The legacy of Professor John Stanley Gardiner FRS to reef science

Initiation into the study of reefs

John Stanley Gardiner's career as a zoologist began at Marlborough School, where his critical thinking was shaped by the science masters and where he was a great supporter of the school's Natural History Society.1 In 1891 he was admitted to Gonville and Caius College, Cambridge, where he studied zoology as his main subject. As a student he was much influenced by Alfred Newton FRS and Adam Sedgwick FRS in the Zoology Department, and after graduating with a first class in both Tripos examinations he took the university's table at the Zoological Station in Naples. As a keen natural historian equipped with a classical zoological training and a fascination with marine biology through his experiences in Naples, the young Gardiner, aged 26 years, would no doubt have been very excited at the prospect of joining the Royal Society Expedition to Funafuti in the Ellice Islands in 1896. Gardiner's first encounter with reefs took place on this expedition where the primary aim was to examine the structure of an atoll by deep boring and thereby test the ‘subsidence theory’ of reef origin proposed by Charles Darwin. Major funding for the expedition came from the Royal Society, which set up a Coral Reef Committee to oversee its organization. The Committee laid down guidance instructions outlining the role that Gardiner should play, namely:

Mr. S. Gardiner will accompany the Expedition as a volunteer with the sanction of the Committee paying his own expenses and selecting his own subjects for study, with the general understanding that he will lend such aid as may be in his power to Professor Sollas in effecting the main object of the Expedition, and will co-operate with him in making the study of the reef, its fauna, flora and vicinity in general as complete as possible.2

With this remit Gardiner set sail first for Sydney, Fiji and then Funafuti. While the reef-boring programme hit technical problems, Gardiner and Hedley (conchologist to the Australian Museum) made detailed investigations of the terrestrial and marine fauna and flora of Funafuti. Gardiner also took the opportunity to describe the atoll of Funafuti, the reefs of nearby Rotuma and the raised and modern reefs of Fiji. While assisting with identification of material from the borings, he also identified living corals on surrounding reefs and considered their growth and nutrition—factors that he felt might provide a better understanding of reef formation.

In terms of coral taxonomy and attention to coral growth and feeding, Gardiner was a pioneer. Certainly, eminent coral taxonomists preceded him but his collections in the Ellice Islands contributed many type specimens to existing lists. He was also one of the first to take meticulous notes on the colour, form and location of colonies collected by dredging, diving or walking on the reef flats at low tide. Gardiner quickly became aware of the great intraspecific variation in coral skeletal morphology, around which species identification is based. Indeed, in his report on perforate corals collected in the South Pacific,3 he commented: ‘The great variety shown between the upper and under sides of the species I have named Acropora tabulata seems to show that there is little value in the naming of the species of this genus from the skeleton alone’. Intraspecific variation in skeletal characters was to confound the identification of corals until the mid 1970s. In an attempt to find alternative taxonomic methods, Gardiner preserved more than 100 coral specimens from the Pacific and shipped them back to Cambridge for later investigation of the soft tissues.

His preliminary experiments on coral nutrition are rarely cited in the literature, yet they form a foundation for the later ‘classic’ experiments on coral nutrition performed 30 years later by C. M. Yonge (FRS 1946) during the Great Barrier Reef Expedition in 1928–29. While in Funafuti and Rotuma, Gardiner collected plankton from reef passages to discover ‘what animals were driven over the reef to form the food of corals’.4 He found few organisms during the day but abundant plankton at night, and noted that many corals expanded only at night-time. He also examined the guts of corals, finding pieces of green weed and a few small oval unicellular algae. He commented that animal remains were rare and seldom identifiable. Feeding experiments were performed in which he supplied large polyped mussid corals with freshly caught plankton before examining their guts. He identified numerous planktonic organisms and so convincingly demonstrated that corals were carnivores. He also maintained corals in glass containers covered with fine bolting silk for periods of up to two months,5 noting that, despite being deprived of plankton, the corals remained healthy with their tissues crammed with algae (on the Great Barrier Reef in 1928–29 Yonge also conducted an exclusion experiment, although in this case he excluded light from fed corals to see whether they could live without their symbiotic algae over a period of several months). Even at this early stage of his studies Gardiner was beginning to question whether heterotrophy was the sole method of feeding in corals and whether the unicellular algae housed in the coral tissue might contribute in some way to coral nutrition. Gardiner also performed experiments in which he inverted glass containers over corals and collected the gases evolved—such gases causing matches to glow—and another set of experiments in which he used metallic sodium and water to produce hydrogen before adding the evolved gas, effecting a ‘distinct explosion’!4 Although he could not confirm that the evolved gas was oxygen, nor whether it was due to the ‘parasitic’ algae present in the coral, he clearly recognized the potential influences of the algae on coral growth at an early stage in his work. In 1932 Yonge and his colleagues noted6 that Gardiner was the first scientist to point out that during daytime the symbiotic algae produce more oxygen than the corals used in respiration, and confirmed this finding in their own work on the Great Barrier Reef Expedition in 1928–29. However, the contribution of unicellular algae to the nutrition and growth of the coral host was a very controversial issue and it continued to be so for at least another 40 years.

In his attempt to evaluate the conditions that affect coral growth, Gardiner conducted some of the first transplantation experiments, removing several different species from an area rich in corals to more depauperate sites and transferring corals to areas outside the zone of their occurrence while maintaining other transplants within their original zones. Although Dana records similar attempts at transplantation by early workers,7 Gardiner gives a more precise account of the outcome of his own manipulations than any before him. Branchlets broken from branching corals and small pieces of massive corals all died after three months, but branching forms ‘removed by the root’, and large blocks of massive species, if confined to their original reef zone, all survived. It was not until 1980, some 82 years later, that Highsmith confirmed a general relationship between fragment size and survivorship in corals, with small fragments generally surviving poorly in comparison with large fragments with high survivorship.8 Such results, although not universal, have influenced coral transplantation practices used to restore damaged reefs in the twentieth century.

Gardiner4 also wounded corals to see ‘how the wounds would heal and be grown over’. He noted that over a three-month period wounded areas failed to heal, leading to scars, which he observed provided an easy entrance to boring animals. Almost a century later, artificial wounding and subsequent coral regeneration became an active area of interest, with subsequent workers showing that the ability of corals to repair damage was generally limited; the lesion perimeter is critical in determining the amount of area that ultimately regenerates.9

Measurements of the rate of growth were important in understanding reef formation, and Gardiner was again among the first to collect such data, commenting in 1931 that ‘the rate of growth of corals has fascinated every field naturalist recently working on coral reefs’.10 In Fiji, Gardiner collected corals on an anchor chain that had been in place for 1030 days in Levuka harbour, Fiji.4 Five colonies were collected, all branching species belonging to either the genus Stylophora or the genus Pocillopora. For these colonies he obtained measurements of dry mass, density, volume and thickness of the corallum, noting that the density of the samples seemed to vary inversely with the rate of growth. Despite the small sample size, Gardiner's measurements compare well with those obtained for other branching corals by subsequent reef workers in the period 1910–59. Extrapolating from such figures in later work in the Maldives, Gardiner11 was to postulate that over a 1000-year period a reef might grow upwards at a maximum rate of 2.6 cm per year. This figure, he highlighted, did not account for bioerosion or for the destructive action of waves and currents—rather, it was a reflection of how little time was necessary for the build-up of coral limestone.

As well as considering the rate of coral growth, Gardiner also recorded the depth of active coral growth in Fiji and Rotuma by means of dredging. He concluded that corals could grow to a maximum depth of 70 m in clear waters,4 although he acknowledged that the most prolific growth occurred at shallower depths of up to 25 m.10 From these and later observations throughout the Indian Ocean, Gardiner concluded that the depth and luxuriance of coral growth were dependent on light penetration. Most importantly, Gardiner believed that such a dependence demonstrated a key role for the symbiotic algae in both nutrition and growth of reef corals. By 1901 he amended his earlier statement on ‘parasitic algae’ to one that focused on ‘reef corals feeding mainly by means of their commensal algae’.12 These early observations and their implications were to provide a research interest that persisted throughout the rest of his working life and culminated in the first detailed experimentation on coral nutrition during the Great Barrier Reef Expedition of 1928–29.

The expeditionary period

There is no doubt that Gardiner is best known for his expeditions into the Indian Ocean during 1899–1900, 1905 and 1908, undertaken because ‘of no area of our great oceans do we at the present day know less than the Indian ocean within the tropics’.13 He also commented:

We felt that the day of vast expeditions, ranging through two or three oceans, was passed. Knowing some of the problems to be solved, we decided to attack them in a restricted area, as free as possible from complications brought in by wide ranges and variations in temperature, currents, winds and indeed all physical conditions.

The first expedition, funded by the Royal Society and the British Association, included Minikoi atoll, the most southern reef of the Laccadive Islands, and many of the Maldivian atolls. The second, known as the Percy Sladen Trust Expedition, covered the Chagos Archipelago, Seychelles, Amirantes, Coetivy, Cargados Carajos, Farquhar, Providence, St Pierre and Mauritius. Through the Royal Society the Admiralty made possible this second ambitious expedition by placing the surveying vessel HMS Sealark and its crew at Gardiner's disposal for six months of the summer of 1905 (figure 1). The third visit to the Indian Ocean, for four months in 1908, involved Gardiner's working on extending the taxonomic collections and studying the geology of Mahé and Silhouette in the Seychelles. A major aim of Gardiner's expeditions was to seek a better understanding of the distribution of marine animals and plants in the Indian Ocean: their origins, evolution and modes of dispersal.14 Such a remit included studies of the formation and growth of coral reefs that Gardiner believed might provide evidence of earlier landforms. Reports of the first expedition to Minikoi and the Maldives were published in two volumes in which Gardiner gave brief reef descriptions together with notes on their possible formation.11 Most of the chapters in these volumes were devoted to illustrated taxonomic descriptions of marine and terrestrial vertebrate and invertebrate groups collected by Gardiner and his assistants, Borradaile and Forster-Cooper, aided by local helpers. A total of 57 chapters were written by taxonomic specialists, with Gardiner reporting on the stony corals. The collection of corals contained more than 1000 dried specimens together with a large number of corals preserved for subsequent histological examination. Rosen considered that the Maldives expedition provided ‘an excellent coral collection’.15 Although a considerable amount of material was worked up by Gardiner, no complete list of corals was ever published. However, these studies yielded valuable information on the biogeographical distribution of corals in the Indian Ocean. Also included in the report of the Expedition11 was a short account of coral pigments by MacMunn, who had been sent coral specimens by Gardiner. MacMunn extracted the pigments in solvents and measured their absorbance at different wavelengths before identifying a chlorophylloid pigment that he attributed either to the digestive products of the coral or to the symbiotic algae. Such observations no doubt stimulated Gardiner's continued interest in the role of symbiotic algae in coral growth and nutrition. Indeed, during the Maldives expedition he followed up earlier observations of coral feeding and concluded:

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Figure 1

Officers and naturalists on HMS Sealark: Stanley Gardiner is second from the right on the front row. (Reproduced with the permission of the Linnean Society, London.)

These fully serve to confirm my previous work on the subject, but most reef corals evidently ingested a certain amount of organic food, although the vast majority undoubtedly obtained their nutriment principally through the agency of their commensal algae.

Gardiner also consolidated his earlier measurements of reef growth10 with collections and measurements of weight, volume, density, areal cover, and height of corals that had grown in a boat channel over a three-year period. Recognizing the role of boring organisms in modifying reef accretion, he made extensive collections of boring sponges, molluscs, sipunculids, polychaetes, cirripedes and algae that infested coral skeletons for later taxonomic identification.

Accounts of the second expedition to the Chagos, Seychelles and other islands in the western Indian Ocean followed a similar format to the earlier Maldives expedition, with detailed taxonomic accounts by specialists of marine and terrestrial organisms as well as descriptions of the structure and formation of islands and their reefs. The expedition results were published in the Transactions of the Linnean Society; Gardiner once more provided taxonomic coverage of the stony corals.14 In all, 142 reports were written by more than 100 authors. Although Gardiner's expeditions covered extensive areas of the Indian Ocean and provided much detailed information on the distribution of marine and terrestrial groups, inevitably time spent on the collections must have left little opportunity for reef study. However, many of the reefs visited and described by Gardiner (particularly in the northern Maldivian atolls) have not been revisited by modern scientists, and Gardiner's accounts remain the only records available.16

It is not surprising that several of the conclusions on reef structure and formation reached by Gardiner in the early 1900s are now not supported either because of later scientific advances, such as dating techniques, or because of more extensive observations in the region. Important examples include the following facts: that crustose coralline algae are of greater significance in reef building than Gardiner supposed; that elevated reefs in the southwest Indian Ocean have a tectonic rather than a eustatic origin as proposed by Gardiner; that dissolution of lagoons cannot be supported by seawater chemistry; and finally, that lagoons are sites of sedimentation, not erosion as Gardiner believed.17 Despite these revisions, Gardiner must be credited as one of two men (the other being his colleague Seymour Sewell) who provided the earliest detailed descriptions of reefs in the Indian Ocean. Furthermore, Gardiner was among the first to highlight that the Indian Ocean fauna varied relatively little regionally and that the focus of evolution lay in the Indonesian region—an area that became termed the ‘Indo-Pacific centre of coral diversity’ by later workers.

Consolidation and laying the foundations for the 1928–29 Great Barrier Reef Expedition

After Gardiner's return to Cambridge after 1908, his personal and academic circumstances changed substantially. He was elected a Fellow of the Royal Society and appointed University Lecturer in Zoology in 1908, and then became Professor of Zoology in 1909 when he remarried, his first wife having died in 1901. These events marked a ‘turning point in his career. The day of major expeditions was now over and, although he by no means entirely gave up visits abroad, his life henceforth centred in Cambridge as Professor of Zoology’.1 In 1909 Gardiner visited the United States, where he met Thomas Wayland Vaughan and possibly Alfred Goldsborough Mayer and Alexander Agassiz ForMemRS. The references to this visit are vague and refer to Gardiner's meeting ‘leading investigators of coral problems’. Gardiner had earlier described Vaughan as ‘our chief authority on living and fossil Madreporaria’ when consulting him on matters relating to the revision of corals in the family Fungiidae,14 and he remained a valued colleague thereafter.

During this period Gardiner laboured ceaselessly to see the collections of the Percy Sladen Expedition worked up and published despite ill-health (he was subject to recurrent bouts of malaria after having contracted the disease in Male in 1899)1 and the intervention of World War I (1914–18). Some measure of the effort involved is evident in the 400 letters written by Gardiner on these matters in the Linnean Society archives. At the same time he undertook the supervision of an Indian PhD student, Mr George Matthai, in 1911. The research topic was a comparative study of the soft parts of astraeid corals in Gardiner's collection from the Indo-Pacific, ‘mainly with a view to determining the natural relationships of the genera and species’.18 The work led to the most detailed histological work that has probably ever been performed on corals. Matthai speaks of serially sectioning 150 polyps from 75 colonies of 27 species. Although the study of soft tissues ultimately did not lead to their widespread use in coral taxonomy, they did confirm the value of budding characteristics as a key taxonomic criterion in faviid species, which had first been proposed by Edwards and Haime;19 moreover, Matthai was able, through his study of the soft parts, to show for the first time how mouths of corals formed and how valleys were derived in meandrine corals. Matthai's studies included substantial anatomical details of coral polyps, with descriptions of all the major tissue and cell types including nematocysts, mucocytes, germ cells and symbiotic algae alongside beautiful illustrations of his sections.18 This work, which also involved field studies at the Dry Tortugas laboratory and in Bermuda, would form a very valuable baseline for scientists studying coral physiology and reproductive biology during the 1928–29 Great Barrier Reef Expedition. It is interesting to reflect on the fact that this remarkable anatomical study is rarely referred to in the literature after 1932, although it is widely cited in the reports of the Great Barrier Reef Expedition. Indeed, when Buchner reviewed20 algal symbiosis in corals he cited Yonge and Boschma as the first to contribute useful anatomical detail on the symbiotic algae, yet their publications appeared at least a decade later than those of Matthai. One reason for the failure to recognize this work may lie in the fact that the title of Matthai's report ‘A revision of the recent colonial Astraeidae possessing distinct corallites’ belies its true content—this is not simply a taxonomic treatise but a valuable first attempt, under Gardiner's guidance, to study the anatomical detail of corals.

By 1920, when Gardiner was President of the Zoology Section of the British Association, it is clear that he had strong views on the way ahead for zoological studies. In his speech at the British Association meeting in Cardiff he advocated a move away from collections and taxonomy to ‘observation and experiment’, to greater interdisciplinary study and ‘the why and how animals live’.21 He commented, ‘My own conviction is that we are in danger of burying our live subject along with our specimens in museums’ and he specifically mentioned the need to understand ‘processes going on in the living body, the adaptation to environment and the problems of heredity’. These views are interesting in the light of how the research programme for the Great Barrier Reef Expedition of 1928–29 developed and how this approach subsequently influenced reef science in later years.

Also in 1920, at the first Pan Pacific Science Conference in Hawaii, Charles Hedley (a former collaborator with Gardiner in 1989 on Funafuti) highlighted the need for a marine zoological station in Australia and the problems faced by economic exploitation of marine resources in Australian waters. This presentation, an address by Professor H. C. Richards to the Royal Geographical Society of Australia on ‘Problems of the Great Barrier Reef’,22 and subsequent papers presented at the third Pan Pacific Science Conference in Australia in 1922 by both Richards and Hedley were instrumental in leading to the formation of the ‘Great Barrier Reef Committee’ in 1922. The purposes of the Committee were to further the investigation of the origin, growth and natural resources of the Great Barrier Reef of Australia. In 1926 Sir Matthew Nathan, the then retiring Governor of Queensland, contacted Gardiner about the despatch of an expedition from Great Britain to assist in marine biological aspects of the work. From this point onwards, with the formation of the ‘Barrier Reef Committee of England’ (to further the formation and funding of an expeditionary party from England to work on the Great Barrier Reef) and its expansion at the Leeds British Association meeting to become the ‘British Association Great Barrier Reef Committee’, Gardiner was closely involved in every detail of the expedition's organization. As joint secretary of this committee he assisted in the development of the scientific programme (both biological and geographical);23 ensured funding for the participation of the expedition leader, C. M. Yonge, and for the provision of equipment and a library from his own departmental resources;24 and followed the expedition progress assiduously. Indeed, Yonge wrote to Richards in 1936 saying, ‘The original Expedition was to a large extent, at least in its earlier stages on this side, his [i.e. Gardiner's] own affair’.25 But in fact Gardiner remained totally absorbed by the Expedition long beyond its completion, particularly in the review and publication of scientific papers from it.26 The letter written by Yonge to Richards in 1936 was actually in reply to concerned query from Richard over Gardiner's failure to secure funding for a second research initiative on the Great Barrier Reef. However, by this time Gardiner was in his mid-sixties and much involved in the construction of a new building for the Zoology Department, so he probably had much less energy than a decade earlier when preparing for the 1928–29 expedition. Indeed, a year later, in 1937, Gardiner retired as Professor of Zoology.

The scientific programme of the Great Barrier Reef Expedition strongly reflected Gardiner's lifelong interests in coral growth and nutrition, plankton availability and coastal geomorphology as well as other complementary studies. As a Balfour Student of Cambridge University, Yonge spent the Michaelmas term of 1927 in the Zoology Department with Gardiner, who would have offered advice based on his extensive field experience to a young man who at that stage had never seen a coral reef. It is interesting to see how Yonge's initial general proposal to the Balfour Managers on 27 March 1927 had become focused by 1 February 1928 to read:

My own particular sphere of work on the expedition will consist of a thorough study, throughout the entire year of the feeding and metabolism of a number of typical corals, not only Madreporians but also Hydrocorallines and Alcyonarians. I hope to make a thorough study of the feeding mechanism of all three, of their food (paying particular attention to seasonal variations), on their mode of digestion and of assimilation, and also of the function, during all periods of the year, of the symbiotic algae, in the hope of establishing definitely their function and true importance in the life of the corals. Studies in the metabolism of the corals and in their powers of calcium deposition, and the method employed will accompany the other work.27

The expedition was quite unlike any other that had preceded it in the coral seas, particularly in the placement of a team of scientists on a remote coral cay for 13 months, none of whom had ever previously visited a coral reef. The scientific results proved to be a milestone in the study of reef corals, providing novel information on coral nutrition, growth and reproduction, some of the first field observations and experimental accounts of coral ‘bleaching’ in response to stress, as well as quantitative ecological descriptions of the reefs in the vicinity of Low Isles on the northern Great Barrier Reef.28 As Stoddart commented, ‘The work of the Great Barrier Reef Expedition of 1928–29 emphasized for the first time the relationships between reef growth and environment and the critical importance of their study in the field’.29 Others saw the expedition as having ‘a profound effect on coral science for the next 50 years’, particularly with respect to the question of the importance of coral's symbiotic algae in coral nutrition.30 Indeed, Mather says that Yonge's view that corals were exclusively carnivores and that the symbiotic algae were of no nutritional importance was not challenged until the 1960s. In fact this was not true, because as soon as Yonge and Nicholls published their findings in 1931,28 Gardiner wrote a paper31 in which he stated that, despite the expedition findings, he still considered that the symbiotic algae contributed carbohydrate to the coral host. This belief, however, was not backed by any new experimental evidence: Gardiner relied only on his earlier work on the lack of planktonic organisms in the guts of corals and his extensive observations on the limiting effects of light on the depths to which corals grew. Although Gardiner did not agree with Yonge's interpretation of the nutrition studies he took every public opportunity of praising the general excellence of Yonge's physiological work on the Great Barrier Reef corals and he remained a firm supporter of Yonge throughout his career. Writing to Yonge in 1932, he recognized the impact of the Expedition's findings, saying, ‘Volume I and II make the expedition a success. III should be good and have much that becomes classical’.26 Indeed, the coral reproductive biology contained in volume III is still cited today, so Gardiner was quite correct in his assessment.

Although the Great Barrier Reef Expedition played an important part in the development of reef science, Gardiner received little credit for his contribution to its success. His wide experience of Indo-Pacific coral reefs—unrivalled certainly in the UK at the time—and his early work at Rotuma provided excellent foundations for the experimental approach he called for in 1920 to be fulfilled in 1928–29 through Yonge and the Great Barrier Reef Expedition. When Gardiner was awarded the Agassiz medal of the US National Academy of Sciences for his contribution to oceanographical science in 1929, he wrote to Hinks at the Royal Geographical Society saying, ‘Some of these Americans tell me how great an honour it is and it is their premier medal etc. … My biological work on the corals and the algae, while not I think the whole story in any single case is also coming to roost’.32 In fact it took a further 36 years before Gardiner's intuition was to be proved correct by the elegant work of Von Holt and Von Holt33 and Muscatine and Cernchiari34, which demonstrated the transfer of labelled carbon from symbiotic algae to the coral host. From this point onwards the fact that symbiotic algae contribute to coral nutrition has never been disputed. None of these later workers cited Gardiner's early experiments, each of them taking Yonge's work on the Great Barrier Reef as the baseline for coral nutrition studies. This is perhaps not surprising because although Yonge extensively cited Gardiner's papers in his Expedition Reports on coral nutrition he gave no specific details of Gardiner's observations, which were almost ‘buried’ in detailed expeditionary reports that focused primarily on geological and biological observations of Pacific and Indian Ocean reefs. Moreover, the Great Barrier Reef Expedition of 1928–29, and the reports that resulted from it, were such a departure from the earlier descriptive studies on coral reefs with their novel experimental approach to the study of coral physiology that for scientists addressing coral nutrition anew in the late 1960s the Expedition Reports became an obvious starting point. Even Gardiner himself recognized this major shift in scientific approach, which he had advocated in his British Association address of 1920, describing the Great Barrier Reef Expedition members as ‘experimentalists’.10

Gardiner's legacy to reef science, therefore, has been much more than descriptive reef studies from the Indian Ocean for which he is still best known, because although he was recognized by his contemporaries for his work on coral and reef growth (by Mayer35, Setchell36, Seymour Sewell37 and Yonge28) and coral nutrition (by Boschma38 and Yonge28), this legacy was not transferred to later generations of scientists. The reasons for this have been outlined above. However, one very important legacy that was, in part, born out of his early simple experiments was the scientific and administrative steerage of the Great Barrier Reef Expedition, which helped to define key questions in reef research and set the scene for a new phase in the development of reef science in the twentieth century.