Coelacanths: a human responsibility

The living coelacanth Latimeria chalumnae has a unique position in world biodiversity which raises important questions about conservation and ethics. Some relevant details of coelacanth biology are summarized, including those obtained by direct observation from submersibles. The importance of the coelacanth for evolutionary theory and palaeontology is shown to be paralleled in cultural, literary and artistic areas of human heritage. Threats to the Comoran coelacanths from artisanal fishing are described and conservation measures discussed in relation to local customs and economies as well as the promotion of tourism to spread a new awareness and concern for coelacanths worldwide.     

Why coelacanths are not ‘living fossils’

A series of recent studies on extant coelacanths has emphasised the slow rate of molecular and morphological evolution in these species. These studies were based on the assumption that a coelacanth is a ‘living fossil’ that has shown little morphological change since the Devonian, and they proposed a causal link between low molecular evolutionary rate and morphological stasis. Here, we have examined the available molecular and morphological data and show that: (i) low intra‐specific molecular diversity does not imply low mutation rate, (ii) studies not showing low substitution rates in coelacanth are often neglected, (iii) the morphological stability of coelacanths is not supported by paleontological evidence. We recall that intra‐species levels of molecular diversity, inter‐species genome divergence rates and morphological divergence rates are under different constraints and they are not necessarily correlated. Finally, we emphasise that concepts such as ‘living fossil’, ‘basal lineage’, or ‘primitive extant species’ do not make sense from a tree‐thinking perspective. Editor's suggested further reading in BioEssays Tree thinking for all biology: the problem with reading phylogenies as ladders of progress Abstract     

Extremely slow rate of evolution in the HOX cluster revealed by comparison between Tanzanian and Indonesian coelacanths

Coelacanths are known as "living fossils" because their morphology has changed very little from that in the fossil record. To elucidate why coelacanths have evolved so slowly is thus of primary importance in evolutionary biology. In the present study, we determined the entire sequence of the HOX cluster of the Tanzanian coelacanth (Latimeria chalumnae) and compared it with that of the Indonesian coelacanth (L. menadoensis), which was available in the literature. The most intriguing result was the extremely small genetic divergence between the two coelacanths. The synonymous divergence of the HOX coding region between the two coelacanths was estimated to be 0.07%, which is ~11-fold smaller than that of human-chimp. When we applied the estimated divergence time of the two coelacanths of 6 million years ago (MYA) and 30 MYA, which were proposed in independent mitochondrial DNA analyses, the synonymous substitution rate of the coelacanth HOX cluster was estimated to be ~11-fold and 56-fold smaller than that of human-chimp, respectively. Thus, the present study implies that the reduction of the nucleotide substitution rate in coelacanth HOX genes may account for the conservation of coelacanth morphology during evolution.     

Habitat and population size of the coelacanth Latimeria chalumnae at Grand Comoro

Synopsis In 1987 and 1989 coelacanths were observed for the first time in their natural habitat with the help of submersibles. Coelacanths were found between 150–253 m depth, their preferential depth seems to be around 200 m; the water temperature ranged between 16.5–22.8° C. During the day coelacanths aggregate in small non-aggressive groups in sheltered lava-caves. Caves might be a limiting factor for distribution. At night they leave the caves for hunting by drifting singly along the steep lava slopes. They migrate between different caves located within a large home range covering more than 8 km coastline. Coelacanths are site-attached, some for a period of at least 2 years. Our own observations and earlier catch records show that only the west coast of Grand Comoro is a suitable coelacanth habitat with more structural complexity and prey fish abundance than other coastlines of the island. From our survey we estimated a total coelacanth population off Grand Comoro to be 150–210 individuals; a saturated population would be 370–510 individuals. This small relict population seems to be stable. International protection of coelacanths against commercial interests is needed     

Relationship among coelacanths,lungfishes, and tetrapods: A phylogenetic analysis based on mitochondrial cytochrome oxidase I gene sequences

To clarify the relationship among coelacanths, lungfishes, and tetrapods, the amino acid sequences deduced from the nucleotide sequences of mitochondrial cytochrome oxidase subunit I (COI) genes were compared. The phylogenetic tree of these animals, including the coelacanth Latimeria chalumnae and the lungfish Lepidosiren paradoxa, was inferred by several methods. These analyses consistently indicate a coelacanth/lungfish clade, to which little attention has been paid by previous authors with the exception of some morphologists. Overall evidence of other mitochondrial genes reported previously and the results of this study equally support the coelacanth/lungfish and lungfish/tetrapod clades, ruling out the coelacanth/tetrapod clade.Correspondence to: K. Watanabe 0592     

Silver coelacanths from Spain are not proofs of a Pre-scientific Discovery

In 1964 and 1965, two silver fish pendants depicting coelacanths and thought to be religious votive from Spanish churches were purchased on the art market in Spain, dated between the 17th and late 19th century, long before the discovery for science of the living coelacanth in 1938. It was speculated that they originated either from the Mediterranean, subtropical Atlantic, or subtropical Pacific (de Sylva 1966, Bruton 1985, Anonymous 1993, Greenwell 1994, Raynold & Mangiacopra 1995). Some authors believe that the silver fish pendants represent a new species of coelacanthiforms (Raynold & Mangiacopra 1995), others claimed the pendants to be only a wishful fantasy of scientists and not coelacanths at all (Thomson 1991). However, new studies revealed that the silver fish artefacts are indeed coelacanths but were in fact produced more recently with the Comorian coelacanth, Latimeria chalumnae, as a model.     

The ecology and conservation of the coelacanth Latimeria chalumnae

Synopsis Studies on the ecology of the living coelacanth, Latimeria chalumnae, are reviewed and assessed. Early predictions on the life history of the coelacanth have proved to be accurate but recent findings have improved our understanding of its habitat and feeding preferences, diel activity patterns and social behaviour. A history of coelacanth conservation reveals that there has been a sustained concern for the survival of this species which has eventually culminated in several effective conservation actions in recent years. The coelacanth is threatened by a number of socio-economic and biological factors, but international action directed at managing the fishery in the Comoros should ensure that the species survives. Recent observations on living coelacanths in their natural environment have greatly improved our knowledge of the behaviour and relative abundance of adults. Important priorities for future research include studies on the distribution and abundance of juveniles and breeding adults, both off the Comoros and elsewhere. The coelacanth is a highly specialised, precocial fish which occupies a unique place in biology. Co-ordinated international efforts should continue to be made to understand and conserve this remarkable fish.     

Enzymes of the coelacanth Latimeria chalumnae evidenced by starch gel electrophoresis

Synopsis The coelacanth, Latimeria chalumnae, is often referred to as a living relic. The opportunity to examine its biochemical molecular structure was sought in an effort to define the degree of its genetic variability. The coelacanth is thought to live only in a small area around the Comoro Islands in the Western Indian Ocean. The scenario presented suggests that the coelacanth may have lost genetic variability as a result of genetic drift within a small population. The narrow geographic range of the coelacanth suggests adjustment to a relatively limited environment. The loss of specific alleles through genetic drift can reduce the ability of a fish population to adapt to changes in environmental conditions. The coelacanth needs strong conservation measures to be taken to curtail the capture of specimens and for the protection of its limited natural habitat.     

Population divergence in East African coelacanths

The coelacanth, Latimeria chalumnae, occurs at the Eastern coast of Africa from South Africa up to Kenya. It is often referred to as a living fossil mainly because of its nearly unchanged morphology since the Middle Devonian. As it is a close relative to the last common ancestor of fish and tetrapods, molecular studies mostly focussed on their phylogenetic relationships. We now present a population genetic study based on 71 adults from the whole known range of the species. Despite an overall low genetic diversity, there is evidence for divergence of local populations. We assume that originally the coelacanths at the East African Coast derived from the Comoros population, but have since then diversified into additional independent populations: one in South Africa and another in Tanzania. Unexpectedly, we find a split of the Comoran coelacanths into two sympatric subpopulations. Despite its undeniably slow evolutionary rate, the coelacanth still diversifies and is therefore able to adapt to new environmental conditions.     

An inventory of all known specimens of the coelacanth Latimeria chalumnae,with comments on trends in the catches

Synopsis A list is presented of all known specimens of the coelacanth Latimeria chalumnae based on a survey of the literature and of museum, aquarium and university holdings. Details are given of the date, place, time and depth of capture, the name and age of the fisherman, the length, weight and sex of the fish, the first literature record, the method of preservation and the present location of specimens, if known. A new number is assigned to each specimen. At least 172 coelacanths are known to have been caught since 1938. The first coelacanth was caught off South Africa but all properly documented, subsequent specimens have been caught off the islands of Grand Comoro and Anjouan in the Comoros. An appeal is made to the Comoran authorities for each specimen that is caught to be made available for scientific study. Museum authorities are also encouraged to allow their specimens to be X-rayed or dissected so that vital information can be obtained on fecundity, foetal nutrition and dietary preferences. It is essential for the coelacanth conservation effort that this inventory is maintained by the Coelacanth Conservation Council.     

Bibliography of the living coelacanth Latimeria chalumnae,with comments on publication trends

Synopsis A list of published references on the coelacanth Latimeria chalumnae is provided. All known publications in the scientific literature are included as well as popular articles and press reports that are considered to provide new information or interpretations. Marked trends are noticeable in the literature as different disciplines have been applied to research on the coelacanth over the past five decades. The bibliography lists a total of 823 publications including 490 papers in journals, 37 books, 3 theses, 45 chapters in books, 166 popular articles, 22 reports and 60 newspaper articles. Studies on taxonomy and morphology initially dominated the literature followed by reports on research in the fields of physiology, behaviour, breeding biology, ecology and conservation as frozen and eventually live specimens became available for study. The literature on the living coelacanth is predominantly in English, French, Japanese and German but references in 12 other languages were also traced. The dominant authors in the first decades of coelacanth research were the French scientists J. Millot and J. Anthony and the South African describer of the first and second coelacanths, J.L.B. Smith. In subsequent years French, British, American, South African, Japanese, Canadian and German authors, among others, have made significant contributions.     

Early Growth Stages in Coelacanth Fishes

ALL known specimens of the Recent coelacanth fish, Latimeria, are large specimens (mostly more than 100 cm total length) and only one female with eggs has been recorded^1,2. Consequently, the ontogeny and the early growth stages of the Recent coelacanth are unknown. In the fossil record, one specimen of Holophagus (= Undina) from the Upper Jurassic of Solnhofen, southern Germany, has been recorded with two young coelacanths inside³. Watson has argued from this finding that the coelacanths are viviparous but it seems more reasonable to interpret this fossil specimen as a cannibal that had just swallowed two young of its own kind. This interpretation is favoured by the position of the two specimens and by the discovery of other fossil coelacanths containing large specimens of other kinds of fishes in their stomachs⁴.     

Probable evolution of the coelacanth's reproductive style: lecithotrophy and orally feeding embryos in cichlid fishes and in Latimeria chalumnae

Synopsis The living coelacanth is a livebearer. Yolk seems to be the main source of nutrients and of oxygen to the embryo (fetus). Long before birth, young may also possibly feed orally on histotrophe secretion and egg debris. This type of reproduction evolved, as in most other fishes, from oviparity. The Carboniferous coelacanth Rhabdoderma exiguum had eggs of much lesser yolk volume and may represent an earlier form of oviparity with hiding, guarding or brooding type of parental care. The Jurassic coelacanth Holophagus (Undina) and the Cretaceous Axelrodichthys appear to have already evolved the internal-bearing style. Much of this evolutionary sequence is similar to that in cichlids. Ancestral cichlids are substrate tenders and nesters, with small eggs, little yolk and a feeding larva with indirect development. Mouthbrooding cichlids evolved a few, large eggs with denser yolk, direct development and, ultimately, orally feeding embryos while yolk is still in ample supply. Mixed feeding from yolk and orally ingested food in cichlids and in coelacanths is shown to be an enhanced mode of food delivery to the embryos over that from each source separately, in order to produce directly a better developed or larger young at the time of release, i.e. independence. Increase in egg size is regarded as an environmentally induced, altered pattern of yolk synthesis and an initial component of the epigenetic mechanism leading towards greater specialization. Carotenoids are incorporated within the yolk to assist the oxidative metabolism of the developing embryo.     

Predicting suitable environments and potential occurrences for coelacanths (Latimeria spp.)

Extant coelacanths (Latimeria chalumnae) were first discovered in the western Indian Ocean in 1938; in 1998, a second species of coelacanth, Latimeria menadoensis, was discovered off the north coast of Sulawesi, Indonesia, expanding the known distribution of the genus across the Indian Ocean Basin. This study uses ecological niche modeling techniques to estimate dimensions of realized niches of coelacanths and generate hypotheses for additional sites where they might be found. Coelacanth occurrence information was integrated with environmental and oceanographic data using the Genetic Algorithm for Rule-set Production (GARP) and a maximum entropy algorithm (Maxent). Resulting models were visualized as maps of relative suitability of sites for coelacanths throughout the Indian Ocean, as well as scatterplots of ecological variables. Our findings suggest that the range of coelacanths could extend beyond their presently known distribution and suggests alternative mechanisms for currently observed distributions. Further investigation into these hypotheses could aid in forming a more complete picture of the distributions and populations of members of genus Latimeria, which in turn could aid in developing conservation strategies, particularly in the case of L. menadoensis.     

Mitogenomic analysis for coelacanths (Latimeria chalumnae) caught in Tanzania

In recent years, a large number of individuals of the species Latimeria chalumnae, one of the living fossil coelacanths, have been landed off the coast of Tanzania. Although L. chalumnae specimens have also been landed at other localities in the western Indian Ocean, so far, viable populations of this species have been identified only at two localities, Comoros and South Africa. Therefore, the recent active catch off Tanzania suggests a new habitat for L. chalumnae. To examine the genetic background of the Tanzanian fish, we analyzed complete mtDNA sequences of two Tanzanian individuals (Kigombe-9 and Songo Mnara-1) collected from the north and south coasts of Tanzania. Using the recently reported criteria for six haplotypes established in a population genetic study for coelacanths living in the western Indian Ocean [Schartl, M., Hornung, U., Hissman, K., Schauer, J., Fricke, H., 2005. Relatedness among east African coelacanths. Nature 435, 901.], we characterized Songo Mnara-1 as haplotype 1 and Kigombe-9 as haplotype 5. We suggest that the Songo Mnara specimen is a member of the Comoran group, but was swept away by the South Equatorial current. The individual from Kigombe may be a member of an undiscovered population that exists near the boundary between Tanzania and Kenya. Further analysis using more than 19 individuals recently captured off the north coast of Tanzania will reveal whether a new population exists there. Our sequence data suggest additional variable sites in the mtDNA sequence that may define the population structure of coelacanths in the western Indian Ocean and also raise the possibility that the previously published Comoran coelacanth mtDNA sequence contains several critical errors including base changes and indels.     

A fiftieth anniversary reflection on the living coelacanth,Latimeria chalumnae: some new interpretations of its natural history and conservation status

Synopsis It all started about 400 million years ago, when representatives of a group of fish-like fleshy-finned creatures appeared in the fossil record (or was it through a childhood dream shared by all of us that we would one day study the coelacanth?). Many of the coelacanth's characters placed them close to the ancestry of terrestrial vertebrates. About 70 million years ago they disappeared from the fossil record. The discovery in 1938 of the first living coelacanth, in 1952 of the second and until now over 200 specimens parallels in excitement an encounter with a live dinosaur on a weekend walk, and in significance even more than that. For this year's 50th anniversary of the famous discovery of the first living coelacanth, we retraced the routes and visited the main actors of this zoological drama. New insights into coelacanth natural history were facilitated by novel interpretation of earlier data and our expeditions to the Comoro Islands, retracing the route of the second specimen, measuring unrecorded specimens, interviewing fishermen and describing their fishing crafts, and taking part in recent events on land and water near the only known habitat of the living coelacanth. Entry into this habitat and observations from the research submersible GEO opened up a new era in coelacanth research. Past studies of preserved specimens, which were caught as an incidental bycatch, were supplemented for the first time by studies of free-living coelacanths in their natural habitat. The first film footage taken from the submersible revealed the entirely unfishlike movements of this creature. Its mode of locomotion is a combination of flying and gliding, interspersed with head stands and belly-up drifts which appear to defy gravity. The narrow range of habitat in which the coelacanth has been encountered has led us to realize how vulnerable this ancient relict is. The members of our expeditions therefore cooperated in establishing an international organisation to coordinate efforts to conserve the coelacanth. Editorial     

A newly recognized fossil coelacanth highlights the early morphological diversification of the clade

Previously considered an actinopterygian or an osteichthyan incertae sedis, the Devonian (Givetian-Frasnian) Holopterygius nudus is reinterpreted as a coelacanth. This genus is among the oldest coelacanths known from articulated remains, but its eel-like morphology marks a considerable departure from the conventional coelacanth body plan. A cladistic analysis places Holopterygius as the sister taxon of the Carboniferous (Serpukhovian) genus Allenypterus. Despite the specialized morphology of these genera, they occupy a surprisingly basal position in coelacanth phylogeny; only Diplocercides and Miguashaia are further removed from the crown. A morphometric analysis reveals that coelacanths were anatomically disparate early in their history. Conflicts between this result and those of previous studies challenge the adequacy of systematic character sets for describing historical patterns of morphological variety. Coelacanths have long had an iconic place in the study of vertebrate evolution for their apparent anatomical conservatism over geological time, but Holopterygius provides clear evidence for rapid morphological evolution early in the history of this clade.     

Function of the pseudomaxillary fold in the mouth opening of the coelacanth, <Emphasis Type="Italic">Latimeria chalumnae</Emphasis>

The oral region of a coelacanth, Latimeria chalumnae, from the Comoro Islands, was examined in fresh condition, and the complex folding of the membrane between the lower jaw and the skull, and a strut-like structure in the membrane were found. When the mouth opened, the pseudomaxillary folds covered the lateral walls of the mouth. The movement of the membrane is inferred from the observation of the specimen. Coelacanths developed a way of covering the lateral sides of mouth that is different from that of other fishes; especially the pseudomaxillary fold above the strut is unique to coelacanths, but the pseudomaxillary fold below the strut is similar to the lower lip fold of the lepidosirenoid lungfish.     

Recovery rates of bottlenose dolphin (Tursiops truncatus) carcasses estimated from stranding and survival rate data

Recovery of cetacean carcasses provides data on levels of human‐caused mortality, but represents only a minimum count of impacts. Counts of stranded carcasses are negatively biased by factors that include at‐sea scavenging, sinking, drift away from land, stranding in locations where detection is unlikely, and natural removal from beaches due to wave and tidal action prior to detection. We estimate the fraction of carcasses recovered for a population of coastal bottlenose dolphins (Tursiops truncatus), using abundance and survival rate data to estimate annual deaths in the population. Observed stranding numbers are compared to expected deaths to estimate the fraction of carcasses recovered. For the California coastal population of bottlenose dolphins, we estimate the fraction of carcasses recovered to be 0.25 (95% CI = 0.20–0.33). During a 12 yr period, 327 animals (95% CI = 253–413) were expected to have died and been available for recovery, but only 83 carcasses attributed to this population were documented. Given the coastal habits of California coastal bottlenose dolphins, it is likely that carcass recovery rates of this population greatly exceed recovery rates of more pelagic dolphin species in the region.     

Molecules,fossils, and the origin of tetrapods

Summary Since the discovery of the coelacanth, Latimeria chalumnae, more than 50 years ago, paleontologists and comparative morphologists have debated whether coelacanths or lungfishes, two groups of lobe-finned fishes, are the closest living relatives of land vertebrates (Tetrapoda). Previously, Meyer and Wilson (1990) determined partial DNA sequences from two conservative mitochondrial genes and found support for a close relationship of lungfishes to tetrapods. We present additional DNA sequences from the 12S rRNA mitochondria gene for three species of the two lineages of lungfishes that were not represented in the first study: Protopterus annectens and Protopterus aethiopicus from Africa and Neoceratodus forsteri (kindly provided by B. Hedges and L. Maxson) from Australia. This extended data set tends to group the two lepidosirenid lungfish lineages (Lepidosiren and Protopterus) with Neoceratodus as their sister group. All lungfishes seem to be more closely related to tetrapods than the coelacanth is. This result appears to rule out the possibility that the coelacanth lineage gave rise to land vertebrates. The common ancestor of lungfishes and tetrapods might have possessed multiple morphological traits that are shared by lungfishes and tetrapods [Meyer and Wilson (1990) listed 14 such traits]. Those traits that seem to link Latimeria and tetrapods are arguably due to convergent evolution or reversals and not to common descent. In this way, the molecular tree facilitates an evolutionary interpretation of the morphological differences among the living forms. We recommended that the extinct groups of lobe-finned fishes be placed onto the molecular tree that has lungfishes and not the coelacanth more closely related to tetrapods. The placement of fossils would help to further interpret the sequence of morphological events and innovations associated with the origin of tetrapods but appears to be problematic because the quality of fossils is not always high enough, and differences among paleontologists in the interpretation of the fossils have stood in the way of a consensus opinion for the branching order among lobefinned fishes. Marshall and Schultze (1992) criticized the morphological analysis presented by Meyer and Wilson (1990) and suggest that 13 of the 14 morphological traits that support the sister group relationship of lungfishes and tetrapods are not shared derived characters. Here we present further alternative viewpoints to the ones of Marshall and Schultze (1992) from the paleontological literature. We argue that all available information (paleontological, neontological, and molecular data) and rigorous cladistic methodology should be used when relating fossils and extant taxa in a phylogenetic framework. Offprint requests to: Axel Meyer