Sexual behavior in the common cuttlefish, Sepia officinalis L.
Bethany L. Lloyd
School of Ocean Sciences
University of Wales, Bangor
Contents page
Introduction 3
1. Overview of Sepia officinalis 3-5
2. Sexual Selection Theory 5-7
3. Sexual Behavior of Sepia officinalis
3.1 Visual Displays 7-10
3.2 Chemical Cues in Communication and Social Interaction 10-15
3.3 Copulation 15-21
4. Laboratory versus Field Observations 21-23
Conclusions 23-24
References 25-28
Introduction
The class Cephalopoda first emerged during the Cambrian period and includes around 700 species of squid, octopus, cuttlefish and the nautilus. Cephalopods are considered to be the most intelligent and highly evolved of the invertebrates, with extremely large brains in relation to their bodies compared to their invertebrate relatives and even to vertebrates such as fish and reptiles (Hanlon and Messenger, 1996). Their range of complex behaviours are more comparable to those of fish than to those of the simpler bivalves, gastropods and other molluscs to which they are more closely related (Packard, 1972). These behaviors, including colour-changing and body-patterning abilities, defense, reproduction, intraspecies communication and learning have been reviewed by Hanlon and Messenger (1996) in their comprehensive book Cephalopod Behaviour. However, this review will concentrate on one aspect of behavior – reproductive behavior – in one representative of the cephalopods, the common cuttlefish Sepia officinalis Linnaeus 1758, in anticipation of a research project intended to observe sexually selective behaviors regarding male and female mate choices, intrasexual competition between males for females, opportunity for sperm competition and resulting reproductive success.
1. Overview of Sepia officinalis
S. officinalis has become a baseline subject in cephalopod research, something of a white mouse or the Drosophilia of laboratory-based behavioral and neurobiological research due to its hardiness in artificial tank environments, short life cycles, fast growth and high food conversion efficiencies, and resistance to disease (Domingues et al, 2001). Despite the usual heavy demand for large amounts of live food necessary for culture of most cephalopods, cuttlefish husbandry is comparatively simple for S. officinalis than for many other cephalopod species and high survival rates can be accomplished (Forsythe et al, 1994). S. officinalis has a wide distribution and is found throughout the eastern Atlantic Ocean including the North Sea, the English Channel and along the west coast of Africa, as well as the Mediterranean and Aegean Seas (Önsoy and Salman, 2005). It was one of the first cephalopods to be described in terms of its behavior (Aristotle, 1991) and its reproductive habits are among the most often studied and best understood among the cephalopods (Tinbergen, 1939; Boletsky, 1983; Hanlon and Messenger, 1996; Boal, 1996 and 1997; Boal and Marsh, 1998; Hanlon et al, 1999; Adamo et al, 2000). However, most of these studies have been performed under laboratory conditions and may or may not reflect behavior under natural conditions. The implications of this will be discussed later.
Sexual dimorphism is apparent in S. officinalis only for adult animals. Sexually dimorphic characters include body patterns and size; adult males maintain higher growth rates than females and will achieve larger maximum sizes (Boletzky, 1983). The maximum size for males over a two-year growth period is 300mm in mantle length (ML), although 150-220mm in ML is average for both sexes under laboratory conditions (Forsythe et al, 1994). Sexual maturity may occur when males are from 114-170mm in ML; females generally become sexually mature between 142-230mm in ML (Dunn, 1999), although mature females have been observed under laboratory conditions at 90mm ML (Önsoy and Salman, 2005). Differences in size at maturity are suggested to result from temperature differences; Boletzky (1987) found that S. officinalis in warmer waters matured earlier than those living in colder waters. S. officinalis cultured at warmer temperatures also have increased feeding and growth rates (Domingues et al, 2001). The lifespan of S. officinalis varies from 6 months to 2 years (Boletzky, 1987; Gauvrit et al, 1997; Domingues et al, 2001) and reproduction may take place after one year in warm waters and after two years in colder waters (Gauvrit et al, 1997).
Spawning in S. officinalis is often intermittent and monocyclic, with egg-laying occurring in separate batches over the spawning period, which may continue for up to 4 months in captivity before death of the female (Boletzky, 1987; Rocha et al, 2001), comprising up to 1/3 of the life cycle (Boletzky, 1987). One S. officinalis female was shown to spawn intermittently for 7 months (Boletzky, 1988 as cited in Rocha et al, 2001), but this has yet to be replicated. Although the intermittent terminal spawning pattern has been observed in the wild (Laptikhovsky et al, 2003), long-term spawning, although possible in cultured S. officinalis, has not been observed in the wild and whether or not such a strategy is employed under certain environmental conditions remains uncertain. Other female S. officinalis spawn only once before dying (Boletzky, 1987), and this is often the case with wild S. officinalis in the colder waters of the English Channel (Gauvrit et al, 1997). A key characteristic of intermittent terminal spawning is the lack of any somatic growth of the animal between spawning events (Rocha et al, 2001). Reproduction in S. officinalis can occur throughout the year but seasonal peaks of mature and reproducing animals from spring (March) to mid-summer (June) have been described in S. officinalis in the Aegean Sea (Önsoy and Salman, 2005). In the English Channel, S. officinalis is known to spawn from February to July (Dunn, 1999). Similar spawning periods, from mid-March to June, have been reported for the Bay of Biscay (Gauvrit et al, 1997). Eggs hatch from July to September (Dunn, 1999), and higher temperatures have been shown to accelerate hatching (Boletzky, 1983). Mortality of both males and females occurs shortly after spawning. Ovarian growth in females, furthermore, is dependent on length of photoperiod (Gauvrit et al, 1997). Eggs are laid in grape-like clusters, each egg from 6-9mm in diameter with larger eggs produced by larger females (Boletzky, 1983). Fecundity has been studied in the Aegean Sea (Laptikhovsky et al, 2003), where females from 94-247mm in ML produced between 130-839 mature and ovulated eggs, with numbers of eggs increasing with body weight of the animal. The same study cited potential fecundity of 1,000-3,000 eggs per female, which is in accordance with the fecundity of 3,000 eggs per female reported by Forsythe et al (1994) in their study of cultured S. officinalis displaying intermittent spawning.
Sex ratios in wild populations have been poorly documented, with varying reports of 1:1 (Pinczon du Sel and Daguzan, 1997) and 1:3 male:female (Showers, 1991). Until more accurate information regarding sex ratios in the field can be obtained, hypotheses regarding their influence on sexual behavior in S. officinalis cannot be tested.
2. Sexual Selection Theory
The theory of sexual selection, as proposed and defined by Darwin (1885), is a separate driving force than environmental selection (together the two modes of competition form the process of natural selection) and results from the competition for mates. According to Darwin (1885), “Sexual selection depends on the success of certain individuals over others of the same sex, in relation to the propagation of the species; while natural selection depends on the success of both sexes, at all ages, in relation to the general conditions of life.” Sexual selection may manifest in two different forms: intrasexual selection and intersexual selection. Intrasexual selection refers to the competition among individuals of a single sex, usually male, for access to mates. Such competition may involve physical fighting and agonistic displays intended to drive away or kill rival males, as well as sperm competition, in which sperm from two or more males compete to fertilize ova (Parker, 1970). In this type of selection, the female role is usually cast as one of passivity and inaction.
Contrastingly, intersexual selection highlights an active role for females who exercise selective mate choice, and for most cephalopods, including Sepia officinalis, the concept of the passive female has been set aside in favor of more active roles (Boal, 1997). Here, competition between males remains a factor, where they engage in various courtship displays in contests to win the “favor” of a discriminating female. Displays are characterized by secondary sex characteristics, traits which give the bearers advantages in mating but which have no direct involvement in reproduction itself. These traits may manifest as behaviors or physical ornamentation, the latter contributing to sexual dimorphism in the given species (Darwin, 1885). Sexual dimorphism in cephalopods is evident in various secondary sexual characters including body size and body patterns (Hanlon and Messenger, 1996), while in other taxa these may take the form of extreme characteristics such as enlarged horns, bright colorations, and elaborate plumage (Darwin, 1885). Similar to selection for tail size in some birds (Harvey and Arnold, 1982), for the squids Alloteuthis subulata and A. africana males possess longer tails than females and this character is suggested to be a factor in sexual selection for the species (Rodhouse et al, 1988). Although many of these exaggerated characters can be detrimental to the overall fitness of males, this is not always the case and some provide side benefits to the gene pool as a whole (Fisher, 1930); in addition, the ability of males to survive with apparent handicaps long enough to mate may act as a discriminating factor for females to choose the fittest males (Lande, 1980). While early theories of sexual selection (Darwin, 1885; Fisher, 1930) presumed some sort of selective advantage in order for female preference to originate, others (Lande, 1980; Kirkpatrick, 1982; Arnold, 1983) have argued that female preference may evolve as a simple correlated response to phenotypic changes in males and may continue as a factor in mate choice regardless of any selective advantage. Furthermore, such preferences are defined according to observable behaviors and are not meant to reflect any conscious decisions or aesthetic senses inherent in animals (Halliday, 1983). Preferences may be frequency-dependent, the strength of the preference depending on the choice of males available, or may result from females copying the mate choices of other females (Kirkpatrick, 1987). However, it has been suggested that mate choice may be indirect and a simple correlation between mating success and secondary sex characteristics does not provide sufficient evidence for a direct choice by females (Wiley and Poston, 1996). Instead, experiments must show that females respond differently to males which possess differences in such characters. For S. officinalis, laboratory trials discussed in the following sections have yielded varying results regarding mate choice and possible selective characters.
3. Sexual Behavior of Sepia officinalis
3.1 Visual Displays
Cuttlefish neither shoal as is the case with squids nor are they solitary like octopods, instead living much of their lives dispersed, loose assemblages formed mainly during spawning times (Hanlon and Messenger, 1996). As with other cephalopods, cuttlefish such as S. officinalis are capable of complex intraspecies visual displays with various body patterns generated by neurally controlled chromatophores in the skin. These chromatophores number into the hundreds of thousands in adult cuttlefish and are capable of producing nearly instantaneous color changes incorporating black, brown, red, orange and yellow. Despite widespread agreement that cephalopods are very visual animals, there is evidence that most cephalopods including S. officinalis are color blind, as only one visual pigment, rhodopsin, has been found in 23 out of the 24 cephalopods whose retinal pigments have been examined (Hanlon and Messenger, 1996). Thus, the colorations in the chromatophore-controlled visual displays are less important for intraspecies communication than the body patterns that are produced. The cuttlefish S. officinalis is capable of producing a number of different body patterns which are important components of specific behaviors such as camouflage, defense, agonistic signaling and mating, each of these patterns consisting of chromatic, textural, postural and locomotor components (Hanlon and Messenger, 1988). The role of such body patterns in mating has been examined in other cephalopods including the octopus Hapalochlaena lunulata (Cheng and Caldwell, 2000), the squid Loligo pealei (Hanlon, 1996) and other cuttlefish such as the giant Australian cuttlefish Sepia apama (Hall and Hanlon, 2002). A similar selective force on body pattern has been established in the guppy Poecilia reticulate which displays preferences for body pattern in mates both in field and laboratory studies (Endler, 1980).
Visual displays in S. officinalis are sexually dimorphic. Mature males are recognized by chromatic components on the fourth arm pairs, specifically White and Black Zebra bands and White arm spots (Hanlon and Messenger, 1988). These components form the basis of the Intense Zebra Display visual signal which mature males will present to all other S. officinalis individuals, both male and female, they encounter. Other components of the Intense Zebra Display include the extension of the fourth arms, dark eye ring and anterior head, and a white fin line (Hanlon and Messenger, 1996). This display is returned only by other male cuttlefish and thus it is presumed to be an indicator of maleness in S. officinalis (Tinbergen, 1939). In an experiment intended to study the optomotor responses in blinded S. officinalis, Messenger (1970) observed that male cuttlefish blinded in only one eye responded differently to other males depending from which side they were approached. Unilaterally blinded males approached from their blind side were unable to see the extension of the fourth arms in and thus did not respond in turn with the Intense Zebra Display. Failure to identify itself as male resulted in attempts by the approaching male to copulate with the blinded male. If the unilaterally blinded males were approached from the other side, however, the appropriate display was returned and no copulation attempts were made by approaching males. This suggests that visual display is the primary and possibly the only indicator of sex in S. officinalis.
A second function of the Intense Zebra Display body pattern is observed in agonistic encounters between males. In experiments conducted by Adamo and Hanlon (1996), the agonistic behaviors of mature male S. officinalis were observed in order to analyze the components of the displays. Males were kept chemically isolated then randomly paired and their interactions recorded and analyzed. As sex was determined post-mortem, males were randomly paired with females as well, and a control using only a mirror was used to determine whether or not visual stimuli alone were responsible for invoking a display. In all cases, the agonistic encounters were initiated by both males producing the Intense Zebra Display. Females were capable of producing similar body patterns but did not extend their fourth arms. Visual displays were followed with physical contact between cuttlefish, although in some cases one male withdrew before contact could occur and males also attacked their mirror images, suggesting visual cues are sufficient to stimulate agonistic response. The length of time between initiation of the visual display and initiation of physical contact did not significantly correlate with size differences between males, and both smaller and larger males were seen to initiate agonistic encounters, but larger males defeated smaller males in physical contents 79% of the time. The intensity of the Intense Zebra Display was variable, most notably in the darkness of the anterior head or “face”. Because cuttlefish are considered highly visual animals and have been shown to be capable of discerning differences in brightness and form, if not color, it was assumed that the S. officinalis in this study were able to distinguish between intensity of faces during displays. Darkness of the face was shown to increase with decreasing distance between agonistic male pairs and in those cases where one male retreated before physical contact could be initiated the retreating male displayed a less dark face than the other male in all cases.