Kendall D. Clements

Local phylogenetic divergence and global evolutionary convergence of skull function in reef fishes of the family Labridae

The Labridae is one of the most structurally and functionally diversified fish families on coral and rocky reefs around the world, providing a compelling system for examination of evolutionary patterns of functional change. Labrid fishes have evolved a diverse array of skull forms for feeding on prey ranging from molluscs, crustaceans, plankton, detritus, algae, coral and other fishes. The species richness and diversity of feeding ecology in the Labridae make this group a marine analogue to the cichlid fishes. Despite the importance of labrids to coastal reef ecology, we lack evolutionary analysis of feeding biomechanics among labrids. Here, we combine a molecular phylogeny of the Labridae with the biomechanics of skull function to reveal a broad pattern of repeated convergence in labrid feeding systems. Mechanically fast jaw systems have evolved independently at least 14 times from ancestors with forceful jaws. A repeated phylogenetic pattern of functional divergence in local regions of the labrid tree produces an emergent family-wide pattern of global convergence in jaw function. Divergence of close relatives, convergence among higher clades and several unusual ‘breakthroughs’ in skull function characterize the evolution of functional complexity in one of the most diverse groups of reef fishes.

Hindgut Fermentation in Three Species of Marine Herbivorous Fish

ABSTRACT Symbioses with gut microorganisms provides a means by which terrestrial herbivores are able to obtain energy. These microorganisms ferment cell wall materials of plants to short-chain fatty acids (SCFA), which are then absorbed and used by the host animal. Many marine herbivorous fishes contain SCFA (predominantly acetate) in their hindgut, indicative of gut microbial activity, but rates of SCFA production have not been measured. Such information is an important prerequisite to understanding the contribution that gut microorganisms make in satisfying the energy needs of the fish. We have estimated the rates of acetate production in the gut of three species of temperate marine herbivorous fish from northeastern New Zealand: Kyphosus sydneyanus (family Kyphosidae), Odax pullus (family Odacidae), and Aplodactylus arctidens (family Aplodactylidae). Ex vivo preparations of freshly caught fish were maintained with their respiratory and circulatory systems intact, radiolabeled acetate was injected into ligated hindgut sections, and gut fluid was sampled at 20-min intervals for 2 h. Ranges for acetate turnover in the hindguts of the studied species were determined from the slope of plots as the log of the specific radioactivity of acetate versus time and pool size, expressed on a nanomole per milliliter per minute basis. Values were 450 to 570 (K. sydneyanus), 373 to 551 (O. pullus), and 130 to 312 (A. arctidens). These rates are comparable to those found in the guts of herbivorous reptiles and mammals. To determine the contribution of metabolic pathways to the fate of acetate, rates of sulfate reduction and methanogenesis were measured in the fore-, mid-, and hindgut sections of the three fish species. Both rates increased from the distal to proximal end of the hindgut, where sulfate reduction accounted for only a small proportion (<5%) of acetate methyl group transformed to CO2, and exceeded methanogenesis from acetate by >50-fold. When gut size was taken into account, acetate uptake from the hindgut of the fish species, determined on a millimole per day per kilogram of body weight basis, was 70 (K. sydneyanus), 18 (O. pullus), and 10 (A. arctidens).

Extreme polyploidy in a large bacterium

Cells rely on diffusion to move metabolites and biomolecules. Diffusion is highly efficient but only over short distances. Although eukaryotic cells have broken free of diffusion-dictated constraints on cell size, most bacteria and archaea are forced to remain small. Exceptions to this rule are found among the bacterial symbionts of surgeonfish; Epulopiscium spp. are cigar-shaped cells that reach lengths in excess of 600 μm. A large Epulopiscium contains thousands of times more DNA than a bacterium such as Escherichia coli, but the composition of this DNA is not well understood. Here, we present evidence that Epulopiscium contains tens of thousands of copies of its genome. Using quantitative, single-cell PCR assays targeting single-copy genes, we have determined that copy number is positively correlated with Epulopiscium cell size. Although other bacteria are known to possess multiple genomes, polyploidy of the magnitude observed in Epulopiscium is unprecedented. The arrangement of genomes around the cell periphery may permit regional responses to local stimuli, thus allowing Epulopiscium to maintain its unusually large size. Surveys of the sequences of single-copy genes (dnaA, recA, and ftsZ) revealed genetic homogeneity within a cell consistent with only a small amount (≈1%) of the parental DNA being transferred to the next generation. The results also suggest that the abundance of genome copies in Epulopiscium may allow for an unstable genetic feature, a long mononucleotide tract, in an essential gene. With the evolution of extreme polyploidy and large cell size, Epulopiscium has acquired some of the advantages of eukaryotic cells.

Fermentation and Gastrointestinal Microorganisms in Fishes

Microbial fermentation and nutrient synthesis are typically important in organisms with a diet high in fiber (Stevens 1988) — i.e., a diet mainly composed of carbohydrates resistant to endogenous digestive enzymes (Annison 1993). Fermentative digestion thus occurs typically in animals with a diet composed predominantly of plant material (Bergman 1990), and symbioses with microorganisms have been well studied in herbivorous mammals, birds, and reptiles (Stevens 1988). It is therefore surprising that the endosymbiotic communities of the dominant aquatic vertebrate herbivores, the fishes, remain poorly understood. Only recently have diverse microbial communities been reported from the guts of herbivorous fishes (Fishelson et al. 1985, Rimmer and Wiebe 1987, Clements et al. 1989, Clements 1991a), and almost nothing is known of the role of these symbioses in digestion. As a result of this, the material covered in this review will be somewhat different from that covered in other chapters.

Intestinal microbiota in fishes: what's known and what's not

High‐throughput sequencing approaches have enabled characterizations of the community composition of numerous gut microbial communities, which in turn has enhanced interest in their diversity and functional relationships in different groups of vertebrates. Although fishes represent the greatest taxonomic and ecological diversity of vertebrates, our understanding of their gut microbiota and its functional significance has lagged well behind that of terrestrial vertebrates. In order to highlight emerging issues, we provide an overview of research on fish gut microbiotas and the biology of their hosts. We conclude that microbial community composition must be viewed within an informed context of host ecology and physiology, and that this is of particular importance with respect to research planning and sampling design.

Fermentation in Tropical Marine Herbivorous Fishes

Short-chain fatty acids (SCFAs) were estimated in the gut and arterial blood of tropical marine fishes collected from the vicinity of Lizard Island, Great Barrier Reef Species sampled were predominantly herbivorous, with some related nonherbivorous species. A total of 253 individuals from the following taxa were examined: Acanthuridae, 18 species; Siganidae, eight species; Scaridae, four species; Kyphosidae, one species; and Pomacanthidae, one species. The highest concentration of SCFA in the gut of all species was in the posterior half of the intestine, where the mean acetate concentration per species ranged from 3 to 40 mM. Lower concentrations of propionate, butyrate, and isovalerate were found in the gut of all species. The highest concentrations of SCFAs were found in species that fed on macroalgae, and the lowest concentrations in species that fed on sediments. Substantial concentrations of SCFAs were found in some planktivorous acanthurids. Acetate was present in the blood of species examined at concentrations of 0.45-3.80 mM. In addition, some species of acanthurids and all species of siganids examined had high blood levels of isovalerate. The high concentration of SCFAs in the intestine of some species suggests that gastrointestinal microorganisms contribute to the nutrition of many of the species examined.

ALGAL MACRONUTRIENTS AND FOOD SELECTION BY THE OMNIVOROUS MARINE FISH GIRELLA TRICUSPIDATA

We used combined field and laboratory studies to investigate the relationships among foraging, food selection, and macronutrient intake and retention by the New Zealand marine reef fish, Girella tricuspidata (F. Girellidae). Gut analyses of field-caught fish revealed a diet comprising significant proportions both of algal and non-algal (copepods, hydroids, and organic detritus) foods, with the relative proportions of algal and non-algal food items varying from 65% of non-algal foods in the winter to 34% in autumn. Observations of the diurnal feeding pattern of free-ranging wild fish showed an increase in bite rate from sunrise to late afternoon, followed by a decrease toward sunset. In laboratory studies we recorded (a) gut throughput rates, (b) macronutrient intake, and (c) macronutrient assimilation by captive G. tricuspidata fed one of three algal species. The algae were Enteromorpha intestinalis and Ulva lactuca, both of which are preferred foods of G. tricuspidata, and Gracilaria chilensis, which has not been recorded in the stomach contents of the fish despite its co-occurrence in some habitats. The two species of preferred algae were found to have a higher starch and lower protein content than the non-dietary G. chilensis. The fish regulated their intake and utilization of the algae such that similar amounts of protein were ingested and assimilated from all three species, but less starch was ingested and assimilated from the non-dietary G. chilensis than from the preferred species. Gut throughput times correlated positively with starch availability in the algae but were lower for all treatments than previous studies would suggest are associated with fermentative digestion. The data suggest that omnivory in G. tricuspidata is likely based on complementarity, rather than substitutability of algal and animal foods.

Disaptation and recovery in the evolution of Antarctic fishes

The radiation of notothenioid fishes provides an excellent system to explore issues of evolution and adaptation. Most studies emphasize adaptation to the extreme Antarctic environment; however, recent work provides cogent examples of disaptation or evolutionary loss of function. The nature and extent of regressive change is revealed by subsequent adaptive recovery. Ancestral notothenioids were benthic but some became secondarily pelagic through the retention of larval characters. Paedomorphosis has produced detrimental changes in lateral-line sensory systems that have been made good by compensatory adaptation. In the icefish family, compensatory adaptation has followed the loss of the oxygen-binding pigments haemoglobin and myoglobin.

The likelihood of extinction of iconic and dominant herbivores and detritivores of coral reefs: the parrotfishes and surgeonfishes

Parrotfishes and surgeonfishes perform important functional roles in the dynamics of coral reef systems. This is a consequence of their varied feeding behaviors ranging from targeted consumption of living plant material (primarily surgeonfishes) to feeding on detrital aggregates that are either scraped from the reef surface or excavated from the deeper reef substratum (primarily parrotfishes). Increased fishing pressure and widespread habitat destruction have led to population declines for several species of these two groups. Species-specific data on global distribution, population status, life history characteristics, and major threats were compiled for each of the 179 known species of parrotfishes and surgeonfishes to determine the likelihood of extinction of each species under the Categories and Criteria of the IUCN Red List of Threatened Species. Due in part to the extensive distributions of most species and the life history traits exhibited in these two families, only three (1.7%) of the species are listed at an elevated risk of global extinction. The majority of the parrotfishes and surgeonfishes (86%) are listed as Least Concern, 10% are listed as Data Deficient and 1% are listed as Near Threatened. The risk of localized extinction, however, is higher in some areas, particularly in the Coral Triangle region. The relatively low proportion of species globally listed in threatened Categories is highly encouraging, and some conservation successes are attributed to concentrated conservation efforts. However, with the growing realization of mans profound impact on the planet, conservation actions such as improved marine reserve networks, more stringent fishing regulations, and continued monitoring of the population status at the species and community levels are imperative for the prevention of species loss in these groups of important and iconic coral reef fishes.

Occurrence and characteristics of unusual protistan symbionts from surgeonfishes (Acanthuridae) of the Great Barrier Reef, Australia

The occurrence of unusual symbiotic microorganisms was examined in the intestines of a range of fish from the Great Barrier Reef, Australia. The fish taxa examined included 26 species of the family Acanthuridae, as well as representatives of phylogenetically related and herbivorous taxa. The microorganisms, referred to as protists, were only found in herbivorous and detritivorous members of the Acanthuridae. Protists were not found in planktivorous acanthurids, nor in any members of the families Kyphosidae, Pomacentridae, Scaridae, Zanclidae, Siganidae and Bleniidae we examined. In addition, protists were absent from the herbivorous acanthurids A. xanthopterus and A. nigricans. A range of protist forms, characterized by differences in size (8 to 417 μm), shape and mode of cell division (daughter-cell production and binary fission), was observed. The occurrence of these forms appeared to be correlated with host feedingecology. Large forms (>100 μm) of the protists were only found in acanthurids which fed over hard-reef substrata. Smaller forms were found in sand-grazing and detritivorous species. One of the protist forms appears identical to protists previously reported from Red Sea acanthurids.