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Assessment of the mating history of female pygmy octopuses and a possible sperm competition mechanism Department
of Biology,
JOHN A. CIGLIANO Boston University, 5 Curnrnington
Street, Boston, MA 023/S.
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(Received 21 July IYY4: initial ncceptonce 14 August IYY4, ,$nal acceplance 17 October 1994: MS. nwnhu: as-1081fci
Sperm precedence has been reported for a wide range of taxa with internal fertilization (see Smith 1984; Birkhead & Mnller 1992). For sperm precedence to occur, (1) females must be able to store viable sperm for an extended period of time, (2) there must be a delay between mating and fertilization, and (3) more than one male must mate with the female during the delay (Waage, 1984). Octopuses (Octopodidae: Octopus) meet all three criteria. Females store viable sperm in two oviducal glands for up to 10 months before laying eggs, there is a considerable delay between mating and egg laying, and females remain sexually receptive after mating (Mangold 1987). Moreover, males of some species exhibit prolonged copulation, transferring several to many spermatophores (Wells & Wells 1972; personal observation). This has been termed sperm loading and functions in some taxa as a sperm competition mechanism to flush out or dilute the sperm of previous males (Dickinson 1986; Birkhead & Hunter 1990). Because of the evidence suggesting that sperm precedence via sperm competition might be occurring in octopuses, I examined the mating behaviour of the pygmy octopus (Octopodidae: Octopus). I tested the prediction that if sperm competition is occurring, a male will modify his mating behaviour if he is mated to a recently mated female, as observed in other taxa (e.g. Corder0 1990). Specifically, the second male might transfer more sperm if sperm loading is occurring, OF show a greater latency of spermatophore transfer if he is manually displacing or removing previously deposited sperm (Birkhead & Hunter 1990). Male octopuses transfer spermatophores by placing the ligula, the tip of the hectocotylus 0003%3472/95/030849+03
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(modified third right arm), into the female’:. mantle cavity. After the oviduct is located. the ligula is inserted and a spermatophore is ejected through the funnel. The spermatophore is transported down the hectocotylus in the sperm groove to the oviduct opening (Wells & Wells 1971). The spermatophore then goes through a ‘spermatophoric reaction’ and free sperm are forced out (Mann et al. 1966). The pygmy octopus is a small (3040 g). benthic octopus found from the northern Gulf of Mexico, along the coast of Florida and in the northwestern Caribbean Sea (Hanlon 1983). It has been referred to incorrectly in the literature as Octopusjouhirzi and is currently undescribed (Forsythe & Toll 1991). The pygmy octopus was chosen because it meets the three criteria for sperm precedence and is one of the easier octopods to maintain in captivity (Hanlon 1983). Ten female and five male octopuses were collected from St Joseph Bay, Florida and shipped to Boston University, Boston, Massachusetts. I kept the octopuses in isolation for at least 1 week before the start of the experiment. Nine females mated with two different males on consecutive days (one re-mating attempt was unsuccessful). 1 chose males randomly to be either the first or second male to mate with that female. I concluded the experiment (1) after the pair completed mating (characterized by separating and moving away from each other) or (2) after 30 min had elapsed. If no mating occurred, 1 chose another male and placed it into the tank. This was repeated until the female had mated. I made all observations under red light to simulate night, because the pygmy octopus is nocturnal (Mather 1978). I recorded the following data by sitting 1 m from the tank and dictating observations into a
r 1995 The Association for the Study of Animal Behav~our 849
850
Animal
Behaviour,
microcassette recorder: duration of mating (from insertion of hectocotylus to completion), latency in spermatophore transfer (from insertion to transfer of first spermatophore), and number of spermatophores transferred. I analysed paired observations for each female (‘first male to mate’ and ‘second male to mate’) using the Wilcoxon matched-pairs signed-ranks test. A one-tailed test was used based on the hypothesis that, if sperm competition is occurring, the second male to mate would increase either the number of spermatophores transferred or the latency in spermatophore transfer. Mating duration was 180.11 rt 80.7 s (x* SE) and consisted of three distinct stages. During Stage I (59.78 & 15.9 s), intromission occurred but no spermatophores were transferred. Stage II (39.80 f 16.0 s) began with ‘arching’ and ‘pumping’ movements (Wells & Wells 1972) followed by spermatophores being transferred (1.67 f 0.4 spermatophores). Stage III (83.90 % 16.3 s) lasted until the completion of the mating. Stages I and III were similar in that the ligula was inserted but no spermatophores were transferred. Males mated longer when they were the second male to mate (103.67 f 13.0 versus 263.22 & 75.8 s; T=5.0, N=9, P=O.O2). This increasewas not becausesecond males transferred more spermatophores (2.10 f 0.4 versus 1.88 f 0.3; T= 13.0, N=9, NS) but becausethey more than doubled the duration of Stage I (34.67 * 7.3 versus 84.89 * 29.3 s; Tx7.0, N=9, P=OM). When males mated on consecutive days as a ‘second male’, mating durations did not differ (F, ,4= 0.04, P= 0.85: single classification ANOVA, data were log-transformed). Also, a male that mated as a ‘first’ male, then as a ‘second’ male on consecutivedays, decreased the duration of Stage I on the second day (52 versus 7 s). Becausemales that mated on consecutive days did not increase the duration of Stage I regardless of whether they were a ‘first’ or ‘second’ male, spermatophore depletion is an unlikely cause of the increase in Stage I. Second males also tended to increase the duration of Stage III (36.33 f 5.4 versus 13144 i 44.6 s; T=9.0, N=9, P=OO6). Male pygmy octopuses were able to determine the mating history of females, as indicated by the increase in mating duration when mating with recently mated females. Male octopuses possibly used the presence/absenceof sperm to determine whether females had recently mated. When a
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female pygmy octopus mated for the first time in this study, she previously had not mated for at least 1 week. It is likely that any remaining sperm had migrated to the oviducal glands and would be undetectable by the male. Recently mated females (within 24 h), would still have sperm in the distal oviduct because sperm takes at least 1 day to migrate from the distal oviducts to the oviducal gland (Jo11 1976). The sperm could therefore be detectable by males. Corder0 (1990) found that male damselflies, Ischnura graellsi, mated longer with non-virgins and suggested that males modified their behaviour because they were able to detect the presence of sperm. When females mate with multiple males, males are expected to modify their behaviour to ensure that their sperm fertilizes the majority of the female’s eggs (Parker 1970). The dramatic increase in mating duration reported here strongly suggests such a sperm competition function. Duration was not extended by increasing the number of spermatophores transferred (Stage II) as would be expected if sperm loading is occurring (Birkhead & Hunter 1990). ‘Second’ males, however, did more than double the duration of Stage I. This increase might occur because males are either removing or displacing previously deposited sperm from the female’s oviduct. Sperm removal is widespread among dragonflies (Siva-Jothy & Tsubaki 1989) and also occurs in damselflies (Waage 1986). The amount of sperm removed is related to the length of copulation (Corder0 & Miller 1992). Sperm displacement by repositioning previously deposited sperm has been observed in dragonflies, Crocothemis erythraea (Siva-Jothy 1984). Male pygmy octopuses place the ligula in the distal portion of the oviduct and so are in a position to manipulate previously deposited sperm. The ligula is ‘spoon’ shaped and may function to scoop out sperm instead of to place the spermatophore into the oviduct as has been traditionally thought. In conclusion, male pygmy octopuses seem to be able to assessthe mating history of a female. If the female has mated within 24 h, males increase the duration of Stage I, suggesting that they are removing or displacing previously deposited sperm. I thank Liza Bowman, Lauren Rader and Dr Fred Wasserman for their help during this study. I also thank Karen Cigliano for all her support.
Short Communications REFERENCES Birkhead, T. R. & Hunter, F. M. 1990. Mechanisms of sperm competition. Trends Ecol. Evol., 5, 48852. Birkhead, T. R. & Msller, A. P. 1992. Spernr Competition in Birds: Evolutionary Causes and Consequences. London: Academic Press. Cordero, A. 1990. The adaptive significance of the prolonged copulations of the damselfly, Ischnura gruellsi (Odonata: Coenagrionidae). Anim. Behav., 40, 4348. Cordero, A. & Miller, P. L. 1992. Sperm transfer, displacement and precedence in Ischnura graellsi (Odonata: Coenanrionidae). Behav. Ecol. Sociobiol.. j0, 261-267. Dickinson, J. L. 1986. Prolonged mating in the milkweek leaf beetle Labidomera clivicollis clivicollis (Coleoptera: Chrysomelidae): a test of the ‘spermloading’ hypothesis. Behav. Ecol. Sociobiol., 18, 331-338. Forsythe, J. W. & Toll, R. B. 1991. Clarification of the western Atlantic ocean pygmy octopus complex: the identity and life historv of Octouus ioubini (Ceuhalopoda: Octopodinae). Bull. mar. ‘Sci.: 49, 88-97: Hanlon, R. T. 1983. Octopus joubini. In: Cephalopod Life Cycles, Vol I (Ed. By P. R. Boyle). pp. 293-310. London: Academic Press. Joll, L. M. 1976. Mating, egg-laying and hatching of Octopus tetrirus (Mollusca:Cephalopoda) in the laboratory. Mar. Biol,, 36, 327-333. Mangold, K. 1987. Reproduction. In: Cephalopod Life Cycles, Vol II (Ed. by P. R. Boyle), pp. 157-200. London: Academic Press.
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