The giant cuttlefish Sepia apama Gray, 1849 (Cephalopoda: Sepiidae)--an intertidal record of a molluscan marvel.
The giant cuttlefish Sepia apama Gray, 1849 is the largest cuttlefish in the world, approaching a weight of 5 kg (Okutani 2015), mantle (or main body) length of 500 mm and total length of 100 cm when fully grown (Norman 2000). It is found along the southern Australian coastline from Brisbane, Queensland, to Shark Bay, Western Australia, and around Tasmania (Norman 2000), to depths of 100 metres (Okutani 2015; Reid 2016). Being active during the day (Norman 2000), common, highly intelligent and curious, it is often encountered by divers. Beachgoers are familiar with its cuttlebone, which is frequently washed ashore along its range. However, the Marine Research Group (MRG) of the Field Naturalists Club of Victoria was recently fortunate to record a living specimen in the intertidal zone, trapped by a very low tide in a large, lower littoral pool. This exciting and extremely rare intertidal encounter has prompted a formal report on the sighting and also an overview of the biology of this species and of cephalopods more generally.
A single animal (Fig. 1) was observed at Merricks Beach, Westernport Bay, on Saturday 8 March 2014, in a very large, lower littoral pool bordered by rocky reef to the north and east, with its southern end composed of sandy bottom bearing a large bed of the seagrass Amphibolis antarctica.
The animal was estimated to be in the order of 250-300 mm from tip of mantle to tip of arms and was gliding calmly within the pool. Sometimes it paused, changed colour and raised papillae on its mantle before gently moving off again. The mantle was always held in the horizontal plane. Observing MRG members standing discreetly in a line along the edge of the pool did not alarm the cuttlefish, which swam quite closely by, to and fro, each pass happily exercising the cameras of all present. It engaged members in this manner for some time before it was left to the peace of its pool and the safe, welcoming embrace of the incoming tide.
General structure and biology
The cuttlefish body consists of a somewhat dorso-ventrally flattened mantle (the main body) containing the cuttlebone (or sepion) and viscera, a head bearing large, highly developed eyes and a mouth surrounded by eight suckerlined arms. In Sepia apama the head has characteristic 'twin rows of three flap-like papillae above each eye' (Adam 1966; Norman and Reid 2000; for illustrations see Lu 1998b Fig. 13.2 D; Figs 1E-H herein) and each arm bears four rows of unequal suckers (Cotton and Godfrey 1940). Arm pairs are numbered taxonomically from dorsal to ventral (Norman 2000) and between the third and fourth pairs is a pair of feeding tentacles (also present in squid). The tentacles have a club-shaped terminal process lined with suckers; when not in use, they can be retracted into a pouch below each eye (Zeidler and Norris 1989). The tentacular clubs of S. apama possess five rows of suckers (the middle row largest), the horny rims of which bear short teeth (as do those on the arms) (Cotton and Godfrey 1940). The tentacles are shot out rapidly to capture quarry (Zeidler and Norris 1989; Norman 2000) which is then drawn to the arms and mouth, the opening of which bears a black beak to kill and tear flesh off the victim (Cotton and Godfrey 1940). The radula, a toothed rasp inside the mouth, further shreds the food, and is one of the two key features distinguishing the mollusca, the other being the mantle (Solem 1974). Water leaves the mantle cavity via an exhalent funnel which can be used to generate propulsion. An undulating fin around the periphery of the mantle confers stability and manoeuvrability. Cotton and Godfrey (1940: 417-419) provide a detailed description of the swimming action in Sepia.
[FIGURE 1 OMITTED]
Sepia apama eats fish and crustaceans (Norman 2000) and lives in crevices or caves on rocky reefs (Zeidler and Norris 1989).
The calcareous sepion distinguishes cuttlefish from their close allies the squids. The latter also have eight arms and two feeding tentacles, but instead of a sepion they bear an internal, flattened, corneous, quill-like structure called a 'pen' or gladius (Norman and Reid 2000). This allows the squid body to be more cylindrical and streamlined (although some cuttlefish also possess quite narrow sepions). Octopuses are benthic animals that have eight arms and no feeding tentacles (Norman and Reid 2000); the lack of an internal shell enables them to squeeze into and through the tightest of gaps and crevices, thereby conferring tremendous offensive and defensive advantages.
Most cephalopods produce ink and this is generally used for defensive purposes but can have other functions (see Norman 2000: 101-103). The nervous system and behavioural patterns of cephalopods are highly developed (see Mangold et al. 1998; Norman 2000). Other aspects of cephalopod internal structure, biology and ecology can be found in Ruppert and Barnes 1994; Lu 1998a, 1998b; Lu and Dunning 1998; Mangold et al. 1998; Scott and Kenny 1998; and Norman 2000. Cuttlefish, squid and octopuses are generally short lived, often in the order of one to two years, sometimes approaching four years, with the larger species having longer lifespans (Wood and O'Dor 2000).
Identification guides for cuttlefish sepions are provided by Bell and Plant (1977) for Victoria, Zeidler and Norris (1989) for southern Australia, and Norman and Reid (2000) for Australia. The sepion is almost as long as the body and lies dorsal to the viscera. Fig. 2 shows a sepion of Sepia apama collected on a beach; sepions of adult S. apama lack a distinct posterior terminal spine. The maximum recorded sepion length of S. apama is 560 mm (Reid 2016). The lightness, buoyancy and softness of dead sepions is explained by their microstructure: they are an intricate lattice, bearing very many fine laminar layers arranged roughly parallel to the plane of the sepion. Schmidt-Neilsen (1979) and Norman (2000) report that delicate calcareous pillars separate these laminar layers, but in Sepia apama this appears to be achieved by a radial arrangement of closely spaced septae running perpendicular to the laminar layers (Fig. 2). The sepion is thus composed of very many hollow spaces. In life, a combination of liquid and gas fills the compartments, adjusted by the animal to create neutral buoyancy and thus conferring an ability to occupy a range of depths (Schmidt-Nielsen 1979; Norman 2000). The fluid in a living sepion is hypo-osmotic to sea water; water thus moves out into the surrounding tissues, allowing gas to diffuse in to replace it; the gas is mostly nitrogen, under a low pressure of approximately 0.8 atmospheres, with a small amount of oxygen (Schmidt-Nielsen 1979). Without such a system of buoyancy, the dense muscular body would make the animal sink (Norman 2000).
The osmotic movement of water out of the sepion is opposed by the surrounding hydrostatic pressure; the higher the latter (i.e. the greater the depth), the greater the opposition to the osmotic gradient (Schmidt-Neilsen 1979). In one estimate for cuttlefish, this threshold occurs at an external pressure of 24 atmospheres, equating to a depth of approximately 240 metres (Schmidt-Neilsen 1979). The other depth-limiting factor is the physical strength of the sepion (Schmidt-Neilsen 1979; Norman 2000). Different cuttlebones implode under the hydrostatic pressure at depths between 200 and 600 m (Norman 2000).
Bell (1979a) showed that the average sepion lengths of beached S. apama in Victoria varied on a monthly basis, with progressive average sizes increasing from December through to November (by about 10 mm per month), followed by a sudden fall from November to December. This suggested that hatching in this region occurred in November/December (Bell 1979a). Cotton and Godfrey (1940) collected egg cases on beaches after storms in October and November. Norman (2000) states that this species breeds and spawns from May to September. Based on a study of width to length ratios, Bell (1979a, b) considered S. apama to be mature when the sepion length reached 100 mm (equating to an age of 10 to12 months based on growth estimates). Given this, the Merricks beach specimen was most likely adult. The largest sepion found by Bell (1979a) was 460 mm long, suggesting an age close to four years if regular growth rates are assumed. This study, however, did not directly consider other important growth-rate variables such as water temperature and food availability (Hall et al. 2007), which can vary across seasons and thus confound age estimates. Rather than total sepion length, Hall et al. (2007) noted that it was growth increment patterns in the sepion microsculpture of S. apama that showed seasonal variation, allowing them to be used to assess age. Accordingly, S. apama has an estimated lifespan of up to two years (Hall et al. 2007) (see also the discussion below under reproduction and mating behaviour).
[FIGURE 2 OMITTED]
Some cephalopods also use a gas-containing shell in a similar manner to cuttlefish to maintain neutral buoyancy. Nautilus has a strong external shell with gas-containing chambers (the gas always at a pressure of less than one atmosphere), linked by a communicating channel called the siphuncule, with the animal occupying the largest last chamber (Schmidt-Neilsen 1979; Norman 2000). The Ram's horn squid Spirula spirula also has a small, partially internalised, chambered shell that functions in much the same way. The greater shell rigidity means that the depth range of these groups usually exceeds that of cuttlefish--the Nautilus shell will implode at around 750 m, and Spirula at about 1000 m (Norman 2000).
Lacking a chambered shell, squids cannot maintain neutral buoyancy and must constantly swim to remain suspended in the water column, but this energy cost is compensated by a streamlined agility conferring predatory efficiency (Norman 2000). Nevertheless, there are examples of squid species using stores of ammonium chloride solution or fatty oils (both less dense than seawater) to confer buoyancy (Norman 2000). Octopuses also lack an internal buoyancy system and, although they swim, most are confined to a life on the benthos. However, even within this group there are exceptions, with one species having a gas-filled bladder that enables it to live as a free-swimming animal in surface waters (see Norman 2000: 41).
Colour changes, camouflage and vision
The cephalopod dermis contains chromatophores (pigment cells) in densities of up to hundreds per square mm (Norman 2000), arranged in groups or layers (Ruppert and Barnes 1994). Each chromatophore stores pigment of a particular colour and can be broadly and flatly expanded (enhancing its colour) or greatly contracted (minimising its colour) via voluntary muscle cells (Ruppert and Barnes 1994; Norman 2000). The dermis also contains leucophores (cells which scatter light to produce white colouration [Norman 2000]), and, in the deeper layers, iridophores (cells that reflect light to produce an iridescent hue) (Ruppert and Barnes 1994; Norman 2000). Cephalopods, especially cuttlefish, are thus capable of a bewildering and unrivalled camouflage ability, rapid colour change and complex pattern displays. Bioluminescence is also a capability present especially in deep water squid species (see Norman 2000 for detailed discussion).
To assist camouflage, Sepia apama (like many cephalopods) can also change its surface texture via dermal muscle fibres, raising complex papillae to mimic and blend in with surrounding surfaces such as algal growth (Norman 2000).
Despite the presence of excellent visual acuity in most species, cephalopods do not see in colour (Norman 2000: 82-84), a remarkable fact given their outstanding camouflage ability.
Reproduction and mating behaviour
Breeding in Sepia apama is well documented through study of annual winter mass-spawning aggregations that occur on shallow rocky reefs at northern Spencer Gulf, South Australia (Norman et al. 1999; Hall and Hanlon 2002; Naud et al. 2004; Hall et al. 2007). Here, males flash courtship displays consisting of rippling dark bands along the body (Norman et al. 1999). In these aggregations, males outnumber females by at least four times (Hall and Hanlon 2002), both males and females seek and receive multiple mates (Hall and Hanlon 2002) and female egg clusters show multiple paternity (Naud et al. 2004). Mating occurs head to head, the male transferring a spermatophore package to the female. Males aggressively defend their chosen female from other males (Norman et al. 1999; Hall and Hanlon 2002). In the presence of larger males, smaller males assume female colour patterns, allowing them to approach guarded females without being perceived as a threat by the attending male. While the attending male is otherwise engaged in warding off rivals, the disguised male then successfully moves in and breeds (Norman et al. 1999; Hall and Hanlon 2002).
Sepion microsculpture growth increment patterns from these breeding aggregations suggest two distinct lifecycles in northern Spencer Gulf. Most animals show rapid growth (within eight months) and breed as small adults within the first mating season post-hatching, whilst others grow slowly in the first year and breed as larger adults in the second mating season post-hatching (Hall et al. 2007). Analysis of microsculpture growth patterns from the sampling of breeding individuals over three consecutive winters showed no evidence that either cohort returned to breed in the following year, suggesting that S. apama is semelparous (that is, it breeds only once and then dies) (Hall et al. 2007). Lu (1998b) notes that semelparity is often the case with cuttlefish, squid and octopuses, although there are exceptions across each of these groups (see Mangold et al. 1998: 470-471).
The egg capsules of Sepia apama are white and stalked, total length up to 60 mm (Cotton and Godfrey 1940) with the ovoid body about 30 mm long (Cotton and Godfrey 1940; Smith et al. 1989). Capsules are laid one at a time in groups attached to crevices or the roof of rocky caves, each bearing a single egg (Hall and Hanlon 2002; Smith et al. 1989). After three to five months (Hall and Hanlon 2002), a swimming hatchling emerges from the capsule (Smith et al. 1989).
We are fortunate to have this remarkable animal living in our coastal waters. The giant cuttlefish, like all of its cephalopod relatives, is a molluscan marvel that demonstrates the extraordinary complexity of invertebrate animals. Although common subtidally, its encounter in the intertidal zone was a first for the gathered MRG members and an occasion that all will remember and treasure.
I thank Anne Morton (FNCV) for her encouragement with this article; Amanda Reid (Australian Museum, Sydney) for valued advice; Robert Burn (MRG) for interesting discussion, and the paper by W Adam; Robin Wilson (Museum Victoria) for assistance with reference material; and Evlambia Vafiadis for help with the figures. I also thank an anonymous referee for helpful suggestions and comments that have greatly improved the manuscript.
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Received 1 October 2015; accepted 9 June 2016
Marine Research Group of the FNCV, PO Box 13, Blackburn, Victoria 3130
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|Publication:||The Victorian Naturalist|
|Date:||Aug 1, 2016|
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