Charles Darwin and Marine Biology Philip S

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Marine Ecology. ISSN 0173-9565

ORIGINAL ARTICLE Charles Darwin and marine biology Philip S. Rainbow

Department of Zoology, Natural History Museum, London, UK

Keywords Abstract Barnacle; Beagle; coral reefs; Darwin; Grant; Lyell; transmutation; unlformltarlanlsm. In a celebration of the 200th anniversary of his birth in 1809, this short essay explores the influence of marine biology on Charles Darwin,vice and versa. Correspondence Darwin made his first forays into the world of marine biology as a medical stu Philip S. Rainbow, D epartm ent of Zoology, dent in Edinburgh from 1825 to 1827. He came under the influence there of Natural History M useum , London SW7 5BD, the Lamarckian Robert Grant, and developed an understanding of the simple UK. organisation of the early developmental stages of marine invertebrates. Yet Dar E-mail: [email protected] win balked at Lamarckian transmutation. The voyage ofBeagle the led to Dar

Accepted: 17 November 2010 win’s perceptive theory of the origin of coral reefs, an origin still mainly accepted today. This theory was steeped in the uniformitarianism of the geolo doi : 1 0 .1 1 1 1/j. 1439-0485.2010.00421 .x gist Lyell, depending on the slow, gradual growth of billions of coral polyps keeping pace with slow sinking of land to produce an atoll. Prom 1846 to 1854 Darwin revolutionised the understanding of barnacles, producing monographs still relevant today. His barnacle studies gave him the credibility to pronounce on the origin of species; he found great variation in morphology, and a series of related species with remarkable reproductive adaptation culminating in the presence of dwarf males. Barnacles showed him an evolutionary narrative laid out before him, and contributed greatly to his qualification and confidence to write with authority on the origin of species.

Born in Shrewsbury on 12 Pebruary 1809, Charles Robertto carry out his external hospital study in Edinburgh Darwin could hardly have been said to have had the sea (Desmond & Moore 1991). Charles, however, became in his blood, but as a child he was an inveterate collectordisillusioned with his medical studies as he experienced of objects such as shells and birds eggs and developed anthe drudgery of his lectures and poor quality of his lec early interest in natural history. By his teens, hunting hadturers, and then the distress of clinical studies with become Charles’ passion, and in 1825 his exasperated associated blood, gore and suffering. Initial diligence father, the well respected local doctor Robert Darwin, gave way to the sampling of student life. On his own came to utter the oft-quoted prediction ‘You care forin his second year, Darwin found a diversion in marine nothing but shooting, dogs, and rat-catching, and youbiology. will be a disgrace to yourself and all your family’ (Des In November 1826, Charles Darwin joined the Plinian mond & Moore 1991). Strong action was needed to halt Society, an undergraduate group discussing natural his Charles’ aimless way of life and so, following his father tory and antiquarian researches, and occasionally going and elder brother Erasmus, medicine was chosen as the on collecting expeditions together. This proved a safety required remedy. valve from medicine, and, over the academic year, Darwin In October 1825, Charles Darwin, aged 16, found accompanied his Plinian friends on zoological walks on himself enrolled in the University of Edinburgh to studythe shores of the Firth of Forth, and ventured out on medicine, accompanied for the first year by Erasmus trawlers fishing at sea. He became familiar with a host of who, although a medical student at Cambridge, was able marine invertebrates previously strange to him, including

130 Marine Ecology32 (Suppl. 1 ) (2011 ) 130-134 © 2011 Blackwell Verlag GmbH Rainbow Charles Darwin and marine biology sponges, soft corals Alcyonium ( digitatum), sea slugs founded as London University in 1826, admitting stu (Tritonia hombergi), polychaetes (the sea mouseAphrodite dents regardless of religion and gender, a secular alterna aculeata) and bryozoans(Flustra foliacea). tive to Oxford and Cambridge. London University was At this time Darwin came under the influence and clearly a more suitable venue for Grant’s seditious views mentorship of a man who would be key to the laterthan God-fearing Edinburgh. development of Darwin’s ideas on evolution. RobertThe 2 years at Edinburgh convinced Charles Darwin Edward Grant was a marine invertebrate zoologist and athat medicine was not for him, and in 1827 he left Edin fellow Plinian, living in Edinburgh on a decreasing legacyburgh a disappointed man: he did not like medicine, nor from his late father (Desmond & Moore 1991). Grant the men who pursued it; he had found no qualities in became Darwin’s unofficial tutor on marine invertebrates,professors to generate long-lasting respect (even Grant teaching him to make observations and to dissect specihad disappointed him); and he was not ready to be a mens. Through Grant, Darwin developed an understandtransmutationist or be labelled a radical like his grandfa ing of animal development and the simple organisation ofther, Erasmus Darwin (Browne 1995). Medicine was not the early life-history stages of particular invertebrates. for him, but he now had little choice - the family fell Grant was an expert on sponges recognised by his peers,back on the typical safety net for second sons, the Church as exemplified by the naming of the newly erected spongeof England. So from 1827 to 1831, Charles Darwin found genus Grantia in his honour by John Fleming in 1828; himself at Christ’s College at the University of Cambridge the common local spongeSpongia compressa, the purse on the first stage of his journey to Holy Orders. There sponge, becameGrantia compressa. It was Grant who was still room for natural history, now under the influ coined the name ‘Porifera’ for the sponges. ence of John Henslow, the Professor of Botany, and for After working with Grant, Darwin (aged 18) gave a talk geology under the influence of Adam Sedgwick, Professor to the Plinian Society on 17 March 1827, showing that of Geology. the larvae of the bryozoanFlustra foliacea use cilia for However, there was no more immediate access to mar locomotion and that the black markings (sea pepperine biology for Darwin until the portentous year of 1831. corns) on the shells of oysters are the eggs of the marine Then Henslow introduced Darwin to Robert FitzRoy, leech Pontobdella muricata. A triumph for a budding captain of HMSBeagle, who subsequently invited to Dar marine biologist but, according to Darwin’s daughterwin to join a voyage around the world as a self-financing Elenrietta, Darwin had been scooped 3 days earlier bygentleman naturalist. The voyage lasted from December Grant in a talk to the more formal (graduate) student 1831 to October 1836. Darwin regularly sent back natural society, the Wernerian Natural History Society - an introhistory and geology collections which gained him a scien duction for Darwin to ‘the jealousy of scientific men’tific reputation in his absence, and the voyage changed (Browne 1995). his life for ever. Grant, however, represented something more - sedition In January 1835, Darwin collected many specimens of a personified (Desmond & Moore 1991). Grant was a fran large intertidal gastropod mollusc on a shore in the Cho cophile who had studied anatomy and embryology innos archipelago, Chile, a collection not considered even France with Geoffroy Saint-Hilaire. Correspondingly,worthy of reference in several editions of Darwin’s journal Grant was a Lamarckian, more openly so later, for hisof the voyage (Darwin 1839). The mollusc concerned was views were still forming at this time. Lamarck (1809) used a muricid gastropod,Concholepas concholepas (as Conc the term ‘transmutation’ for his theory that described the holepas peruviana), the shells of which were riddled with altering of one species into another. Lamarck did notcavities containing minute animals, no bigger than pin propose common ancestry but considered that complexheads. These were to be later identified as boring barna forms transmutated from simple forms of life created cles, and these were also destined to affect Darwin’s continuously by spontaneous generation. As a Lamarckfuture life enormously. ian, Grant arranged life into chains, considering that the Before leaving on theBeagle, Darwin had been greatly origins of animals and plants lay in the simplest forms;influenced by Sir Charles Lyell, a leading geologist of the and that the natural ordering, simple to complex, oftime, who had published the first edition of hisPrinciples sponges represented the historical order of appearance ofo f Geology in three volumes (1830, 1832, 1833). Lyell was sponges. Thus Grant directly exposed Darwin to evolua believer in uniformitarianism, a philosophy claiming tionary theory, with the associated concepts of structuralthat geological and biological forces have always been homology and unity of plan with similar organs presentworking in the same way and at the same intensity over in different animals. Grant went on in 1827 to becomeages. This view of uniformitarianism was in conflict with Professor of Comparative Anatomy for life (1874) at Unithe then-prevailing theory of catastrophism, which con versity College, London. University College had beensidered that the earth experienced major changes only as

Marine Ecology32 (Suppl. 1) (2011) 130-134 © 2011 Blackwell Verlag GmbH 131 Charles Darwin and marine biology Rainbow a result of large catastrophic events. A key considerationunstudied for 6 years. Robert Grant, now in London, was whether the earth was old enough to experience volunteered to help, particularly with ‘lower animals’, but large-scale changes in any other way, but Lyell thought it was turned down by Darwin who had become a compe necessary to create a vast time scale for Earth’s history to tent (and competing) coral expert, given his interest in vouch for fossil remains of extinct species, excluding sudcoral reef formation. In fact, ironically, the corals were den geological catastrophes. Charles Darwin shared a sup not monographed. Nor did Darwin and Grant have any port for uniformitarianism. thing more to do with each other (Desmond & Moore The formation of coral reefs was a lively topic for1991). debate at the time, and in the second volume (1832) of By October 1846, Darwin thought that he had Principles of Geology, Lyell had explained the origin of described all his Beagle specimens, and turned his atten coral atolls as coral reefs growing up from the crater rims tion to a single remaining barnacle species, the boring of underwater volcanoes. Volume 2 was sent out to Darbarnacles in the gastropod shells collected in Southern win by his mentor and faithful correspondent ProfessorChile in January 1835. The barnacle was clearly ‘quite Henslow, to reach him in Montevideo in November 1832.new and curious’ - he called it that ‘ill-formed little Darwin’s observations on Beagle, the however, had con monster’ - certainly aberrant and the world’s smallest vinced him otherwise. Darwin drafted an alternative the barnacle. Darwin did not know how to classify it, refer ory for the origin of coral reefs that essentially stands ring to it as ‘Mr Arthrobalanus’. A new microscope was today. Lyell accepted it immediately. necessary, but so was a comparison with ‘more normal’ An essential point in coral reef formation is that reef-barnacles. So Darwin started borrowing the necessary building corals only grow in well-lit shallow waters, supspecimens, and the project grew and grew as he soon plying light to their symbiotic zooxanthellae, and couldappreciated the state of chaos of the knowledge of bar not grow up from deeper, dark depths. In Darwin’snacles. explanation, corals form fringing reefs just below low tide Why did Darwin embark on a project that was to along tropical coastlines, and eventually the coral reef willoccupy the next 8 years? Darwin had been formulating grow out to become a barrier reef. Darwin had seen the his ideas on variation and natural selection, resulting effects of earthquakes in Chile and knew that land couldeventually inThe Origin of Species (Darwin 1859), and he rise or fall. If the coast is sinking slowly, then the growth agreed with the view of his botanist friend Joseph Hooker of coral could keep pace. If the land sinks beneath thethat no-one had a right to examine the question of spe waves - an atoll is formed. His first hand observations incies who had not described many. So Darwin would earn Keeling Atoll helped convince him of his views. Darwin that right. Barnacles would establish his credentials, and a could see that, although coral reefs were huge geological thorough examination of all barnacle varieties could put structures on a world scale, they were created by the slow, him in a commanding position when discussing natural gradual growth of billions of tiny creatures over vastselection. In fact, as he proceeded, he began to uncover reaches of time. This was an example of Lyell’s ‘uniformi- the most extraordinary proofs of his notebook specula tarian’ principle in action, the cumulation of smalltions (Desmond & Moore 1991). changes over a long period, to be repeated in Darwin’s So Darwin studied barnacles (‘my beloved barnacles’) studies on earthworms years later. Later observations ofin his study at Down House in Kent from 1846 to 1854. cores of coral limestone to great depths (culminating inHe would go on to deliver a thorough reappraisal of both studies in Bikini Atoll in the 1950s) provided supportingliving and fossil barnacles, monographs that still com evidence for land sinking at an appropriate rate - coralmand the field today (Darwin 1851a,b, 1854a,b). could simply not have grown up from these depths in the So what are barnacles? Zoological folklore has it that absence of light. Louis Agassiz described a barnacle as ‘nothing more than Darwin publishedCoral Reefs in 1842 (Darwin 1842). a little shrimp-like animal, standing on its head in a lime It showed the tight logical structure to become evident stone house and kicking food into its mouth’. again in the Origin o f Species to be published in 1859. Barnacles are indeed crustaceans, crustaceans that lack On his return from theBeagle in 1836, Darwin sought an abdomen and with a head enormously developed as a to place his collections with experts to identify andstalk or, as in the sessile barnacles, that limestone house describe them - not altogether an easy task. The mam of overcalcified cuticle. Darwin (1851a) drew a diagram mals were placed with Richard Owen - later to found the (Fig. 1) of the relationship between the anatomy of a Natural History Museum in South Kensington and vehestalked barnacle(Lepas) and a decapod crustaceanLuci ( mently oppose Darwin’s views on evolution. He avoidedfer) discussing similarities or differences in terms of Robert Brown (Keeper of Botany) at the British Museumthe homologies of the body parts, a conceptual way of who had been sitting on a collection of Galapagos plants,thinking with which he was clearly happy. Typically we

species of the stalked barnacle genusScalpellum showed a gradient from complete hermaphroditism to hermaphro dites with small complemental ‘dwarf males with the lar ger ‘hermaphrodite’ acting as a female (e.g. Scalpellum scalpellum). Was this an example of what transmutation might look like? Darwin (1851a) also discovered that the stalked barnacleIbla cumingii also has large females with small complemental males. The dwarf male shows great reduction in form as it becomes specialised for reproduc tion only. Transmutation? The study of barnacles indeed provided Charles Dar win with many of the facts that he needed to support Fig. 1.The diagram drawn by Darwin (1851a) of the relationship his ideas on evolution - both through comparative between the anatomy of a stalked barnacle(Lepas) and a planktonic anatomy and through the study of fossils. What Darwin decapod crustacean(Lucifer) to show the homologies of the external found in his barnacles (Stott 2003) was variation parts (m, mouth). beyond his wildest imaginings, and reproductive modes that took his breath away, with the development of Table 1.Barnacles and their relatives are members of the class Max complemental males living parasitically on the female, illopoda, together with the likes of tantulocarids, branchiurans, pent-no more than reproductive sacs of sperm, with no astomids, mystacocarids and copepods (Martin & Davis 2001). heads, stomachs or digestive systems. Barnacles had Subclass Thecostraca adapted to their environments and an evolutionary nar Infraclass Facetotecta rative branched out before his eyes (Stott 2003). Dar Infraclass Ascothoracida win’s barnacles showed him what transmutation could Infraclass Cirripedia look like. Bit by bit, each apparently trivial adaptation Superorder Acrothoracica in living structure accumulated, one after another, until Superorder Rhicocephala animals became so distinct from their parents and cous Superorder Thoracica Order Pedunculata ins that they could be called a different species (Browne O rder Sessilia 1995). While Darwin made fundamental contributions to the study of coral reefs and barnacles, clearly in return, mar recognize three groups of cirripede barnacles today (Acroine biology contributed much to Darwin’s development thoracica, Rhizocephala, Thoracica), closely related to two of evolutionary thinking. The interaction of marine biol other taxa, the Ascothoracida and Facetotecta (Table 1, ogy and the intellect of Darwin was key to the develop after Martin & Davis 2001). ment of his supreme contribution to biology - the So what was that ‘ill-formed little monster’ ‘Mr Arthro- mechanism of natural selection acting on natural varia balanus’ found boring into the shellsConcholepas of conction to explain the origin of species and the evolution of holepas, collected in southern Chile in January 1835? Inorganisms. 1849, Hancock described a boring barnacle from the colu mella of whelk shells, Buccinum undatum, occupied by Acknowledgements the hermit crab Pagurus bernhardus - Alcippe (now Try petesa) lampas (Hancock 1849). ‘Mr Arthrobalanus’ This essay results from an invited lecture given at the turned out to be a close relative. Darwin (1854a)44th European Marine Biology Symposium in Liverpool described it as Cryptophialus minutus, and placed both in 2009 in acknowledgement of the 200th anniversary of species in a new order, the Abdominalia. The order was the birth of Charles Darwin. The lecture attempted to renamed the Acrothoracica by Gruvel (1905) because bring Darwin’s specific contributions in marine biology these burrowing barnacles lack an abdomen, the taxonto a wide audience of marine biologists, perhaps under featuring as a superorder in Table 1. Acrothoracicans livestandably only aware of Darwin’s hugely significant con in burrows in calcareous rocks and shells, and have tribution a of natural selection as a mechanism body and cirri not dissimilar to that of the more comunderpinning evolution. I am indebted to Professor Chris mon thoracicans. Frid for the invitation. It will come as no surprise to Darwin discovered reproductive modes in some barnareaders that this is not a paper of original scholarship, cles that astounded him. Most barnacles are hermaphro but simply a secondary compilation from excellent works dite, but not all. Darwin (1851a) discovered that different of real biographical scholarship published on Charles

Darwin. I have leant heavily on the outstanding biograDarwin C.R. (1854a)A Monograph on the Subclass Cirripedia. phies by Janet Browne (1995, 2002) and by Adrian Des Vol.2 The Balanidae, The Verrucidae, Ray etc.. Society, Lon mond and James Moore (1991), to whom interested don: 684 pp. readers are referred. Rebecca Stott (2003) has produced a Darwin C.R. (1854b)A Monograph on the Fossil Balanidae and fascinating account of the barnacle years which domi Verrucidae of Great Britain. Palaeontographical Society, Lon nated the life of Darwin and his family at Down House don: 44 pp. from 1846 to 1854. Darwin C.R. (1859) On the Origin of Species by Means of Natu ral Selection, or the Preservation of Favoured Races in the Struggle for Life. John Murray, London: 502 pp. References Desmond A.J., Moore J.R. (1991)Darwin. Michael Joseph, London: 808 pp. Browne J. ( 1995)Charles Darwin: Voyaging. Jonathan Cape, Gruvel A. ( 1905) Monographie des Cirrhipèdes ou Thécosracés. London: 605 pp. Masson et Cie, Paris: 472 pp. Browne J. (2002) Charles Darwin: The Power of Place. Jonathan Hancock A. (1849) Notice of the occurrence on the British Cape, London: 591 pp. coast of a burrowing barnacle belonging to a new order of Darwin C.R.. (1839)Journal of Researches into the Geology and the class Cirripedia. Annals and Magazine of Natural History, Natural Histoiy of the Various Countries Visited by H.M.S. 4, 305-314. Beagle etc.. Henry Colburn: London: 629 pp. Lamarck J.-B. (1809) Philosophie Zoologique, ou Exposition des Darwin C.R. (1842) The Structure and Distribution of Coral Considérations Relatives à l’Histoire Naturelle des Animaux. Reefs. Part 1 of The Geology of the Voyage of the Beagle etc. Dentu et l’Auteur, Paris: 422 pp. Smith Elder and Co., London: 214 pp. Martin J.W., Davis G.E. (2001) An updated classification of Darwin C.R. (1851a) A Monograph on the Subclass Cirripedia. the recent Crustacea. Natural History Museum of Los Angeles Vol.l The Lepadidae. Ray Society, London: 400 pp. County Contributions in Science. 39, 1-124. Darwin C.R. (1851b) A Monograph on the Fossil Lepadidae, or, Stott R. (2003) Darwin and the Barnacle. Faber and Faber, Pedunculated Cirripedes of Great Britain. Palaeontographical London: 309 pp. Society, London: 88 pp.