Mantles Most Splendid: Tridacna spp.

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Giant clams (Tridacna spp.) on display at the California Academy of Sciences in San Francisco.  There are more or less seven species of giant clams inhabiting the shallow tropical reefs of the Indo-Pacific (Klumpp, Bayne, & Hawkins 1991).  Image credit: California Academy of Sciences / Curious Sengi.

The elegant shapes and colorful patterns of shells often define the identity of the molluscs we encounter and gleefully collect.  But what we hold in our hands is a largely inert structure of calcium carbonate, devoid of its occupant, its essence incomplete.  What is missing are the squishy bits — the animal itself.  The soft tissues of clams and snails can be breathtaking in their colors and patterns.  One of the better known examples of this are the giant clams, Tridacna spp.

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Discarded shells of the largest clam in the world, Tridacna gigas.  Image credit: David Hall via Arkive.

Residing the shallow sunlit seas of the tropical Indo-Pacific, tridacnids are the largest clams in the world, with one individual measuring 1.4 m (4.6 ft) in length and 263 kg (863 lbs) in weight (Beckvar 1981).  While the shells have been collected as curios for their child-bathtub-sized novelty and undulating, fluted edges, there is little else that stands out about these shells.  What is mind-blowing about tridacnids are the vivid colors and patterns of iridescent blue, green, black, yellow, brown and violet of the exposed living tissue, the mantle.

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Tridacnid spotted off Thailand.  Image credit: Walkabout Alex.

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Get close to a world of color and fascination!  Detail of siphon and feathery gills.  Image credit: Fatherree via Reefs.com.

What makes these fleshy frills so psychedelic is a complex interplay between the tridacnid clam and its unicellular dinoflagellate symbionts called zooxanthellae.  The zooxanthellae primarily reside in the upper layers of tissue of the enlarged mantle and siphon, where they are exposed to sunlight and photosynthesize.  The simple sugars that are the result of photosynthesis — glucose and glycerol — are released into the bloodstream, thus providing a source of energy for the tridacnid (Goreau, Goreau, & Yonge 1973; Morton 1978; Fitt & Trench 1981; Wilkins 1986; Buck, Rosenthal, & Saint-Paul 2002).  Generally, clams are filter feeders, drawing in water and sorting out all the plankton and organic particulates for digestion.  While giant clams retain a fully functional and efficient filter feeding apparatus, the clear, nutrient-sparse waters of the tropics has likely driven the evolution of symbiotic relationships that provide alternate energy sources.  Adult tridacnids can probably sustain themselves on photosynthates alone and it is hypothesized that this influx is behind the spectacular growth rate of approximately 100 mm (4 in) per year observed in the species Tridacna gigas (Bonham 1965; Klumpp, Bayne, & Hawkins 1991).

zooxanthellae

Zooxanthellae live as free cells into a branched tubular system running under the surface of the mantle and siphon tissue (Buck, Rosenthal, & Saint-Paul 2002).  Giant clams acquire symbiotic zooxanthellae through the environment; at around 20 to 25 days old, after the floating larvae settles into a more benthic post-metamorphic state, the clam ingests motile zooxanthellae.  How the symbionts are transferred from the stomach into the visceral and mantle tissues is unknown.  Growth accelerates after acquisition of symbionts (Jameson 1976; Fitt & Trench 1981).  Interestingly, free-living zooxanthellae will keep all products of photosynthesis inside their cell, but the presence of host tissues causes photosynthates like glucose and glycerol to be secreted, suggesting some kind of chemical regulation by the host (Muscatine 1967).  The purple spots are reflective iridophores.  Image credit: Science Photo Library via Getty Images.

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What does the nuclear tests off Bikini Atoll have to do with giant clams?   Bonham (1965) was able to calculate growth rates of T. gigas from Bikini Atoll by correlating dates of atomic tests and the deposition of radioactive strontium-90 in the growing shell.  Measuring from one radioactive growth line to the next, one specimen measured 10 cm long during the 1956 atomic tests and then 24 cm during the 1958 tests, indicating a growth rate greater than any other bivalve.  Image credit: Getty Images via The Independent.

So here is our first color component:  zooxanthellae use green chlorophyll and a red carotenoid called peridinin as photosynthetic pigments, rendering the single-celled organisms a brown or reddish-brown color (Fatherree 2007).

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T. squamosa.  Image credit: Wikimedia Commons.

The host clam itself generates accessory pigments — greens, browns, and yellows — that extend the range of usable wavelengths of light available for the symbiont’s photosynthesis (Fatherree 2007).  In addition, specialized cells (iridocytes) form clusters in the mantle called iridophores that act both as reflectors to redirect light into deeper tissue and as a sunscreen to prevent the zooxanthellae from getting fried from intense sun exposure.  Each iridocyte contains a stack of crystalline reflective platelets that scatter light, which makes pigments appear more vivid, creates those eye-popping electric blue-green colors, and makes the mantle shimmer with iridescence (Goreau, Goreau, & Yonge 1973; Griffths, Winsor, & Luong-Van 1992; Fatherree 2007; Todd, Lee, & Chou 2009).

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Iridescent sheen on the blue lip of this tridacnid.  Possible hybrid between T. noae and T. maxima.  Image credit: Jake Adams via Reef Builders.

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Blue-rimmed T. derasa.  Image credit: Ora Farm.

Photosynthetic pigments of zooxanthellae, accessory pigments and iridophores of the host tridacnid clam completes the palette of colors.  But how are these colors arranged into striped, spotted, and mottled patterns?  While variation in color is caused by localization of zooxanthellae (Todd, Lee, & Chou 2009), the pattern-generating mechanism remains unknown.  Despite some broad parameters of patterning seen between species, the role of genes remain ambiguous.  Offspring are observed to have a tremendous variety of colors and patterns different from their parents, suggesting a weak genetic link (Fatherree 2007).

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Bed of giant clams at low tide on Orpheus Island.  Image credit: goestaf via Panoramio.

Much of the tridacnid’s anatomy and behavior is focused on fostering the intimate relationship with their zooxanthellae symbionts.  The super-sized mantle and siphon blossom from the shell during the day and orient themselves to the light like flowers tracking the sun (Morton 1978; Wilkins 1986). This makes the exposed fleshy parts vulnerable to predation, especially from roaming fish looking for a quick bite.  Tridacnids do have several hundred well-developed pinhole eyes along the mantle and siphon that can detect shadows and moving objects, triggering immediate retraction and closing of the shell (Wilkins 1986; Land 2003; Todd, Lee, & Chou 2009).

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Giant clam researcher, Dr. Rick Braley, demonstrates a defensive response in T. gigas — squirting powerful jets of water upon tactile stimulus (Wilkins 986).  Image credit: Aquasearch.

However, responding to each threat by clamming up is hardly beneficial to the zooxanthellae that need to be exposed for hours a day for photosynthesis.  Todd, Lee, and Chou (2009) hypothesized that the colors and patterns of the mantle are actually cryptic, breaking up the outline of the animal and camouflaging it against the cluttered background of the reef.  High levels of morphological variation, i.e., polymorphism, is common in organisms inhabiting complex and unpredictable environments.  Analysis of RGB color values of mantles and background reef substrate indicate some color matching camouflage against fish predators with trichromatic color vision.  That a given set of parents spawns wildly polymorphic offspring might be a bet-hedging strategy that potentially some of the dispersing larvae will match their given substrate.  This also allows for colonization of a large range instead of being limited to one type of microhabitat for which they are a perfect background match.

color-morphs

A study of color and pattern polymorphism in T. crocea by Todd, Lee, and Chou (2009) identified eight general color morphs in this species.  Larger individuals tended more towards greens and browns, while smaller individuals were vivid blue.  The researchers hypothesized a tradeoff:  that the blue structural color caused by iridophores act as a sunscreen that might be more vital to smaller clams than larger ones.  Image credit:  Todd, Lee, & Chou 2009.

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T. gigas and diver.  Image credit: Rick Hankinson via Wikimedia Commons.

Though the flamboyant mantles of tridacnids may serve to hide the clams from predators, they have captured the attention of human collectors.  Giant clams have long been an easily-accessible and prized food source for native Pacific Islanders.  With the opening up of global markets, tridacnid meat and shells have come into high demand, quickly exhausting local stocks (Jameson 1976; Benzie & Williams 1995; Foyle et al. 1997).  Overfishing has stimulated successful efforts at industrial-scale aqua- and mariculture (Klumpp, Bayne, & Hawkins 1991).  However, the heavy investment necessary to build large nursery facilities and the seven year growing time to bring species like Tridacna gigas to meat harvesting size was not within reach of many communities throughout the Indo-Pacific.  Instead, villagers have turned their attention to smaller species like T. crocea, T. maxima, and T. squamosa for the saltwater aquarium trade.  It only takes five to seven months for those species to reach a size suitable for shipping, making this an economical feasible option (Foyle et al. 1997).  The ability to breed tridacnids in captivity also creates opportunities to reseed depleted reefs (Beckvar 1981).

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T. maxima farmed for the aquarium trade.  More intense blue and green colors seem characteristic of smaller clams (Todd, Lee, & Chou 2009).  Image credit: PacificEastAquaculture via ReefEdition.

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Solomon Island local, Erik Koti, cleaning T. maxima and T. derasa in a family-run enterprise to raise giant clams for the aquarium trade.  Koti was trained by WorldFish Center and WWF in sustainable aquaculture methods.  Image credit: Jürgen Freund.

The success of raising tridacnids in captivity may have saved them from overfishing, but there is a new threat, one that impacts all marine creatures with photosynthetic zooxanthellae.  The symbiont in giant clams is a dinoflagellate named Symbiodinium microadriaticum, and this same species is supposedly found in all reef-building corals, many sea anemones, gorgonians (sea fans), and the Upside-Down Jellyfish, Cassiopeia (Fitt & Trench 1981).  With warming of ocean surface waters, symbiotic zooxanthellae are expelled, leaving their hosts bleached white.  One experiment recreated the conditions for an observed bleaching event on the Great Barrier Reef of Australia and determined that increased light intensity and water temperature were the main factors resulting in loss of zooxanthellae.  It is unclear whether the zooxanthellae are leaving or if they are being ejected by their hosts (Buck, Rosenthal, & Saint-Paul 2002).  In some cases, bleaching is a temporary loss of color that can last well over a year.  But in more severe cases, the damage is permanent — the spaces that once held zooxanthellae degenerate and the giant clam is left to struggle on its own, undoubtedly with poor outcomes (Norton et al. 1995).

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Localized bleaching in an animal for sale in the aquarium trade.  Stress from transport can cause loss of zooxanthellae.  Image credit: Fatherree via Reefs.com.

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Bleached and dead giant clam on Australia’s Great Barrier Reef.  Tridacnids derive the majority of their energy from their symbionts.  Rising water temperatures cause zooxanthellae to leave their hosts.  Image credit: Jake Adams via Reef Builders.

Incidence of coral reef bleaching is becoming more frequent and widespread.  This is not necessarily always fatal, but it does require immediate response to global climate change.

A clam is more than just its empty shell, to be discarded or set upon a shelf.  By delving into something as superficial as color and pattern, we have uncovered something about the essence of the tridacnid giant clam — the symbiotic relationship with zooxanthellae that is a vital focus of its form and function.

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Baby giant clams. Go, babies, go!  Image credit: Neo Mei Lin via Psychedelic Nature.

References

Beckvar, N.  1981. “Cultivation, Spawning, & Growth of the Giant Clams Tridacna gigas, T. derasa, & T. squamosa in Palau, Caroline Islands.”  Aquaculture 24:  21 – 30.

Bonham, Kelshaw.  1965.  “Growth Rate of Giant Clam Tridacna gigas at Bikini Atoll as Revealed by Radioautography.”  Science 149 (3681):  300 – 302.

Buck, Bela Hieronymous, Harald Rosenthal, & Ulrich Saint-Pail.  2002. “Effect of increased irradiance and thermal stress on the symbiosis of Symbiodinium microadriactum and Tridacna gigas.”  Aquatic Living Resources 15:  107 – 117.

Fatherree, James W.  2007.  “Why Do Tridacnids Look the Way They Look?”  Tropical Fish Magazine April 2007.  Accessed 17 September 2016.

Fitt, William K. & Robert K. Trench.  1981.  “Spawning, Development, & Acquisition of Zooxanthellae by Tridacna squamosa (Mollusca, Bivalvia).”  Biological Bulletin 161:  213 – 235.

Foyle, Timothy P., J.D. Bell, M. Gervis, & I. Lane.  1997.  “Survial and growth of juvenile fluted giant clams, Tridacna squamosa, in large-scale grow-out trials in the Solomon Islands.”  Aquaculture 148:  85 – 104.

Goreau, T.F., N.I. Goreau, & C.M. Yonge.  1973.  “On the utilization of photosynthetic products from zooxanthellae and of a dissolved amino acid in Tridacna maxima f. elongate (Mollusca:  Bivalvia).”  Journal of Zoology 169:  417 – 454.

Griffiths, D.J., H. Winsor, & T. Luong-Van.  1992.  “Iridophores in the Mantle of Giant Clams.”  Australian Journal of Zoology 40 (3):  319 – 326.

Jameson, Stephen C.  1976.  “Early Life History of the Giant Clams Tridacna crocea Lamarck, Tridacna maxima (Röding), and Hippopus hippopus (Linnaeus).”  Pacific Science 30 (3):  219 – 233.

Klumpp, D.W., B.L. Bayne, & A.J.S. Hawkins.  1991.  “Nutrition of the giant clam Tridacna gigas (L.). I.  Contribution of filter feeding and photosynthates to respiration and growth.”  Journal of Experimental Marine Biology and Ecology 155 (1):  105 – 122.

Land, Michael F.  2003.  “The spatial resolution of the pinhole eyes of giant clams (Tridacna maxima).”  Proceedings of the Royal Society B 270:  185 – 188.

Morton, Brian.  1978.  “The diurnal rhythm and the processes of feeding and digestion in Tridacna crocea (Bivalvia:  Tridacnidae).”  Journal of Zoology 185:  371 – 387.

Muscatine, Leonard.  1967.  “Glycerol Excretion by Symbiotic Algae from Corals and Tridacna and Its Control by the Host.”  Science 156 (3774):  516 – 519.

Norton, J.H., H.C. Prior, V. Baillie, & D. Yellowless.  1995.  “Atrophy of the Zooxanthellal Tubular System in Bleached Giant Clams Tridacna gigasJournal of Invertebrate Pathology 66:  307 – 310.

Todd, P.A., J.H. Lee, & L.M. Chou.  2009.  “Polymorphism & crypsis in the boring giant clam (Tridacna crocea):  potential strategies against visual predators.”  Hydrobiologia 635:  37 – 43.

Wilkens, Lon A.  1986.  “Visual system of the giant clam Tridacna:  Behavioral adaptations.”  Biological Bulletin 170 (3):  393 – 408.

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