Overview

Brief Summary

Introduction

The Australian Giant Cuttlefish (Sepia apama) is the largest cuttlefish species in the world, with a maximum recorded size of 520 mm mantle length (ML) and 6.2 kg weight . It is endemic to Australian waters, with a distribution reported to extend across temperate southern Australia from southern Queensland to Point Cloates in Western Australia, and including northern Tasmania. Its life span is 1 year, perhaps 2 in some cases. It occurs on rocky reefs, seagrass beds and areas of mud and sand to depths of 100m. This species is famous for its unique and very large spawning aggregation that occurs every austral fall (May - July) in northern Spencer Gulf, northwest of Adelaide.


References

Hall, K. C. and R. T. Hanlon. 2002. Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca : Cephalopoda). Mar Biol 140: 533-545

Norman, M. R. 2000. Cephalopods, a world guide : Pacific Ocean, Indian Ocean, Red Sea, Atlantic Ocean, Caribbean, Arctic, Antarctic, ConchBooks, Hackenheim, Germany 318 pp.

Wikipedia

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Interesting Facts

This is the only known large spawning aggregation of cuttlefish in the world.
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Succinct

Largest cuttlefish species in the world, endemic to southern Australian waters.
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Comprehensive Description

Description of Sepia apama

Sepia apama is the Australian Giant Cuttlefish. It is the world\'s largest cuttlefish species, growing to 50 cm in mantle length and over 10.5 kg in weight. S. apama is native to the coast of Australia, from Brisbane in Queensland to Shark Bay in Western Australia. It occurs on rocky reefs, seagrass beds, and sand and mud seafloor to a depth of 100 m. Breeding takes place with the onset of the southern winter. Males abandon their normal cryptic colouring and set out to dazzle the females by adopting rapidly changing bright colours and striking patterns. Devious males mimic female colouring and form in order to gain access to females protected by dominant males. Death follows shortly after mating and laying of eggs that will spawn the next generation. Sepia apama are primarily diurnal and have a small home range (90-550 meters) over short recording periods. They are able to channel most of their energy directly into growth because they spend 95% of the day resting, suggesting bioenergetics more like that of an octopus than a squid. Very little time is spent foraging (3.7% during the day and 2.1% during the night), most of their time is spent resting and hiding in crevices from predators. The exception to this behavioral routine is the mass spawning aggregation, where cuttlefish are far more active during the days or weeks that they spend there.
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Coloration

Sepia apama skin posesses a dense layer of pigmented chromatophore organs of 3 color classes: yellow, red, and black/brown, as well as underlying structural reflectors of 2 types: iridophores (creating iridescence in the skin ) and leucophores, which produce whiteness in their body patterns. They also have controllable skin papillae that can dramatically alter their appearance. The overall appearance of the animal - termed the body pattern - can change in less than a second due to direct neural control of the skin patterns. This is unique among all animals but is characteristic of cephalopods.


Reference

Oceanworld Cuttlefish Fact Files

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Distribution

Range Description

This species is endemic to Australia (Reid et al. 2005). Its range stretches across southern Australia to Pointes Cloates in Western Australia to Shoalwater Bay in Queensland (Reid et al. 2005). It is also found around Lord Howe and Norfolk Island (Reid et al. 2005).
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Distribution map of S. apama. (Credit: Mark Norman & Amanda Reid, 2000)

Sepia apama occurs in the southern half of Austrlia from Brisbane in the east to Sharks Bay in the west.


Reference

Norman, M. R. 2000. Cephalopods, a world guide : Pacific Ocean, Indian Ocean, Red Sea, Atlantic Ocean, Caribbean, Arctic, Antarctic, ConchBooks, Hackenheim, Germany 318 pp.

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Physical Description

Size

Physical Description

The giant cuttelfish is the largest cuttelfish species in the world. Sepia apama have eight sucker-lined arms and two retractable tentacles, which they use for capturing prey. Cuttlefish have a highly developed central nervous system and well developed complex eyes. They have a thick, internal calcified shell (the "cuttlebone") beneath an elongated muscular mantle. The mantle is expanded and contracted to expel water from the mantle cavity through the funnel. The mouth consists of a parrot-like beak, jaws, and a rasping tongue (a typical molluscan radula).


References

Animal Diversity Web

BBC Giant Cuttlefish Fact File

Hanlon, R.T. & J.B. Messenger. 1996. Cephalopod Behaviour. Cambridge University Press, 232pp.

Nixon, M. & J. Z. Young. 2003. The Brains and Lives of Cephalopods. Oxford University Press, 392pp

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Diagnostic Description

Formal Description

Diagnostic features: Adults very large. Sucker-bearing surface of tentacular club raised off of the stalk, attached only by a thin membrane; 5 suckers in rows across the manus, median suckers enlarged; swimming keel of the club extending along stalk a distance equal to the club length. Web between arms deep: equal to half of arm length between dorsal arms, two-thirds of arm length between lateral arms, absent between ventral arms. Three flat, semicircular, flap-like papillae posterior to each eye. Fins broad. Colour: deep maroon.


References

Roper, C. F. E., M. J. Sweeney and C. E. Nauen. 1984 FAO Species Catalogue Vol 3. Cephalopods of the World: An Annotated and Illustrated Catalogue of Species of Interest to Fisheries. FAO Fisheries Synopsis 125(3).

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Ecology

Habitat

Habitat and Ecology

Habitat and Ecology
This species is a neritic species that occurs in a variety of habitats including: coral reefs, rocky reefs, seagrass beds and muddy and sandy areas (Norman 2003). They are active by day preying on fish and crustaceans (Norman 2003, Reid et al. 2005). During breeding, ritualized visual displays are observed (Norman 2003). After mating the large eggs are laid in crevices and take three to five months to hatch at low temperatures (12°C) (Reid et al. 2005). The distribution of this species may be restricted to cool southern waters because low temperatures reduce the problems associated with gas exchange in large eggs (Reid et al. 2005). The young develop directly (Norman 2003). The adults are preyed upon by dolphins, particularly during the spawning season (Norman 2003) and albatrosses (H. Battam pers. comm.). They appear to spawn in aggregations based on suitable habitat for egg laying.

Systems
  • Marine
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Depth range based on 8 specimens in 1 taxon.
Water temperature and chemistry ranges based on 5 samples.

Environmental ranges
  Depth range (m): 1.5 - 71.5
  Temperature range (°C): 14.137 - 17.433
  Nitrate (umol/L): 0.094 - 2.747
  Salinity (PPS): 35.417 - 35.773
  Oxygen (ml/l): 5.358 - 5.626
  Phosphate (umol/l): 0.139 - 0.312
  Silicate (umol/l): 0.831 - 2.015

Graphical representation

Depth range (m): 1.5 - 71.5

Temperature range (°C): 14.137 - 17.433

Nitrate (umol/L): 0.094 - 2.747

Salinity (PPS): 35.417 - 35.773

Oxygen (ml/l): 5.358 - 5.626

Phosphate (umol/l): 0.139 - 0.312

Silicate (umol/l): 0.831 - 2.015
 
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S. apama is native to southern Australia, from Brisbane in the east to Shark Bay in the west. It occurs on rocky reefs, seagrass beds, and sand and mud seafloor to a depth of 100 m.
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Population Biology

Population Structure

In general, the sex ratio in the populations is thought to be 1:1. However, there is a highly skewed male-biased operational sex ratio in the spawning aggregation (up to 11:1). This is the highest known among cephalopods. The change in the S. apama sex ratio during the spawning season (from more to less skewed towards males) suggests that males arrive before females at the start of the season. Therefore, males may not aggregate in response to a concentration of females, but rather at a particular location or habitat type. Recent genetic evidence (using allozyme electrophoresis, microsatellites and mitochondrial nucleotide sequences) has revealed three major genetically distinct groups of Sepia apama. It has been recommended that each of these groups be managed separately to preserve genetic diversity.


Reference

Hall, K. C. and R. T. Hanlon. 2002. Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca : Cephalopoda). Mar Biol 140: 533-545

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General Ecology

Ecological Determinants/Niche

S. apama is native to southern Australia, from Brisbane in the east to Shark Bay on the west coast. It occurs on rocky reefs, seagrass beds, and sand and mud seafloor to a depth of 100 m.
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Ecosystem Role

  • Sepia apama eat crustaceans and fish and have many predatorrs including: fur seals, sea lions, albatross, dolphins and sharks.


    References

    Battam, H. and W. A. Buttemer. 2000. Some aspects of energy assimilation and use in four southern albatrosses. Marine Ornithology 28.

  • Gales, R., D. Pemberton, C. C. Lu, and M. R. Clarke. 1993. Cephalopod diet of the Australian fur seal - variation due to location, season and sample type. Australian Journal of Marine and Freshwater Research 44: 657-671.

    McIntosh, R. R., B. Page, and S. D. Goldsworthy. 2006. Dietary analysis of regurgitates and stomach samples from free-living Australian sea lions. Wildl Res 33: 661-669.

    Animal Diversity Web

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    Life History and Behavior

    Behavior

    Giant cuttlefish have the remarkable ability to dynamically change color and pattern for a wide variety of key behaviors involving camouflage and communication. Sepia apama is mainly active during the day and uses camouflage to hide among rock reefs and seaweed. Cuttlefish usually sit on or hover slightly above the bottom. Sepia apama can move slowly with stealth, swim or employ jet propulsion in bursts of surprising speed. This species preys on live fish, crabs and other crustaceans. All members of the Sepioidea use jets of ink to confuse foes during escapes. They are generally solitary animals (except when breeding) and curious about divers. Sepia apama skin posesses a dense layer of pigmented chromatophores, mainly yellow, red, black and brown, as well as a wide variety of iridophores (creating iridescence in the skin for camouflage and communication) and leucophores that produce whiteness in their body patterns. They also have controllable skin papillae that can dramatically alter their appearance.

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    Night Camouflage

    In addition to camouflaging themselves during daylight hours, Sepia apama uses adaptable night camouflage to conceal itself from nightime predators; animals in spawning aggregations have been shown to cease sexual signaling behaviors and become sessile and camouflaged during the night. Remarkably, the camouflaged body patterns at night are tailored to each microhabitat that the animal might rest in, providing evidence that their night vision is excellent and that night predators also have keen vision.


    References

    Hanlon, R. T., M. J. Naud, J. W. Forsythe, K. Hall, A. C. Watson, and J. McKechnie. 2007. Adaptable night camouflage by cuttlefish. Am Nat 169: 543-551

    EurekAlert! Stealth camouflage at night

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    General Camouflage

    Cuttlefish are capable of showing dozens of body patterns for camouflage and these body patterns can be grouped into three categories: uniform/stipple, mottle, and disruptive. Aside from skin patterns, cuttlefish can augment camouflage with postural and 3-D skin texture: by contorting their arms in different postures that generally imitate nearby algae, and by sprouting spiky skin projections, called papillae, imitating the physical texture of the surrounding seaweed, rock or coral. The chromatophores and skin papillae can change about one second faster than any other animal. Both skin texture and color changes are directly controlled by the animal's brain. Messages enter the brain through the eye via the optic nerve, are processed in the CNS, and then the skin is changed by direct neural control of the pigmented chromatophores.


    References

    Hanlon, R. T. and J. B. Messenger. 1996. Cephalopod Behavior. Cambridge: Cambridge University Press, 1996.

    Hanlon, R. T., M. J. Naud, J. W. Forsythe, K. Hall, A. C. Watson, and J. McKechnie. 2007. Adaptable night camouflage by cuttlefish. Am Nat 169: 543-551

    Mathger, L. M., A. Barbosa, S. Miner, and R. T. Hanlon. 2006. Color blindness and contrast perception in cuttlefish (Sepia officinalis) determined by a visual sensorimotor assay. Vision Research 46(11): 1746-1753.

    Oceanworld Cuttlefish Fact Files

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    Reproductive Behavior - Overview

  • Every winter thousands of Giant Cuttlefish (Sepia apama Gray) aggregate to spawn along a restricted area of rocky reef in northern Spencer Gulf, South Australia. It is the only known spawning aggregation of cuttlefish in the world and represents an exceptional cuttlefish mating system of high complexity. Females move around the area paying little heed to males, and males pursue females and compete for them. S. apama male tactics are diverse. Females attach their eggs individually to the underside of rocks, ledges, and caves in subtidal rocky reef habitats, and the eggs hatch in 3–5 months.


    References

    Hall, K. C. and R. T. Hanlon. 2002. Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca : Cephalopoda). Mar Biol 140: 533-545

    ABC News Article: So, which rock did you crawl out from under? Deep-sea dates do the business off Whyalla

    Short Story: King of the Cross-Dressers

  • The University of Adelaide News Story: Cross-dressing cuttlefish to sex up tourism

    Discover Magazine: Cuttlefish in Love

    The Independent News Article: Cross-dressing cuttlefish is Casanova of the reef

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    Male Behavior

    Since the sex ratio on the spawning grounds ranges from 4-11 males/1 female, there is a high level of competition for females. Males on the spawning grounds are sexually dimorphic by size. Large males (mean 370 mm mantle length, ML) pair with and guard females (mean 250 mm ML) temporarily (pre- and postcopulation). Large lone males search for lone females or challenge consorts with agonistic displays. Large males engage in agonistic contests that pass through increasingly complex stages of display, culminating in a dramatic passing cloud display and sometimes physical contact and biting (see video of courtship behavior). Contests ended with one male swimming away. Small lone males guard females if there is no large male in the vicinity, or search for lone females with whom they mate without guarding. Small males (150–250 mm ML) may also use opportunities for extrapair copulations (EPCs). They use "open stealth" (overt sneak mating), "hidden stealth" (concealed sneak mating, e.g. under a rock) and female mimicry to achieve sneaker EPCs (see video of males mimicking females). Female mimicry leads to increased acceptance of mating with the female, and to immediate fertilization, as demonstrated by DNA fingerprinting.


    References

    Hall, K. C. and R. T. Hanlon. 2002. Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca : Cephalopoda). Mar Biol 140: 533-545

    Hanlon, R. T., M. J. Naud, P. W. Shaw, and J. N. Havenhand. 2005. Behavioural ecology - Transient sexual mimicry leads to fertilization. Nature 433: 212-212

    Naud, M. J., R. T. Hanlon, K. C. Hall, P. W. Shaw, and J. N. Havenhand. 2004. Behavioural and genetic assessment of reproductive success in a spawning aggregation of the Australian giant cuttlefish, Sepia apama. Anim Behav 67: 1043-1050

    Norman, M. R. 2000. Cephalopods, a world guide : Pacific Ocean, Indian Ocean, Red Sea, Atlantic Ocean, Caribbean, Arctic, Antarctic, ConchBooks, Hackenheim, Germany 318p

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    Female Behavior

    Females ultimately determine whether to accept a mating attempt. They reject a large percentage of mating attempts (up to 70%) and sometimes reject large consort males to mate with a small lone male. Females possess a sperm receptacle below the mouth and may use stored sperm from this receptacle or sperm from spermatangia placed in the buccal area to fertilize their eggs. Thus, females may accumulate sperm from consecutive matings and create considerable potential for sperm competition; it is not known if females exert cryptic sperm choice. Individual females can be extremely active on the spawning grounds: in a single day one female was documented to mate 17 times, with 8 different males, and lay 37 eggs in the course of 9 hours.


    References

    Hall, K. C. and R. T. Hanlon. 2002. Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca : Cephalopoda). Mar Biol 140: 533-545

    Hanlon R, T. and J. B. Messenger. 1996. Cephalopod Behavior. Cambridge: Cambridge University Press, 1996.

    Naud, M. J., R. T. Hanlon, K. C. Hall, P. W. Shaw, and J. N. Havenhand. 2004. Behavioural and genetic assessment of reproductive success in a spawning aggregation of the Australian giant cuttlefish, Sepia apama. Anim Behav 67: 1043-1050

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    Mating

    Female Sepia apama alternate mating with egg-laying and often mate with multiple males between egg-laying events. Mating occurs in the head-to-head position during which the male flushes water over the buccal area before placing spermatophores there. Eggs are extruded singly and held amidst the female's arms - this appears as a bulge in her arms; at this time, sperm from the spermatangia in that area, or sperm released from the sperm receptacle, compete to fertilize the egg. Females then attach their eggs individually to the underside of rocks, ledges and reefs in subtidal rocky habitat.


    Reference

    Hall, K. C. and R. T. Hanlon. 2002. Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca : Cephalopoda). Mar Biol 140: 533-545.

    Naud, M. J., R. T. Hanlon, K. C. Hall, P. W. Shaw, and J. N. Havenhand. 2004. Behavioural and genetic assessment of reproductive success in a spawning aggregation of the Australian giant cuttlefish, Sepia apama. Anim Behav 67: 1043-1050.

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    Life Cycle

    Life History

    Sepia apama have a life span of 1-2 years. Not much is known about their life history outside of the breeding season. Breeding takes place during the austral winter (May to September), when hundreds of thousands of animals aggregate in northern Spencer Gulf to mate and lay eggs. Recent research based on analysis of growth increments of cuttlebones suggests that Sepia apama has two alternative life cycles (for both sexes). The first involves rapid juvenile growth during the first summer after hatching, with maturity reached within 7–8 months. These individuals return to spawn in their first year as small individuals. The second life cycle involves much slower juvenile growth during the first summer, with maturity deferred until their second year, when they return to spawn as much larger individuals.


    Reference

    Hall, K. C., A. J. Fowler, and M. C. Geddes. 2007. Evidence for multiple year classes of the giant Australian cuttlefish Sepia apama in northern Spencer Gulf, South Australia. Rev Fish Biol Fish 17: 367-384.

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    Evolution and Systematics

    Systematics or Phylogenetics

    Classification

    Kingdom: Animalia
    Phylum: Mollusca
    Class: Cephalopoda
    Order: Sepiida
    Family: Sepiidae
    Genus: Sepia
    Species: Sepia apama


    References

    ITIS Report: Sepia apama

    Gray, J. E. 1849. Catalogue of the Mollusca in the British Museum. Part I. Cephalopoda Antepedia. 164.

    Lipinski, M. R., F. A. Naggs, and M. A. Roeleveld / N. A. Voss, M. Vecchione et al., eds. 1998. Nominal type specimens of Sepiidae in The Natural History Museum, London (BMNH). Systematics and Biogeography of Cephalopods. Smithsonian Contributions to Zoology, 586 (I-II): 157.

    Lu, C. C. / N. A. Voss, M. Veccione, R. B. Toll and M. J. Sweeney, eds. 1998. A synopsis of Sepiidae in Australian waters (Sepioidea: Cephalopoda). Systematics and Biogeography of Cephalopods. Smithsonian Contributions to Zoology, 586 (I-II): 159-190.

    Sweeney, M. J. and C. F. E. Roper / N. A. Voss, M. Vecchione, R. B. Toll and M. J. Sweeney, eds. 1998. Classification, type localities and type repositories of recent Cephalopoda. Systematics and Biogeography of Cephalopods. Smithsonian Contributions to Zoology, 586 (I-II): 561-599.

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    Concepts and Synonymy

    Amplisepia parysatis Iredale, 1954, Sepia palmata Owen, 1881


    References

    Iredale, T. 1954. Cuttle-fish "Bones" again. Australian Zoologist 1(1): 63-82.

    Rudman, W. B. 1983. The Cephalopod Collections of the Australian Museum. Memoirs of the Museum of Victoria 44: 67-68.

    Lu, C. C. / N. A. Voss, M. Veccione, R. B. Toll and M. J. Sweeney, eds. 1998. A synopsis of Sepiidae in Australian waters (Sepioidea: Cephalopoda). Systematics and Biogeography of Cephalopods. Smithsonian Contributions to Zoology, 586 (I-II): 159-190.

    Owen, R. 1881. Descriptions of some new and rare Cephalopoda (Part II). Transactions of the Zoological Society of London 11(5): 131-170.

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    Physiology and Cell Biology

    Physiology

    Vision

    Cuttlefish have a uniquely shaped pupil comprising several slits in different orientations - some are W-shaped and others, like S. apama, have one horizontal slit that bends obliquely vertical. Light entering the eye is controlled by altering the shape of the entire eyeball. To focus on nearby objects a cuttlefish contracts a surrounding layer of the muscle, moving the lens forward, away from the retina and it focuses on distant objects by drawing the lens in. Cuttlefish are known to be color-blind, having only one visual pigment at 492nm. Despite being color-blind cuttlefish are very good at blending into colorful natural environments (at least in shallow depths of water).


    References

    Oceanworld Cuttlefish Fact Files

    Marshall, N. J. and J. B. Messenger. 1996. Colour-blindcamouflage. Nature 382: 408–409

    Mathger, L., A. Barbosa, S. Miner and R. T. Hanlon. 2006. Color blindness and contrast perception in cuttlefish (Sepia officinalis) determined by a visual sensorimotor assay. Vision Res. 46: 1746-1753.

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    Physiology and Biochemistry

    A recent energetics study found that Sepia apama are primarily diurnal and have a small home range (90-550 meters) over short recording periods. They are able to channel most of their energy directly into growth because they spend 95% of the day resting, suggesting bioenergetics more like that of an octopus than a squid. Very little time is spent foraging (3.7% during the day and 2.1% during the night), most of their time is spent resting and hiding in crevices from predators. The exception to this behavioral routine is the mass spawning aggregation, where cuttlefish are far more active during the days or weeks that they spend there.


    References

    Aitken, J. P., R. K. O'Dor and G. D. Jackson. 2005. The secret life of the giant Australian cuttlefish Sepia apama (Cephalopoda): Behaviour and energetics in nature revealed through radio acoustic positioning and telemetry (RAPT). J Exp Mar Biol Ecol 320: 77-91

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    Molecular Biology and Genetics

    Molecular Biology

    Molecular Biology and Genetics

    Several microsatellite markers have been produced for the assessment of genetic diversity and paternity analyses in Sepia apama (Genbank accession numbers EF368216-224, AY617047, AY617024, AY616977, AY616950, AF533071-8, AY294335-353). Recent genetic evidence (using allozyme electrophoresis, microsatellites and mitochondrial nucleotide sequences) has revealed three major genetically distinct groups of Sepia apama. It has been recommended that each of these groups be managed separately to preserve genetic diversity. Initial paternity analysis of the complex mating system of the giant cuttlefish indicates that this mating system has a high level of multiple mating that results in multiple paternity; males of any size or status can obtain successful fertilizations. Genetic analysis has also shown that the two female sperm storage areas (the short-term spermatangia - in the buccal area- and the long-term sperm receptacle - beneath the beak) both can contain sperm from multiple males. Of the two storage areas, sperm from the spermatangia (recent matings within a few hours or days) is used more frequently to fertilize eggs than sperm from the receptacle.

    References

    Kassahn, K. S., S. C. Donnellan, A. J. Fowler, K. C. Hall, M. Adams, and P. W. Shaw. 2003. Molecular and morphological analyses of the cuttlefish Sepia apama indicate a complex population structure. Mar Biol 143: 947-962.

    Naud, M. J., P. W. Shaw, R. T. Hanlon, and J. N. Havenhand. 2005. Evidence for biased use of sperm sources in wild female giant cuttlefish (Sepia apama). Proc R Soc Lond Ser B-Biol Sci 272: 1047-1051.

    Naud, M. J., R. T. Hanlon, K. C. Hall, P. W. Shaw, and J. N. Havenhand. 2004. Behavioural and genetic assessment of reproductive success in a spawning aggregation of the Australian giant cuttlefish, Sepia apama. Anim Behav 67: 1043-1050.

    Shaw, P. W. 2003. Polymorphic microsatellite DNA markers for the assessment of genetic diversity and paternity testing in the giant cuttlefish, Sepia apama (Cephalopoda). Conserv Genet 4: 533-535.

    Wheaton, L., S. C. Donnellan, M. C. De, M. G. Gardner, and B. M. Gillanders. 2007. Isolation of additional polymorphic tri- and tetranucleotide microsatellite loci for the giant Australian cuttlefish (Sepia apama). Mol Ecol Notes 7: 893-895.

    GenBank

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    Conservation

    Conservation and Fisheries

    Prior to mid 1990s, the spawning aggregation at Whyalla, in northern Spencer Gulf, was fished at sustainable levels for snapper bait. However, in the mid 1990’s, fishers actively targeted cuttlefish, and large numbers of the breeding aggregation were removed from the system. Since the lifecycle of Sepia apama is very short (1-2 yrs), if a cohort of breeders is fished out, the following generation is likely to be severely impacted. To avoid long-term population decline, even local extinction, a renewable moratorium preventing fishing was introduced in 1999. In subsequent years, the cuttlefish numbers increased again, and ecotourism in the area began to thrive, as it does at this writing (2007). The most recent survey, done in 2005, showed a slight decline in abundance since the estimates made in 1998 and 2001. This survey indicates that declines may be the result of multiple factors - not solely over-exploitation from targeted human fishing. More precise molecular data on population genetics will help determine the composition of the hundreds of thousands of cuttlefish that constitute this extremely unique mass spawning aggregation. This is a clear case of ecotourism aiding conservation.


    References

    The University of Adelaide Cuttlefish Project

    Steer, M. A. and K. C. Hall. 2005. Estimated abundance and biomass of the unique spawning aggregation of the giant Australian cuttlefish (Sepia apama) in northern Spencer Gulf, South Australia. Report to Coastal Protection Branch, Department for Environment and Heritage, South Australia. South Australian Research and Development Institute (Aquatic Sciences), Adelaide, RD 05/0012-1.

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    Conservation Status

    IUCN Red List Assessment


    Red List Category
    NT
    Near Threatened

    Red List Criteria

    Version
    3.1

    Year Assessed
    2012

    Assessor/s
    Barratt, I. & Allcock, L.

    Reviewer/s
    Reid, A., Rogers, Alex & Bohm, M.

    Contributor/s
    Battam, H., Gillanders, B., Hilton-Taylor, C., Herdson, R. & Duncan, C.

    Justification
    Sepia apama has been assessed as Near Threatened. Intense fishing in one location has resulted in massive local population declines. Although this has had limited impact across the species range, it is coupled with the potential (but not evidence/occurrence so far) for intense localized fishing elsewhere, albeit on smaller aggregations. Because the species is short-lived (one to two years) and semelparous, the impact of such fishing would likely be catastrophic and we therefore consider this species Near Threatened (as it almost qualifies for a threatened listing under criterion A3d). We believe that a population reduction of greater than 20% may occur in the future based on existing exploitation of the largest known breeding aggregation and potential future exploitation of other smaller breeding aggregations elsewhere along the coast. If the population in the upper Spencer Gulf is shown to be a separate species then the Spencer Gulf species would be assessed as Endangered.
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    Population

    Population
    The population size of this species is unknown. Estimates of abundance and biomass at the spawning aggregation area in northern Spencer Gulf, South Australia show a 57% decline between 2001 and 2008 (Hall 2008) and this is assumed to be the result of intense fishing activity in this area. This spawning aggregation, which is easily detected by divers and exploited by fishers, is associated with the physical features of the Gulf itself. Compared with the open coast, the water is relatively sheltered and the Gulf has plenty of hard substrate providing good attachment sites for eggs. The only other subpopulation for which information is available is Wollongong. The information from this area is anecdotal and comes from albatross researchers (the albatross feed on the spawning aggregations of cuttlefish). In the Wollongong region, aggregations also appear to be dependent on the availability of suitable habitat. The S. apama seaward distribution boundary appears to be determined by water depth, and is estimated at about 75 metres. The coastal strip between Red Point (Pt Kembla) and Austinmer appears to be the area where S. apama is most concentrated (total area 70-80 m²). It is suspected that this is due to the nature of the sea bottom, as this area has numerous reefs, which are not typical of the sea floor to the north and south of the region. The number of S. apama carcasses and bones observed at sea does vary from year to year, but a maximum estimate is several thousand (cumulative annual total). Smaller concentrations of S. apama occur at other locations, including Sussex Inlet and Ulladulla, which are south of Wollongong. It is unknown what proportion of the total population the Spencer Gulf breeding aggregation represents but, in terms of area, the Spencer Gulf IMCRA province encompasses about 15 % of the total shelf provinces inhabited by S. apama. Hence, if the population size elsewhere has remained stable, and the breeding aggregation in Spencer Gulf is only drawn from Spencer Gulf, then the total population decline to date is equivalent to about 8.5 %.

    Population Trend
    Decreasing
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    Threats

    Major Threats
    Ocean acidification caused by increased levels of carbon dioxide in the atmosphere is potentially a threat to all cuttlefish. Studies have shown that under high pCO2 concentrations, cuttlefishes actually lay down a denser cuttlebone which is likely to negatively affect buoyancy regulation (Gutowska et al. 2010). This species is the target of commercial fisheries (e.g. Spencer Gulf, Norman 2003), which have reduced population size by 57% in the Spencer Gulf. It is also taken by hook-and-line or spear fishing and as bycatch off southern Australia (Reid et al. 2005). The Spencer Gulf population is additionally suffering from threats imposed by a proposed desalination plant development at Point Lowly. This may lead to high levels of salinity in Spencer Gulf, higher temperatures, increased turbidity levels, decreased oxygen levels and possibly the discharge of contaminants, which would likely reduce the Spencer Gulf population even further. Unpublished data suggest from the Geelong area suggest a two year pre-breeding harvest could eliminate the whole population. Local fisherman report that in March-April S. apama embark on a pre-breeding feeding frenzy. They attack hooked fish and are detached with much difficult when brought to the surface. Within this period, they would appear to be extremely vulnerable to fishing. Hence, the greatest threat to this species is probably intense localised fisheries on breeding aggregations (albeit smaller than the Spencer Gulf aggregation) around the coast.
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    How to Grow

    Dr. Karina Hall (2002) reared the eggs to juvenile adult stage but growth was very slow compared to that of other cuttlefish such as Sepia officinalis. A great deal more aquaculture effort on a larger scale is needed to assess the convenience of culturing this species in the laboratory or for providing a food source. The largest problem is that cuttlefish are carnivores that strongly prefer live food such as crustaceans and fish.

    References

    Hall, K. C. 2000. Cuttlefish mysteries. Southern Fisheries 7

    Forsythe, J. W., R. H. DeRusha, and R. T. Hanlon. 1994. Growth, reproduction and life span of Sepia officinalis (Cephalopoda: Mollusca) cultured through seven consecutive generations. J. Zool. 233: 175–192.

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    Management

    Conservation Actions

    Conservation Actions
    Recent fishing activity targeting the mass spawning aggregations at Spencer Gulf caused a decline in numbers leading to a temporary closure of the fishing grounds (Norman 2003). These mass spawning areas are easily accessible and could be used as tourist attraction (Norman 2003). Further research is recommended to determine the population trends, distribution, life history traits and threats impacting this species.
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    Relevance to Humans and Ecosystems

    Benefits

    Uses

    Since ca. 1999, this species has been an important ecotourism attraction to the city of Whyalla, South Australia. Divers come from around the world to see this amazing underwater spectacle of thousands of active cuttlefish on the spawning aggregation. This spectacle has grown in its popularity and continues to be featured in international television productions around the world. There is even a bus tour that features the giant cuttlefish (see image below). Outside of the protected spawning areas, this cuttlefish supports a small scale bait fishery, and some animals are eaten by humans. Importantly, this highly unique spawning aggregation has become a biological model for mating systems (see many scientific journal papers published on this since 1999).


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    Wikipedia

    Sepia apama

    Sepia apama, also known as the giant cuttlefish and Australian giant cuttlefish,[2] is the world's largest cuttlefish species, growing to 50 cm in mantle length and over 10.5 kg (23 lb) in weight.[3] Using cells known as chromatophores, the cuttlefish can put on spectacular displays, changing color in an instant.

    S. apama is native to the southern coast of Australia, from Brisbane in Queensland to Shark Bay in Western Australia. It occurs on rocky reefs, seagrass beds, and sand and mud seafloor to a depth of 100 m.[4]

    Life cycle and reproduction[edit]

    Sepia apama live from two to three years. Breeding takes place with the onset of the southern winter. Males abandon their normal cryptic coloring and set out to dazzle the females by adopting rapidly changing bright colours and striking patterns. Females are polyandrous, and collaborative research indicates the tendency for females to reproduce using male genetic material deposited in spermatangia more favorably than in sperm receptacles directly. Females then attach their eggs to the underside of rocks in caves or crevises where they will hatch within three to five months. Sepia apama are semelparous and death follows shortly after a single mating cycle and laying of eggs that will spawn the next generation.[5] Sepia apama have poor anaerobic capability compared to most aquatic invertebrates and a lack of food leads to catabolism. Stomach content analysis indicates fasting during the breeding season and as Sepia apama can catabolise no more than 50% of their body weight they slowly lose physical condition as the season progresses and eventually die. Throughout their range, Sepia apama breed in pairs or small groups, laying eggs in suitable caves or rock crevises. Loose spawning aggregations can form but rarely exceed 10 animals in any one location,[6] with one known exception: hundreds of thousands aggregate off Point Lowly in the Upper Spencer Gulf. While surveys suggest that juveniles leave the spawning ground after hatching, nothing is known of their subsequent movement or lifestyle strategies as a juvenile.

    Physiology and biochemistry[edit]

    Genetic studies have shown that there is little if any interbreeding between Sepia apama populations. While there is some genetic divergence, the various populations are not considered taxonomically distinct and are commonly referred to by their location, e.g. Sepia apama upper Spencer Gulf population.[5] The upper Spencer Gulf population is unique in that a permanent salinity gradient in the Spencer Gulf may physiologically exclude other populations from the zone occupied by the upper Spencer Gulf population.[5] Research suggests that the upper Spencer Gulf population may in fact be a separate species as it does show some hallmarks, such as genetic separation, differences in morphology and different patterns of sexual dimorphism to adjacent populations.[6][7]

    Sepia apama is a neritic demersal species. They are carnivorous, opportunistic and voracious predators who feed predominantly on crustaceans and fish.[6] Using neurally controlled cells known as chromatophore organs (red to yellow), iridophores (iridescent: spans the entire visible spectrum from blue to near-IR) and leucophores (white), the cuttlefish can put on spectacular displays, changing colour and patterns in a fraction of a second. Located in three layers under the skin, leucophores make up the bottom layer, with chromatophores the outermost. By selective blocking, the three layers work together to produce polarised patterns. Unlike those in most animals, cuttlefish iridophores are physiologically active; they can change their reflectivity and the degree of polarization can also be controlled. Cuttlefish are colourblind, however the photoreceptors of cuttlefish eyes are arranged in a way which gives them the ability to see the linear polarization of light. While the Mantis shrimp is the only known creature to have true polarization vision, it is believed that cephalopods may also.[8] Because the optic lobes of cuttlefish are larger than any other region of the brain and their skin produces polarized reflective patterns, it has been postulated that they may communicate through this visual system.[9] By raising elaborate papillae on their skin, S. apama can change the shape and the texture of their skin to imitate rock, sand or seaweed.[10]

    A recent energetics study found that Sepia apama are primarily diurnal and have a small home range (90–550 metres) over short recording periods while travelling large distances to breed. They are able to channel most of their energy directly into growth because they spend 95% of the day resting, suggesting bioenergetics more like that of an octopus than a squid. Very little time is spent foraging (3.7% during the day and 2.1% during the night), most of their time is spent resting and hiding in crevices from predators. The exception to this behavioral routine is the mass spawning aggregation, where cuttlefish are far more active during the days or weeks that they spend there.[11][12]

    Role in ecosystem[edit]

    The Australian giant cuttlefish is eaten by Indo-Pacific bottlenose dolphins, which have been observed (in South Australia's Spencer Gulf) to have developed a technique for removing the ink and cuttlebone from a cuttlefish before eating it.[13]

    Upper Spencer Gulf population[edit]

    Dorsal (left) and ventral views of Sepia apama: lithographic proofs from Prodromus of the Zoology of Victoria by John James Wild

    Discovered by divers in the late 1990s, the upper Spencer Gulf population is the world's only known mass cuttlefish spawning aggregation with hundreds of thousands of Sepia apama congregating on sub-tidal reefs around Point Lowly near Whyalla between May and August. While outside of the breeding season, the sex ratio is 1 to 1, Spencer Gulf males outnumber females by up to 11 to 1 in the spawning aggregation. It is unclear if this is due to fewer females taking part or to males breeding for a longer period of time than females. With densities of one cuttlefish per square metre, covering approximately 61 hectares (150 acres), the sheer number of Sepia apama makes this breeding aggregation unique in the world. As the cuttlefish are oblivious to divers while spawning, they are now a major regional tourist attraction for divers from around the world.[6] Professor Roger Hanlon of the Woods Hole Oceanographic Institution has called the breeding aggregation "the premier marine attraction on the planet."[7]

    The Sepia apama upper Spencer Gulf population displays two alternative life cycles in both sexes (growth pattern polymorphism). The first involves rapid growth with maturity reached in seven to eight months with small adults returning to spawn in the first year. The second involves slow growth with maturity reached in two years with large adults returning to spawn in the second year.[5] The upper Spencer Gulf population displays reproductive behaviours unique to this population, possibly as a result of the high spawning densities. Large males defend females and egg laying sites while small males mimic female colouring and form in order to gain access to the females being protected by the dominant males which are extremely territorial. Male genetic material is deposited in sperm receptacles directly. The females, who potentially lay hundreds of eggs, extracts one egg at a time and fertilises it by passing it over the sperm receptacle before attaching it to the underside of a rock at depths of 2 metres (6.6 ft) to 5 metres (16 ft).[6]

    Prior to the mid-1990s, the population was fished for snapper bait with annual catches of around four tonnes (approx 4,000 cuttlefish). During the 1995 and 1996 spawning seasons, commercial fishing of the spawning grounds harvested around 200 tonnes annually. Over exploitation was recognised after 245 tonnes was harvested in 1997, leading to 50% of the grounds being closed to commercial fishing in 1998. Despite half of the grounds being closed, commercial fishers took 109 tonnes in 1998 (approximately half of the estimated biomass) before dropping to 3.7 tonnes in 1999. The catch data for 2000 to 2005 has not been released for confidentiality reasons.[14] Surveys indicated that the cuttlefish biomass remained stable from 1998 to 2001. A further survey in 2005 revealed a 34% decrease in biomass since 2001 that was attributed to natural variability and illegal fishing during the peak spawning period.[14] The closure was subsequently expanded to the entire spawning grounds and anecdotal observations suggested increased numbers in 2006 and 2007, however, a new survey in 2008 found the biomass had decreased a further 17%.[5][6]

    In 2011, it was estimated that only 33% of the 2010 population had returned to breed, less than 80,000 cuttlefish. Beginning in May, the cuttlefish leave deep water and migrate along coastal reefs to reach their spawning grounds. Local fishermen claim that a small "finger of land" near Point Lowly extends outside the exclusion zone and that commercial fishers have been targeting the area, intercepting the Sepia apama before they can reach the spawning grounds. Being semelparous breeders, ecologist Bronwyn Gillanders believes the cuttlefish to be in danger, stating that it is hard to determine whether this a natural phenomenon or something else and that the cause requires more research.[15]

    In 2012, the number of cuttlefish that returned to the spawning ground again dropped dramatically with numbers as low as 6,000 estimated. A state government working group had been unable to determine the cause of the 2011 decline and have now recommended investigating broader ecological factors. Tour guide Tony Bramley, who had been taking divers to view the spawning grounds since they were discovered stated "It's heartbreaking, when you look at what's left...[once] there were so many animals you couldn't land on the bottom, you had to push them aside."[16] The Conservation Council of SA, which believes the population to be a separate species, has warned that the Spencer Gulf cuttlefish face extinction within two or three years if nothing is done to protect them. The state government working group had recommended an immediate ban on fishing for the cuttlefish, however, this was rejected by State Cabinet on 3 September with Fisheries Minister Gail Gago stating; "There is no strong evidence to suggest that fishing is impacting on the giant cuttlefish, therefore, further closures would be ineffective."[7]

    On 28 March 2013, the State Government introduced a temporary ban on fishing for cuttlefish in the northern Spencer Gulf for the 2013 breeding season. Fisheries Minister Gago announced that research into the reasons behind the 90% decline in the cuttlefish population had ruled out commercial fishing as a cause but was otherwise inconclusive and that further areas of Spencer Gulf would be closed in 2014.[17][18]

    Effect of local industrialisation[edit]

    In 1984, before the spawning grounds were discovered, Santos built a hydrocarbon processing plant at adjoining Port Bonython. There is some concern over the possible impact of the plant on the cuttlefish population and there have been two major spills at the plant.[19][20] Santos denies that the recent spill spread off-site, but the SA EPA said hydrocarbons had migrated through the rock strata beyond the plant and the barrier trench built by Santos. Santos now provides funding for cuttlefish research.[21]

    BHP Billiton has plans to build a desalination plant at Point Lowly to supply fresh water to Roxby Downs copper and uranium mine. The plant, located within 200 metres (660 ft) of the breeding grounds, would release around 120 megalitres (32,000,000 US gal) of brine (46–60 ppt) into the area each day. As cuttlefish embryos die off as salinity levels rise (optimal range 28–38 ppt, 100% mortality at 50 ppt), there has been considerable public opposition to the proposed plant because of the expected environmental impact.[21][22][23]

    Due to its proximity to the ore deposits of the Middleback Ranges, several mining companies have indicated they want to build petrochemical and diesel refining facilities at Port Bonython, adjacent to Point Lowly. A second wharf for the loading of iron ore, and possibly copper concentrates and uranium, is also planned. The Cuttlefish Coast Coalition has been formed to fight these proposed developments.[21]

    As a result of the above threats, in 2010 an application was made to list that population of Sepia apama in the list of threatened species. On February 2, 2011, the Threatened Species Scientific Committee ruled the species was not eligible for listing as the affected population was not taxonomically distinct from the rest of Sepia apama for the purposes of the Act.[23]

    Sepia apama in popular culture[edit]

    In May 2009, D'Faces of Youth Arts and Snuff Puppets produced a live theatre performance for Come Out Festival. It featured several large cuttlefish puppets and appeared in Adelaide's Victoria Square, at the Adelaide Airport and at a Whyalla performance. There was some controversy surrounding the performances after a participant in the project was openly critical of the plan to build a desalination plant at Point Lowly.[24] The major sponsor of Come Out Festival in 2009 was the BHP Billiton Youth Fund, the same company which proposes to construct the desalination plant. The over-arching theme of the festival that year was 'Colliding Worlds'.[25] BHP Billiton has not sponsored the Come Out Festival since the 2009 event.

    Stobie the Disco Cuttlefish at Adelaide Fringe Festival 2014

    During the Adelaide Fringe Festival in March 2012, the RiAus presented Sepia, an original work by Welsh playwright, Emily Steel.[26] Set in Whyalla, the play told the story of the fictitious character Neil, the proprietor of a caravan park who was struggling to come to terms with the cuttlefish decline whilst trying to keep his family together. The play also featured at the Melbourne Fringe Festival.[27] Presenting partner RiAus is sponsored by the oil and gas company Santos. Santos was responsible for hydrocarbon groundwater contamination at Port Bonython, adjacent to the cuttlefish breeding grounds, first discovered in 2008.

    In 2014, the Adelaide Fringe Festival launched Stobie the Disco Cuttlefish, a 13 m long electrified cuttlefish puppet, equipped with strobing, coloured lighting and a sound system. Stobie the Disco Cuttlefish first appeared during the Adelaide Fringe Opening Parade, then performed with a troupe of dancers each Saturday night during the festival.[28] The soundtrack to the performance included samples from The Beegees hit 'Stayin' Alive'[29] and the entire theme song from the movie Fame.

    The mass aggregation of Sepia apama at Point Lowly has inspired the development of a retro arcade game called Cuttle Scuttle which is scheduled for release in 2014.[30]

    See also[edit]

    References[edit]

    1. ^ Barratt, I. & Allcock, L. 2012. Sepia apama. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2. <www.iucnredlist.org>. Downloaded on 27 October 2012.
    2. ^ "Giant Cuttlefish - Sepia apama". Australian Museum. Retrieved 27 August 2014. 
    3. ^ Reid, A., P. Jereb, & C.F.E. Roper 2005. Family Sepiidae. In: P. Jereb & C.F.E. Roper, eds. Cephalopods of the world. An annotated and illustrated catalogue of species known to date. Volume 1. Chambered nautiluses and sepioids (Nautilidae, Sepiidae, Sepiolidae, Sepiadariidae, Idiosepiidae and Spirulidae). FAO Species Catalogue for Fishery Purposes. No. 4, Vol. 1. Rome, FAO. pp. 57–152.
    4. ^ Norman, M.D. 2000. Cephalopods: A World Guide. ConchBooks.
    5. ^ a b c d e Amendment to the list of Threatened Population under the Environment Protection and Biodiversity Conservation Act 1999 (EPBC Act). Threatened Species Scientific Committee.
    6. ^ a b c d e f Natural History of the Giant Australian Cuttlefish BHP Billiton
    7. ^ a b c Clare Peddie, Heather Kennett The cuttle scuttle The Advertiser September 29, 2012 Pg 67
    8. ^ Silvery fish reflect polarised light; they reflect the same amount of light in the same direction as the light they are viewed against, making them almost invisible in water. If the polarisation is reduced, the fish become easily visible. Cuttlefish will ignore fish with reduced polarisation and preferentially attack fish emitting polarised light.[1]
    9. ^ Mäthger et al (April 21, 2009). "Do cephalopods communicate using polarized light reflections from their skin?". The Journal of Experimental Biology 212, 2133-2140. Retrieved 4 November 2011. 
    10. ^ Alison King The Colourful World of Cephalopods - Cephalopod body patterning II. The Cephalopod Page.
    11. ^ Hanlon, R.T. 2008. Australian Giant Cuttlefish - Physiology and Biochemistry. Encyclopedia of Life.
    12. ^ Aitken, J.P., R.K. O'Dor & G.D. Jackson. 2005. The secret life of the giant Australian cuttlefish Sepia apama (Cephalopoda): Behaviour and energetics in nature revealed through radio acoustic positioning and telemetry (RAPT). Journal of Experimental Marine Biology and Ecology 320: 77–91.
    13. ^ Catch cuttlefish, drain off the ink, then fillet. Serves five (dolphins): Scientists stunned by mammals' elaborate culinary preparations
    14. ^ a b MA Steer and KC Hall Estimated Abundance and Biomass of the Unique Spawning Aggregation of the Giant Australian Cuttlefish (Sepia apama) in Northern Spencer Gulf, South Australia. PIRSA October 2005
    15. ^ Mystery of the Missing Cuttlefish. The Advertiser, July 24, 2011. p. 7.
    16. ^ Drastic loss in giant colony. The Advertiser, September 25, 2012. p. 24.
    17. ^ "Cuttlefish update". Primary Industries and Regions SA. Primary Industries and Regions SA. Retrieved 25 June 2013. 
    18. ^ AAP (27 March 2013). "Giant cuttlefish decline prompts catch ban parts of South Australia's Spencer Gulf". The Advertiser. Retrieved 25 June 2013. 
    19. ^ http://www.amsa.gov.au/marine_environment_protection/major_oil_spills_in_australia/Era/index.asp
    20. ^ http://www.abc.net.au/news/2010-03-22/epa-fears-bigger-santos-oil-spill/374516
    21. ^ a b c Cuttlefish chaos at Whyalla. Archived from Dive Pacific Issue No. 116, Feb/Mar 2010.
    22. ^ Desalination and South Australia's Gulfs ecosystems. Fishers For Conservation Inc.
    23. ^ a b Conservation Assessment. Advice to the Minister for Sustainability, Environment, Water, Population and Communities from the Threatened Species Scientific Committee (the Committee) on Amendment to the list of Threatened Population under the Environment Protection and Biodiversity Conservation Act 1999 (EPBC Act) February 2, 2011.
    24. ^ McDonald, Patrick "Fun with a serious message as Come Out'09 launched" The Advertiser, South Australia (2009-05-17). Retrieved 2014-01-22.
    25. ^ Come Out Festival 2009 Program Come Out Festival, South Australia (2009). Accessed 2014-01-22.
    26. ^ Fuss, Eloise "Cuttlefish controversy takes centre stage" ABC North & West SA, South Australia (2012-02-17). Retrieved 2014-02-20.
    27. ^ Sepiatheplay.com Accessed 2014-01-21.
    28. ^ Keen, Suzie "Record line-up for 2014 Adelaide Fringe" InDaily (2013-11-29)
    29. ^ Disco Cuttlefish - Adelaide Fringe Festival (2014). Accessed 2014-02-20.
    30. ^ "Cuttle Scuttle" Facebook.com. Accessed 2014-06-13.
    • Kassahn, K.S., S.C. Donnellan, A.J. Fowler, K.C. Hall, M. Adams & P.W. Shaw 2003. Molecular and morphological analyses of the cuttlefish Sepia apama indicate a complex population structure. Marine Biology 143(5): 947–962. doi:10.1007/s00227-003-1141-5
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