviors that coordinate the activities of (sex- Despite their small size [to 7 cm mantle length (ML)] and ual) partners in time; orient (sexual) partners in space; and excellent camouXage, individuals are easy to locate and fol- increase sexual motivation” Tinbergen 1953]. Mate guard- low in the wild for extended periods. During preliminary ing and mate competition are forms of resource defense in observations in Sulawesi, Indonesia, males appeared to which “animals keep others away from resources by Wght- exhibit mate guarding, sneaker matings, and aggressive ing or aggressive displays” (Krebs and Davies 1993). These contests during which they fought over mates (HuVard have not been documented for octopuses even under cir- 2007). Large males and females occupied adjacent dens cumstances in which they might be expected, such as when [deWned as such if the male could extend his hectocotylus populations are very dense (Aronson 1989) or in what are (mating arm) to the female’s den while resting at his own] considered rare cases when multiple males simultaneously for up to a week and copulated repeatedly both at the dens have tried to copulate with a single female (Ambrose in and on the foraging bouts (Fig. 1a, Supplementary Videos Hanlon and Messenger 1996). These views regarding a 1, 2). These observations suggest the possibility that mating simple mating system in octopuses are supported by labora- by A. aculeatus involves (1) precopulatory mate choice, (2) tory studies and brief Weld anecdotes on more than a dozen diVerential copulation rates by individuals employing diVer- species (Cheng 1996; reviewed in Hanlon and Messenger ent mating tactics, and (3) distant sex identiWcation, features 1996; Cheng and Caldwell 2000), but remain to be tested that are common in other behaviorally complex animals by any in-depth study in the wild. (Andersson 1994). To quantify behaviors and address these Of the octopuses for which mating behavior has been hypotheses, two substantial local populations were identi- documented, nearly one-third demonstrate behaviors that Wed where individuals could be recognized by arm injuries suggest a more complex mating system than that accommo- and scars (as with Octopus cyanea and Octopus briareus in dated in current views. Male and female Octopus cyanea Yarnall 1969 and Aronson 1989, respectively), and den form dens adjacent to each other during the mating season Wdelity allowed individuals to be relocated. These attributes (Yarnall 1969; Norman 1992) and a single example of allowed for the Wrst long-term (hours to days) observations sneaker mating has been reported for this species in the of interactions among known octopuses in the wild. wild (Tsuchiya and Uzu 1997) suggesting the potential for repeated interactions, alternative reproductive tactics, and male–male mate competition. Male mating displays have Methods been described for Octopus digueti (Voight 1991), O. cya- nea (Wells and Wells 1972; Tsuchiya and Uzu 1997), Behavioral categories Octopus vulgaris (Wells and Wells 1972), and an unidenti- Wed member of Abdopus (Young 1962). Although all of Based on preliminary observations of mating behavior, these behaviors have the potential to inXuence competition, male (#) and female ($) octopuses were categorized as W sex identi cation, mate choice, and/or courtship, studies ‘Adjacent Guarding’ (GA), ‘Temporarily Guarding’ (GT), Fig. 1 a Adjacent Guarding (GA) male and female mating at their dens. Note raised supra- ocular papilla and ‘BWS’ body pattern in male. Drawn from frame of video. b Male Sitting Tall at den while exhibiting BWS and exposing oral portion of lateral and ventral arms. Drawn from Weld notes 123 Mar Biol Table 1 Behavioral categories of mating Abdopus aculeatus in Sulawesi, Indonesia Mating tactic DeWnition ‘Adjacent A male–female pair that occupied a den within arm’s reach of each other. This pair copulated in mate-guarding Guarding’ (GA) situations both at their dens and while out foraging. ‘Temporarily A male–female pair occupying dens not adjacent to each other, that temporarily entered into a guarding situation. Guarding’ (GT) ‘Transient’ (T) Any octopus that was not observed in a guarding situation. When observed to mate Transient individuals parted after Wnal withdrawal of the hectocotylus. These included both Sneaker and Non-Sneaker males. ‘Sneaker’ (S) Males that visually segregated themselves from guarding males to avoid aggression while mating with the guarded female. Sneaker males were a type of Transient male. Table 2 Acronyms for behavioral categories used throughout the text necessary to identify injuries and measure the mantle length of animals, octopuses were caught with a dip net and han- Reproductive tactic Male Female dled brieXy in situ with cloth gloves. Males as small as ‘Adjacent Guarding/Guarded’ #GA $GA 19 mm ML were easily identiWed by the presence of an ‘Temporarily Guarding/Guarded’ #GT $GT unpigmented groove along the ventral
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