Edward Forbes and His Azoic Hypothesis for a Lifeless Deep Ocean

Review Endeavour Vol.30 No.4

Deserts on the sea ﬂoor: Edward Forbes and his azoic hypothesis for a lifeless deep ocean

Thomas R. Anderson and Tony Rice

George Deacon Division, National Oceanography Centre, Southampton, UK SO14 3ZH

While dredging in the Ægean Sea during the mid-19th ship. The captain’s cabin became a laboratory-cum- century, Manxman Edward Forbes noticed that plants museum, where Forbes dissected and drew the animals and animals became progressively more impoverished collected and preserved them in bottles of alcohol. The the greater the depth they were from the surface of the captain and crew were there to help, although it is likely water. By extrapolation Forbes proposed his now infa- that some of the sailors were less than enthusiastic about mous azoic hypothesis, namely that life would be extin- the work involved. However, this work provided evening guished altogether in the murky depths of the deep entertainment for Forbes at least, who frequently turned ocean. The whole idea seemed so entirely logical given his artistic hand to drawing cartoons (Figure 2). the enormous pressure, cold and eternal darkness of this Forbes’ main aim was not, however, to describe the apparently uninhabitable environment. Yet we now animals themselves, but rather to understand their dis- know that the sea floor is teeming with life. Curiously, tribution across different types of habitat. Gathering it took 25 years for the azoic hypothesis to fall from together his results from the Ægean, the influence of depth grace. This was despite the presence of ample contrary was of obvious importance. ‘The sea-bed presents a series evidence, including starfishes, worms and other organ- of zones or regions,’ he wrote ‘each peopled by its peculiar isms that seemingly originated from the deep seabed. inhabitants’ [1]. Seaweeds dominated the uppermost lit- This is a tale of scientists ignoring observations that ran toral zone, below which came the laminarian zone – named counter to their deep-seated, yet entirely erroneous, for its characteristic large brown kelps but occupied also by beliefs. a myriad of fish and invertebrates. Next came the corraline zone, where the abundance of plants declined dramatically The azoic hypothesis in the fading light. Finally, a zone of deep-sea corals that Cruising in the Ægean Sea looking for weird and wonderful existed down to 230 fathoms provided refuge for only a few life-forms on the seabed, Edward Forbes (Figure 1) had an animals, including sponges and molluscs [2]. ‘The number unparalleled opportunity to pursue his great interest – the of species and of individuals diminishes as we descend,’ distribution of animals and plants in the sea. The year was exclaimed Forbes, ‘pointing to a zero in the distribution of 1841 and Forbes, a brilliant naturalist who is considered by animal life as yet unvisited’ [3]. By extrapolation, he many to be the founder of British marine biology, had reasoned that life would be extinguished altogether at a boarded the HMS Beacon under the captaincy of Thomas depth of around 300 fathoms (approximately 550 metres). Graves as part of a surveying mission to the eastern Mediterranean. Dredging in deep water in search of an Evolution of an idea underworld beneath the waves was, however, a major Born on 12 February 1815, it was not long before the undertaking. Although steam engines had been fitted in romantic beauty of his native Isle of Man was to captivate ships from the early years of the 19th century – by 1840 the the young Forbes and inspire him as a naturalist. He spent Royal Navy had no fewer than 50 paddle steamers – most hours arranging, classifying and drawing all manner of naval vessels, like the Beacon, were still driven entirely by objects, including minerals, fossils, shells, dried sea-weeds, the wind and had only man-powered capstans. In these hedge-flowers and dead butterflies. Indeed, by the age of 12 circumstances, it was difficult to maintain a constant he had founded a museum in his own home, and at 16 he course and speed for the duration of a deep dredge haul; left home for London intending to become an artist. The and hand-hauling a heavy, wet rope and a mud-filled Royal Academy refused to admit him. Instead, he followed dredge was time-consuming, backbreaking work. his mother’s wishes and enrolled at the University of Nevertheless, during the 18-month expedition, the crew Edinburgh to study medicine. As things turned out, Forbes of the Beacon made over 100 hauls of the dredge down to a never completed his course because he spent his every depth of 230 fathoms (some 420 metres). In the main, they spare minute pursuing his first love: natural history. Dred- conducted these operations from the Beacon’s tenders, ging the seabed in search of animal life held a particular which were marginally easier to control than the mother captivation for him, with expeditions to the Firth of Forth

Corresponding author: Anderson, T.R. ([email protected]). in May 1832, the Irish Sea around the Isle of Man in 1834 Available online 13 November 2006. and the Orkney and Shetland Islands in 1839. www.sciencedirect.com 0160-9327/$ – see front matter ß 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.endeavour.2006.10.003 132 Review Endeavour Vol.30 No.4

oaks and shrubs at higher altitudes [4]. In similar fashion, Forbes had noted the importance of the influence of eleva- tion above sea level on the distribution of pulmoniferous Mollusca (land snails) in Britain. The number of species declined with altitude until just a single species, Helix alliaria, could tolerate the exposed conditions near moun- tain summits [5]. Aquatic Mollusca were, however, Forbes’ favourite creatures (Figure 3), and it was his dredging studies around the British coasts that inspired the idea of depth-related zones of submarine life [6]. The parallel between terrestrial and marine systems was obvious: extreme environments, be they on the tops of mountains or at the bottom of the sea, would surely lead to extinction of life forms. In fact, the English geologist Henry de la Beche (1796– 1855) had already suggested the idea of a lifeless deep sea as early as 1834. ‘The surface of the deep ocean teems with animal life,’ he wrote, ‘and this is probably not less well proportionably tenanted down to depths where, from the want of necessary conditions, it ceases to exist’ [7]. The work of de la Beche would have been well known to Forbes, from his days as a student in Edinburgh. But it was to be Forbes’ own work in the Ægean, ten years later, that propelled the azoic hypothesis to prominence. His data provided clear evidence for an azoic zone; or so he believed. The scientific community readily embraced Forbes’ azoic hypothesis. It was, after all, so entirely logical. Figure 1. Portrait of Edward Forbes by J.H. Maguire, circa 1850. ßThe Royal Society. How could animals possibly withstand the pressure, cold and eternal darkness of the deep sea floor? The case was stated succinctly by the renowned Swiss-born naturalist By this time, the concept of zonation in land plants had and geologist Louis Agassiz (1807–1873): ‘The depths of the become established. Following his travels to Latin America ocean are quite as impassable for marine species as high between 1799–1804, the great German naturalist and mountains are for terrestrial animals...Not only are no explorer Alexander von Humboldt (1769–1859) remarked materials found there for sustenance, but it is doubtful if that the ‘organic development and abundance of vitality’ of animals could sustain the pressure of so great a column of plant life increased as one went from the poles towards the water’ [8]. Or, as eminent geologist David Page (1814– equator, with different zones of vegetation having their 1879) put it: ‘According to experiment, water at the depth own distinctive character. Furthermore, the same zonation of 1000 feet is compressed 1/340th of its own bulk; and at could be seen on tropical mountains: the palms and bana- this rate of compression we know that at great depths nas found at sea level being replaced by cypresses, pines, animal and vegetable life as known to us cannot possibly exist – the extreme depressions of seas being thus, like the extreme elevations of the land, barren and lifeless soli- tudes’ [9]. Yet we now know that the deep sea floor supports rich animal populations that in terms of species richness might outnumber tropical rainforests and shallow-water coral reef communities many times over [10]. So where did Forbes go wrong? Why did he not find an abundance of animals when dredging the depths of the Ægean Sea? A combination of two factors conspired against him. First, that area is one of the most oligotrophic (nutrient-poor) in the world, resulting in low abundance and few species. Second, the dredges available to Forbes were inefficient, a problem exacerbated by the relatively small size of species that are found there [11]. Danish biologist O.F. Mu¨ ller (1730–1784) might have been the first to use a dredge for scientific purposes. Mu¨ ller’s dredge was a rather coarse netting bag attached to a square iron frame with towing points at each corner Figure 2. Cartoon depicting dredging for marine fauna by Edward Forbes (frontispiece to [2]). Reproduced courtesy of the National Oceanic and (Figure 4a). With such a gaping mouth, it was vulnerable Atmospheric Administration/Department of Commerce. to losing its catch during hauling. By Forbes’ time the www.sciencedirect.com Review Endeavour Vol.30 No.4 133

Figure 3. British nudibranch molluscs (plate A.A.A from Forbes and Hanley, 1853 [26]). Reproduced courtesy of the Natural History Museum, London. preferred dredge (Figure 4b) had a much narrower mouth bottom, reducing the chances of catching one of the frame, smaller than but similar in design to the oyster relatively uncommon larger animals. To make matters dredges used by commercial fishermen. Furthermore, worse, the filtration efficiency of such a bag would have whereas commercial dredges had a lip or scraper for dig- been extremely low and it would rarely even catch the more ging into the seabed on only one of the long sides of their abundant, small mud-dwelling creatures. Forbes can mouths, the naturalists’ version had scrapers on both long therefore be forgiven for conjecturing, apparently quite sides so that it worked equally well either way up. For reasonably on the basis of his data, the flawed azoic dredging in deep water, presumably including his work in hypothesis for which he is often best remembered. But the Ægean, Forbes preferred a dredge bag made of canvas surely it would be only a matter of time before the truth with eyelet holes rather than a rope network [12]. But such was established and accepted by the scientific community? a dredge would fill rapidly with mud once it reached the As events transpired, this took 25 years. www.sciencedirect.com 134 Review Endeavour Vol.30 No.4

Figure 4. Early bottom samplers (not to scale): (a) Otto Frederick Mu¨ ller’s dredge ([20], p.239); (b) Edward Forbes’ dredge ([12], p.405); (c) John Ross’s deep-sea clamm ([13] Figure 1); and (d) Dredge with ‘hempen tangles’, as used on the HMS Porcupine in 1869 and 1870 ([20], p.257).

Counter evidence also brought up annelid worms and a most impressive As early as 1818, decades before Forbes’ adventures in the starfish (Figure 5), apparently from depths of 800 fathoms Ægean, evidence that might have discredited the azoic (approximately 1465 metres) and beyond [13]. In fact, Ross hypothesis began to accumulate. Captain John Ross RN overestimated his deepest soundings, the true depth being (1777–1856), sailing in the Isabella, made a series of no more than 600 fathoms (approximately 1095 metres), soundings off the northeast coast of Canada in the region although this was not recognized for more than 150 years of Baffin’s Bay when searching for the elusive northwest [14]. Yet, although these lesser depths would have been passage. He calculated depth using a sounding line low- sufficient to discredit Forbes’ ideas, Ross’ evidence never ered over the side of the ship on the end of which was got an airing because some of the other members from that attached a snapping device known as a ‘deep-sea clamm’ expedition became embroiled in controversy on their (Figure 4c). When the clamm hit the bottom, the amount of return to the UK: Ross reported a range of fictitious moun- line paid out revealed the depth and the jaws of the device tains blocking Lancaster Sound [15]; and, in addition, grabbed samples of mud from the seabed. Astonishingly, it several of Ross’ shipmates, including his nephew James www.sciencedirect.com Review Endeavour Vol.30 No.4 135

Figure 5. The starfish Gorgonocephalus arcticus Leach (1819). This is probably the very specimen brought up entangled in Ross’ sounding line in 1818 (see [14]). Scale is in cm. Reproduced courtesy of the Natural History Museum, London.

Clark Ross (1800–1862), believed their contributions had army after a career as a surgeon, joined Captain not been adequately acknowledged in Ross’ official account Sir Leopold McClintock (1819–1907) on the HMS of the voyage. Bulldog on an expedition to Iceland, Greenland and Subsequent to Forbes proposing the azoic hypothesis, Newfoundland. Midway between Greenland and Rockall, dredging investigations of the seabed at relatively shallow a sounding line was brought up from a depth of 1260 depths, 200–300 fathoms (approximately 365–550 metres), fathoms (approximately 2305 metres) with no less than provided further evidence that animal life was more abun- 13 starfishes attached to it. ‘This sounding far exceeds in dant there than Forbes had previously found in the Ægean. importance any previous sounding on record,’ Wallich James Clark Ross dredged up beautiful specimens of living exclaimed. ‘It proves the fallacy of several of the condi- coral and a variety of other marine invertebrates from tions which have heretofore been supposed to limit the depths of up to 400 fathoms (approximately 730 metres) bathymetrical distribution of animal life, and points to during his famous Antarctic expedition in the HMS Erebus the existence of a new series of creatures peopling the and HMS Terror from 1839–1843. ‘I have no doubt,’ he deeper abysses of the ocean’ [18].Butthescientific remarked, ‘that from however great a depth we may be community ignored Wallich’s findings, probably because enabled to bring up the mud and stones of the bed of the he was such an irascible character. This left him bitter ocean we shall find them teeming with animal life’ [16].A and incensed at what he saw as unjust treatment at the few years later, Michael Sars (1805–1869), Professor of hands of the scientific establishment, represented by the Zoology at Christiania (now Oslo) University, used dredges Royal Society and, in particular, his arch-enemies to study the animal life on the sea floor off the Norwegian and rivals Charles Wyville-Thomson (1830–1882) and Coast. Between 1850–1868 he and his son, George Ossian William Carpenter (1813–1885) [19]. Sars, catalogued hundreds of different animal species In autumn 1860, a cable across the Mediterranean when dredging between 200–300 fathoms [17]. Yet, stran- between Sardinia and Bona broke at a depth of 1200 gely, despite the contrast between this abundance of life fathoms (approximately 2195 m). The Mediterranean and Forbes’ results from similar depths, most naturalists Telegraphy Company gave the job of retrieving the did not consider the new observations enough to discredit cable to Henry Fleeming Jenkin (1833–1885), Professor the azoic hypothesis. Only evidence of life from much of Engineering at Edinburgh University. To Jenkin’s great greater depths could do that. surprise, a variety of animal life was found attached to the In 1860, George Charles Wallich (1815–1899), a cable when it was brought up, including solitary corals, naturalist who had been invalided out of the Indian oysters and clams. www.sciencedirect.com 136 Review Endeavour Vol.30 No.4

ladenness of observation’ [23]. Prejudiced by the notion that life would be impossible in the extreme environment of the deep sea, naturalists embraced Forbes’ hypothesis and simply disregarded evidence to the contrary. Matters were not helped by the fact that much of the counter evidence was not collected in purpose-built dredges, with naturalists reluctant to accept evidence that came from any other source [19]. But how, for example, could starfishes collected attached to sounding lines have come from anywhere but the bottom? The mysteries of how animals are able to survive on the deep sea floor took many years to resolve. It was not until after the great Challenger expedition of 1872–1876, for example, that the mode of nutrition of deep-sea animals became understood, namely that they rely on the rain of debris of animals and plants falling to the bottom from the Figure 6. An aggregation of sponges: Pheronema carpenteri, approximately 15–20 cm in diameter, photographed at a depth of 1250 metres in the Porcupine surface [24]. Nevertheless, the likes of Wallich and Wyville- Seabight (518 400N, 138 000W) in August 1984. In the foreground is a starfish Thomson were prepared to question the azoic theory with- (Plutonaster bifrons). The sampling location is close to the routes taken during the out any such resolution. They were willing to contemplate first and second cruises of HMS Porcupine in 1869, thus showing the sorts of life- forms that Charles Wyville-Thomson and William Carpenter are likely to have the seemingly impossible, the existence of life in the deep encountered in their dredge hauls. Reproduced courtesy of the DEEPSEAS Group, sea. The bulk of the scientific community was not. National Oceanography Centre, Southampton, UK. The benefits of false hypotheses The Scottish naturalist Wyville-Thomson had noted The controversy surrounding the azoic hypothesis was not these developments, and determined to settle the issue so much due to problems with the theory itself, but rather once and for all. He contacted his friend Carpenter who was the reluctance of many contemporary scientists to accept vice president of the Royal Society, urging him to obtain a contradictory evidence. By proposing it, Forbes paved the ship from the Admiralty to undertake dredging work. The way for later discoveries by stimulating the debate among council of the Royal Society gave their consent, initially leading naturalists of the day about how the marine envir- providing them with the HMS Lightning: ‘A cranky little onment influences the distributions of the plants and vessel...perhaps the very oldest paddle-steamer in her animals that live in it. For theories, including erroneous Majesty’s Navy’ [20] and subsequently the somewhat stur- ones, are absolutely necessary for the advancement of dier HMS Porcupine, also a paddle steamer. The two science. As Thomas Henry Huxley so admirably remarked naturalists dredged the deep waters off the British Isles as early as 1853: ‘... there are periods in the history of and Spain, and in the Mediterranean, from 1868–1870. every science when a false hypothesis is not only better The dredges used by Wyville-Thomson and Carpenter were than none at all, but it is a necessary forerunner of, and quite similar to those employed by Forbes, but with several preparation for, the true one’ [25]. We now know more significant improvements. The frames were up to 4 feet about the deep sea than Forbes could ever have dreamt of. 6 inches (1.35 metres) wide and carried much more effi- Nevertheless, the pitfalls of following received wisdom are, cient dredge bags consisting of a coarse outer mesh that as in Forbes’ day, just the same. Indeed, in an era where was lined by much finer netting in an attempt to collect the science is used as a means of confronting issues such as smaller organisms. Despite their best efforts, however, the overpopulation, pollution and climate change, the conse- dredge worked rather badly in deep water so that ‘while quences could be much more serious. few objects of interest were brought up within the dredge, many echinoderms, corals, and sponges came to the surface References sticking to the outside of the dredge-bag...’ [21].Ina 1 Forbes, E. (1844) On the light thrown on geology by submarine renewed effort to catch the smaller creatures, the Captain researches; being the substance of a communication made to the of the Porcupine, Edward Killwick Calver (1813–1892), Royal Institution of Great Britain, Friday Evening, the 23d suggested attaching teased out lengths of hemp rope to February 1844. Edinburgh New Philosophical Journal 36, pp. 319– 327 (op. cit. p. 319) the dredges (Figure 4d),a technique that was so successful 2 Forbes, E. and Godwin-Austen, R. (1859) The Natural History of the that ‘hempen tangles’ became a standard feature for many European Seas, John Van Voorst (London, UK) years. This approach dredged up hundreds of sea creatures 3 Forbes, E. (1844) Report on the Mollusca and Radiata of the Aegean previously unknown to science (Figure 6), showing ‘beyond Sea, and on their distribution, considered as bearing on geology. Report of the British Association for the Advancement of Science for 1843 question that animal life is varied and abundant, repre- , pp. 129–193 (op. cit. p. 167) sented by all the invertebrate groups, at depths in the 4 Von Humboldt, A. (1850) Views of Nature: Or Contemplations on the ocean down to 650 fathoms at least’ [22]. The azoic hypoth- Sublime Phenomena of Creation (Otte´, E.C. and Bohn, H.G., trans.), esis was at last falsified. H.G. Bohn (London, UK), p. 217 and p. 231 5 Forbes, E. (1840) Report on the distribution of Pulmoniferous Mollusca in the British Isles. Report of the British Association for the Believing the impossible Advancement of Science for 1839, pp. 127–147 The endurance of the azoic hypothesis in the face of 6 Forbes, E. (1840) On the associations of Mollusca on the British coasts, counter evidence is a good example of the so-called ‘theory considered with reference to Pleistocene geology, In The Edinburgh www.sciencedirect.com Review Endeavour Vol.30 No.4 137

Academic Annual for 1840 Consisting of Contributions in Literature 15 Dodge, E.S. (1973) The Polar Rosses. John and James Clark Ross and and Science, pp. 175–183, Adam and Charles Black (Edinburgh, UK) Their Explorations, Faber and Faber (London, UK) 7 De La Beche, H.T. (1834) Researches in Theoretical Geology, Charles 16 Ross, J.C. (1847) A Voyage of Discovery and Research in the Southern and Knight (London, UK), p. 262 Antarctic Regions, DuringtheYears1839–43 (Vol. 1), John Murray, p. 202 8 Agassiz, L. and Gould, A.A. (1851) Outlines of Comparative Physiology, 17 Sars, G.O. (1872) Some Remarkable Forms of Animal Life from the H.G. Bohn, pp. 365–366 Great Deeps off the Norwegian Coast, Brøgger and Christie 9 Page, D. (1856) Advanced Text-book of Geology, William Blackwood (Christiania, Norway) (Edinburgh, UK), p. 20 18 Wallich, G.C. (1862) The North Atlantic Sea-Bed: Comprising a Diary of 10 Grassle, J.F. and Maciolek, N.J. (1992) Deep-sea species richness – the Voyage on Board H.M.S. Bulldog, in 1860; and Observations on the regional and local diversity estimates from quantitative bottom Presence of Animal Life, and the Formation and Nature of Organic samples. American Naturalist 139, pp. 313–341; Angel, M.V. (1996) Deposits, at Great Depths in the Ocean, John Van Voorst, p. 68 Ocean diversity. In Oceanography. An Illustrated Guide 19 Rice, A.L. et al. (1976) G. C. Wallich M. D. – megalomaniac or mis-used (Summerhayes, C.P. and Thorpe, S.A., eds), pp. 228–243, Manson oceanographic genius? Journal of the Society for the Bibliography of Publishing (London, UK) Natural History 7, pp. 423–450 11 Peres, J.M. (1982) Major benthic assemblages. In Marine Ecology (Vol. 20 Thomson, C.W. (1873) The Depths of the Sea, Macmillan (London, UK), 5, Part 1) (Kinne, O., ed.), pp. 373–522, John Wiley (Chichester, UK) p. 57 12 Forbes, E. (1844) On the dredge. In Anatomical Manipulation (Tulk, A. 21 Ibid., p. 255 and Henfrey, A., eds), pp. 405–406, John Van Voorst; See also Rehbock, 22 Ibid., p. 79 P.F. (1979) The early dredgers: ‘naturalizing’ in British Seas, 1830–1850. 23 Hanson, N.R. (1958) Patterns of Discovery: An Inquiry into the Journal of the History of Biology 12, pp. 293–368 Conceptual Foundations of Science, Cambridge University Press 13 Ross, J. (1819) A Voyage of Discovery, Made Under the Orders of the (New York, NY, USA) Admiralty, in his Majesty’s Ships Isabella and Alexander, for the 24 Moseley, H.N. (1880) Deep-sea dredging and life in the deep sea III. Purpose of Exploring Bafﬁn’s Bay, and Inquiring into the Probability Nature 21, pp. 591–593 of a North-West Passage, John Murray (London, UK), p. 178 25 Huxley, T.H. (1853) The cell-theory. The British and Foreign Medico- 14 Rice, A.L. (1875) The oceanography of John Ross’s Arctic Expedition of Chirurgical Review 12, pp. 285–314 (op. cit. p. 291) 1818; a re-appraisal. Journal of the Society for the Bibliography of 26 Forbes, E. and Hanley, S. (1853) A History of British Mollusca and Natural History 7, pp. 291–319 Their Shells (Vol. 1), John Van Voorst

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