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On the validity of the Trieste Flatfish: dispelling the myth.

In 1960, the first-ever manned dive to the deepest place on earth (11,000 m) took place. The pilots reported that on contact with the seafloor they observed a 'flatfish." This story captured the public imagination yet bears no scientific credibility. In the myriad of publicity surrounding James Cameron's latest dive, some 52 years later, the story of the flatfish is once again being perpetuated in the popular media, misinforming the public about deep-sea biology. This study attempts to dispel the story of the flatfish by exploring more recent developments in deep-sea exploration and biological research: (1) the mismatch of depths compared with fish of similar body form, (2) an improbable window of opportunity to have made the observations, (3) the absence of fish from other cameras deployed in the trenches, (4) the absence of fish from subsequent exploration of the area, and (5) new hypotheses that predict that fish are, at a cellular level, physiologically incapable of surviving at depths greater than 8500 m. On the basis of all these aspects, it is clear that the Trieste flatfish story is either a misidentification or entirely erroneous.

On the 23rd of January 1960, the Bathyscaphe Trieste descended to the deepest place on Earth--Challenger Deep (10,916 m) in the Mariana Trench, Central Pacific Ocean. This exercise represented the first human presence in the deepest part of the oceans. Such an achievement was understandably embroiled in a myriad of publicity at the time, and the story of Jacques Piccard and Don Walsh's exploit has been told in the contexts of ocean exploration and human endeavor ever since. The legendary status of the Trieste dive is founded not only upon being the first to achieve such feats but also to have remained the only humans to have done so for more than 50 years.

The story of the Trieste is once again at the forefront of popular science news and media, partly due to the 50th anniversary of the dive in 2010 and more recently as a result of the X Prize Foundation competition to construct a manned submersible capable of transporting humans to and from the deepest place on Earth. This "race" to Challenger Deep involved several competitors including high-profile personalities such as Virgin Group Chairman Sir Richard Branson, Google founder Eric Schmidt, and the Hollywood film producer James Cameron, who recently won the race.

While this renewed and high-profile interest in sending humans to Challenger Deep represents a ground-breaking endeavor in terms of new deep-submergence technology, promotion of the deep-sea environment, and inspiration for future generations of scientists and technologists, it has also resurrected details from the Trieste story that are misleading and most likely erroneous. Recent media coverage has brought the story of the "Trieste flatfish" back into the public arena. The story relates to a flatfish observed through the viewport of the Trieste by Jacques Piccard at nearly 11,000 m deep. Very little was known about the geographic and bathymetric distribution of deep-sea fauna at the time of the dive, and the story of the flatfish sighting was heralded as proof that life exists at full ocean depth and provided the kind of detail that made the dive such a success and so popular. However, 50 years on from the Trieste dive, considerable progress has been made in understanding the bathymetric distribution of fish and exploring the trenches, and despite the ever-increasing wealth of information to suggest that the flatfish sighting is dubious, the story still persists. For example, Philippe Cousteau Jr., an environmental advocate, even related this story live on CNN to an international audience of presumably millions on the 29th of February 2012. The questionable nature of this story is not even new; within a year of the Trieste dive, an expert in trench biology published an article in Nature specifically casting doubt on the flatfish story (1) but was widely ignored by the public media.

It is the scientific community's responsibility to ensure that, where possible, scientific findings are portrayed to the public via mass media outlets in a correct and responsible manner to prevent the perpetuation of misleading or erroneous findings. The story of the Trieste flatfish requires reexamination in an attempt to distinguish fiction from fact.

The Trieste reached the bottom of the Challenger Deep after a 5-h descent and upon landing resuspended considerable seabed sediments. The bathyscaphe remained on the bottom for 20 min before ascending back to the surface. Jacques Piccard said of the sighting, "Lying on the bottom just beneath us was some type of flatfish, resembling a sole, about 1 foot long and 6 inches across. Even as I saw him, his two round eyes on top of his head spied [us, and] ... extremely slowly, this flatfish swam away. Moving along the bottom, partly in the ooze and partly in the water, he disappeared into his night" (2).

However, Don Walsh recounted a slightly less detailed version: "As we landed, a cloud of sediment was stirred. This happened with all of our dives and usually after a few minutes it would drift away. Not this time. The cloud remained for the entire time on the bottom and showed no signs of moving away. It was like looking in a bowl of milk" (3).

More recently Walsh stated "Just before we landed we spotted what appeared to be a small, whitish flatfish resting on the seafloor. We judged it about a foot long. Jacques was at the window and made the sighting." He also said "In the half century since our dive, there has been some speculation that we did not see a flatfish. And this is entirely possible. Neither Jacques nor I were trained biologists and the critter could have been something else" (4).

This latest account of the story appears to be the first time that Walsh has cast doubt on the accuracy of the observation, and unfortunately Jacques Piccard died in 2008. Also, the Trieste was not equipped with any imaging equipment and therefore there are no photographs to corroborate the story.

Shortly after the Trieste dive, Torben Wolff of the Zoological Museum at the University of Copenhagen, Denmark, an expert in trench fauna having participated in the RV Galathea expeditions in the 1950s, published an article in Nature reporting on the deepest recorded fishes (1). The majority of this, albeit short, article is dedicated to questioning the validity of the Trieste observation. Wolff described the sighting as "somewhat dubious" in that flatfish are rarely found beyond 1000 m and the Danish Galathea and Soviet Vityaz expeditions did not find fish deeper than 7587 m despite multiple trench-sampling campaigns using a variety of methods successful in recovering representatives of most major taxa. He concluded that the flatfish was far more likely to have been a holothurian, in particular the bathypelagic "cushion shaped" Galatheathuria aspera, which is white, oval, and about a foot long.

Three years later, Jorgen Nielson, another expert on deep-sea fish, reiterated the point that the flatfish "was in reality probably not a fish" (5). In 1977, the same author published a description of Abyssobrotula galathea, which is thought to be the deepest living fish (6). A. galathea is an ophidiid (cusk eel) and was trawled from the Puerto Rico Trench from a depth of 8370 m in 1970. This fish is still considered to be the deepest living fish by the deep-sea biology community.

There is a multitude of new evidence to suggest the Trieste flatfish does not exist. Firstly, the description of the Trieste fish ranges from "flatfish" to "flounder-like," to "sole," suggesting that the observers were confident that the fish was of the order Pleuronectiformes (dabs, flounders, halibuts, plaice, sole, tonguefishes, turbots, and whiffs) of which there are 570 species, known to live in shallow to moderate depths in arctic, temperate, and tropical localities. Flatfish are primarily a littoral order with some bathyal representatives, but they lack an abyssal species, let alone a hadal one (1). This is evident when extracting bathymetric data for all known Pleuronectiformes from http://www.Fishbase.org (7), the largest online repository for fish data. Although there are several species with a maximum depth exceeding 1500 m, most have typically shallower depth ranges, suggesting that the deeper records are either rare or spurious. Giving the benefit of the doubt, the Pleuronecti-formes depth range data shows the Trieste flatfish to be 7916 m deeper than the deepest known flatfish and 8916 m deeper than the next deepest flatfish (Fig 1 a). It appears improbable that one species would be so far removed bathy-metrically from all others in the same order.

The next most suitable fish with similar body forms are skates and rays, but they are also found principally at shallower depths. A study showed that Chondrichthyes (cartilaginous fishes including rays and skates) are absent from the abyssal zone (8). The maximum depths of 669 species of Chondrichthyes place the Trieste flatfish 7241 m deeper; therefore it appears highly unlikely to be a ray or skate.

The next question is the likelihood of observing a fish in the few seconds the observers had between being in visual range of the seafloor and being engulfed by the resuspended sediment. It can be assumed that this would have been on the order of seconds. The University of Aberdeen's Oceanlab (UK) has been using a fleet of free-fall baited camera landers to study deep-sea fish for 30 years. It is estimated that Oceanlab has carried out close to 400 deployments at depths ranging from 100 m to 9900 m in most major oceans. Regardless of location and species present, there has never been a case of landing on a fish. With baited cameras, there is, however, a linear global trend of first fish arrival time with depth (9) that ranges from about 30 min at depths above 2000 m to more than 2 h below 6000 m; thus if fish were at 10,000 m or more, the predicted arrival time would be close to 10 h. Furthermore, the Trieste did not have bait as an attractant.

Since the Trieste, two more deep-submergence vehicles have explored Challenger Deep. Both are remotely operated vehicles (ROVs): the Japanese Kaiko (10) and the American Nereus (11). By the time of its loss in 2003, Kaiko had completed more than 20 dives to full ocean depth, which presumably resulted in hundreds of hours of film footage, and yet no fish were ever found. Likewise, in 2009, the ROV Nereus completed two successful dives to over 10,900 m in Challenger Deep. In over 13 h of continual bottom time, no fish were encountered (11).

Linear regression of the log species numbers of all known fish records from http://www.FishBase.org (9360 records) predicts a maximum depth of fish to be between 8000 and 8500 m (8), which coincides with the Abyssobrotula galathea specimen found at 8370 m (6). This would still place the Trieste flatfish nearly 3000 m deeper than any other fish (Fig. 1b).

The HADEEP projects (Universities of Aberdeen, UK, and Tokyo, Japan, and NIWA, New Zealand) have conducted baited camera surveys in five hadal trenches of the Pacific Rim since 2007. To date there have been 29 deployments between 4500 and 9900 m and the most conspicuous trend is the presence of fish at depths less than 8000 m and the complete absence of fish deeper than 8000 m. Furthermore, the fish found living closer to 8000 m do not diminish in numbers but still appear in large aggregations (12), (13). Generally, the deep-sea fishes found at the lower abyssal depths are macrourids (rat-tails) and ophidiids (cusk-eels), and at hadal depths, liparids (snailfish). To date, the deepest fish seen alive was the snailfish Pseudoliparis amblysto-mopsis at 7703 m in the Japan Trench (12).

In addition to the observational data, there is growing theoretical evidence to suggest why fish do not inhabit depths greater than 8000-8500 m. One of the defining characteristics of the deep sea is hydrostatic pressure; there-fore, adaptation to such pressure is a prerequisite to survival in the deep trenches. Hydrostatic pressure can have large perturbing effects on biological molecules. Proteins from deep-sea organisms have been found to have structural adaptations that confer pressure resistance (14). However, many proteins from deep species, while having evolved a degree of pressure resistance, still retain some sensitivity. In recent years a different adaptation to pressure involving "piezolytes" has been hypothesized. These are small organic solutes first discovered as osmolytes, solutes accumulated by most marine organisms to prevent osmotic shrinkage of their cells by osmoconforming to the environment (osmotic pressure of about 1000 mOsm). Among the main osmolytes in many marine animals is trimethylamine oxide (TMAO). In contrast to osmoconformers, shallow-living marine Osteichthyes (bony fish) are osmoregulators, maintaining an internal osmotic pressure of about 300-400 mOsm with some TMAO, but only at about 40-50 mOsm.

Many organic osmolytes are not simply used for regulating osmosis. Many of them stabilize macromolecules and can counteract a variety of perturbants (15). This may be of fundamental importance to deep-sea adaptation, because analyses of deep-sea bony fishes have revealed that TMAO contents increase with depth (16), (17), resulting in an increase in internal osmotic pressure. In the laboratory, TMAO counteracts the perturbing effects of hydrostatic pressure on enzyme kinetics and protein stability and assembly (15), (18), (19), (20). Thus, it is hypothesized that TMAO (and perhaps other stabilizing osmolytes), acting as piezolytes, help organisms adapt to the deep-sea, and that the ability to accumulate such solutes may limit depth distributions.

TMAO analyses have only been done on fishes down to 4900 m, but they do show a clear linear increase with depth. When the trend of increasing TMAO in bony fishes with depth is extrapolated to hadal depths, the point at which the fishes would become isosmotic (osmoconforming) with seawater is 8000-8500 m, coinciding nicely with the maximum depth of fish from database records and observational data. If this extrapolation proves to be correct, fish might be unable to live deeper because they would need more TMAO, making them hyperosmotie to seawater.

All the evidence suggests that it is highly improbable that a bathyscaphe would land on a fish at all and that it would be a flatfish (or even a ray or skate). For a species of fish, especially one with such a high profile, to have gone unnoticed in subsequent Kaiko and Nereus dives to the same area also seems highly unlikely. Furthermore, the growing evidence from global database records, cutting edge trench research, and novel physiological hypotheses all suggest that Piccard did not see a flatfish, but rather perhaps a large holothurian (1).

With a new wave of trench exploration at our doorstep, and given that environmental research is perhaps more pertinent now than ever, new and potentially inspiring events such as the race to the Challenger Deep must be accompanied by sound scientific fact.

Received 12 April 2012; accepted 6 May 2012.

* To whom correspondence should be addressed. E-mail: a.jamieson@abdn.ac.uk

Literature Cited

(1.) Wolff, T. 1961. The deepest recorded fishes. Nature 190: 283-284.

(2.) Piccard, J., and R. S. Dietz. 1961. Seven Miles Down. Longmans. London.

(3.) Walsh, D. 2009. In the beginning ... A personal view. Mar. Technol. Soc. J. 43: 9-14.

(4.) Burton, A. 2012. Way down deep. Front. Ecol. Environ. 10: 112.

(5.) Nielsen, J. G. 1964. Fishes from depths exceeding 6000 meters. Galathea Rep. 7: 113-124.

(6.) Nielson, J. G. 1977. The deepest living fish Abyssobrotula galathea. A new genus and species of oviparous ophidiids (Pisces, Brotulidae). Galathea Rep. 14: 41-48.

(7.) Frouse, R., and D. Pauly. 2012. FishBase. World Wide Web electronic publication. [Online]. Available: http://www.fishbase.org [2012, June 6].

(8.) Priede, 1. G., R. Froese, D. M. Bailey, 0. A. Bergstad, M. A. Collins, J. E. Dyb, C. Henriques, E. G. Jones, and N. King. 2006. The absence of sharks from abyssal regions of the world's oceans. Proc. R. Soc. Lond. B Biol. 273: 1435-1441.

(9.) Jamieson, A. J., T. Fujii, M. Solan, A. K. Matsumoto, P. M. Bagley, and I. G. Priede. 2009. Liparid and macrourid fishes of the hadal zone: in situ observations of activity and feeding behaviour. Proc. R. Soc. Lond. B Biol. 276: 1037-1045.

(10.) Mikagawa, T., and M. Aoki. 2001. An outline of RN Kairei and recent activity of the multichannel seismic reflection survey system (MCS) and ROV Kaiko. J. Mar. Sci. Tech. 6: 42-49.

(11.) Fletcher, B., A. Bowen, D. R. Yoerger, amd L. L. Whitcomb. 2009. Journey to the Challenger Deep: 50 years later with the Nereus hybrid remotely operated vehicle. Mar. Technol. Soc. J. 43: 65-76.

(12.) Fujii, T., A. J. Jamieson, M. Solan, P. M. Bagley, and I. G. Priede. 2010. A large aggregation of liparids at 7703 m depth and a reappraisal of the abundance and diversity of hadal fish. BioScience 60: 506-515.

(13.) Jamieson, A. J., N. M. Kilgallen, A. A. Rowden, T. Fujii, T. Horton, A.-N. Lorz, K. Kitazawa, and I. G. Priede. 2011. Bait-attending fauna of the Kermadec Trench, SW Pacific Ocean: evidence for an ecotone across the abyssal-hadal transition zone. Deep-Sea Res. I 58: 49-62.

(14.) Hochachka, P. W., and G. N. Somero. 2002. Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford University Press, Oxford.

(15.) Yancey, P. H. 2005. Organic osmolytes as compatible, metabolic, and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208: 2819-2830.

(16.) Kelly, R. H., and P. H. Yancey. 1999. High contents of trimethylamine oxide correlating with depth in deep-sea teleost fishes, skates, and decapod crustaceans. Biol. Bull. 196: 18-25.

(17.) Samerotte, A. L, J. C. brazen, G. L. Brand, B. A. Seibel, and P. H. Yancey. 2007. Correlation of trimethylamine oxide and habitat depth within and among species of teleost fish: an analysis of causation. Physiol. Biochem. Zool 80: 197-208.

(18.) Yancey, P. 11., and J. F. Siebenaller. 1999. Trimethylamine oxide stabilizes teleost and mammalian lactate dehydrogenases against inactivation by hydrostatic pressure and trypsinolysis. J. Exp. Biol. 202: 3597-3603.

(19.) Yancey, P. H., A. L. Fyfe-Johnson, R. H. Kelly, V. P. Walker, and M. T. Aunon. 2001. Trimethylamine oxide counteracts effects of hydrostatic pressure on proteins of deep-sea teleosts. J. Exp. Zool. 289: 172-176.

(20.) Yancey, P. H., M. D. Rhea, K. M. Kemp, and D. M. Bailey. 2004. Trimethylamine oxide, betaine and other osmolytes in deep-sea animals: depth trends and effects on enzymes under hydrostatic pressure. Cell. Mol. Biol. 50: 371-376.

ALAN J. JAMIESON, (1) * AND PAUL H. YANCEY (2)

(1.) Oceanlab, University of Aberdeen, Institute of Biological and Environmental Science, Main Street, Newburgh, Aberdeenshire, AB4I 6AA, United Kingdom; (2.) Biology Department, Whitman College, Walla Walla, Washington 99362
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Author:Jamieson, Alan J.; Yancey, Paul H.
Publication:The Biological Bulletin
Article Type:Report
Geographic Code:4EUUK
Date:Jun 1, 2012
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