Bruno Frederich

Iterative Ecological Radiation and Convergence during the Evolutionary History of Damselfishes (Pomacentridae)

Coral reef fishes represent one of the most spectacularly diverse assemblages of vertebrates on the planet, but our understanding of their mode of diversification remains limited. Here we test whether the diversity of the damselfishes (Pomacentridae), one of the most species-rich families of reef-associated fishes, was produced by a single or multiple adaptive radiation(s) during their evolutionary history. Tests of the tempo of lineage diversification using a time-calibrated phylogeny including 208 species revealed that crown pomacentrid diversification has not slowed through time as expected under a scenario of a single adaptive radiation resulting from an early burst of diversification. Evolutionary modeling of trophic traits similarly rejected the hypothesis of early among-lineage partitioning of ecologically important phenotypic diversity. Instead, damselfishes are shown to have experienced iterative convergent radiations wherein subclades radiate across similar trophic strategies (i.e., pelagic feeders, benthic feeders, intermediate) and morphologies. Regionalization of coral reefs, competition, and functional constraints may have fueled iterative ecological radiation and convergent evolution of damselfishes. Through the Pomacentridae, we illustrate that radiations may be strongly structured by the nature of the constraints on diversification.

Trophic niches of thirteen damselfishes (Pomacentridae) at the Grand Récif of Toliara, Madagascar

The damselfishes, with more than 340 species, constitute one of the most important families that live in the coral reef environment. Most of our knowledge of reef-fish ecology is based on this family, but their trophic ecology is poorly understood. The aim of the present study was to determine the trophic niches of 13 sympatric species of damselfishes by combining stable isotope (δ15N and δ13C) and stomach content analyses. Isotopic signatures reveal three main groups according to their foraging strategies: pelagic feeders (Abudefduf sexfasciatus, A. sparoides, A. vaigiensis, Chromis ternatensis, C. dimidiata, Dascyllus trimaculatus and Pomacentrus caeruleus), benthic feeders (Chrysiptera unimaculata, Plectroglyphidodon lacrymatus and Amphiprion akallopisos) and an intermediate group (D. aruanus, P. baenschi and P. trilineatus). Stomach contents reveal that planktonic copepods and filamentous algae mainly represent the diets of pelagic feeders and benthic feeders, respectively. The intermediate position of the third group resulted from a partitioning of small planktonic prey, small vagile invertebrates and filamentous algae. In this last feeding group, the presence of a wide range of δ13C values in P. trilineatus suggests a larger trophic niche width, related to diet-switching over time. Some general considerations about the feeding habits of damselfishes reveal that their choice of habitat on the reef and their behavior appear to be good predictors of diet in this group. Benthic (algae and/or small invertebrates) feeders appear to be solitary and defend a small territory on the bottom; zooplankton feeders remain in groups just above the reef, in the water column.

Agonistic sounds in the skunk clownfish Amphiprion akallopisos: size‐related variation in acoustic features

Fourteen individuals of the skunk clownfish Amphiprion akallopisos of different sizes and of different sexual status (non-breeder, male or female) were analysed for four acoustic features. Dominant frequency and pulse duration were highly correlated with standard length (r = 0.97), and were not related to sex. Both the dominant frequency and pulse duration were signals conveying information related to the size of the emitter, which implies that these sound characteristics could be useful in assessing size of conspecifics.

Bipartite life cycle of coral reef fishes promotes increasing shape disparity of the head skeleton during ontogeny: an example from damselfishes (Pomacentridae)

BackgroundQuantitative studies of the variation of disparity during ontogeny exhibited by the radiation of coral reef fishes are lacking. Such studies dealing with the variation of disparity, i.e. the diversity of organic form, over ontogeny could be a first step in detecting evolutionary mechanisms in these fishes. The damselfishes (Pomacentridae) have a bipartite life-cycle, as do the majority of demersal coral reef fishes. During their pelagic dispersion phase, all larvae feed on planktonic prey. On the other hand, juveniles and adults associated with the coral reef environment show a higher diversity of diets. Using geometric morphometrics, we study the ontogenetic dynamic of shape disparity of different head skeletal units (neurocranium, suspensorium and opercle, mandible and premaxilla) in this fish family. We expected that larvae of different species might be relatively similar in shapes. Alternatively, specialization may become notable even in the juvenile and adult phase.ResultsThe disparity levels increase significantly throughout ontogeny for each skeletal unit. At settlement, all larval shapes are already species-specific. Damselfishes show high levels of ontogenetic allometry during their post-settlement growth. The divergence of allometric patterns largely explains the changes in patterns and levels of shape disparity over ontogeny. The rate of shape change and the length of ontogenetic trajectories seem to be less variable among species. We also show that the high levels of shape disparity at the adult stage are correlated to a higher level of ecological and functional diversity in this stage.ConclusionDiversification throughout ontogeny of damselfishes results from the interaction among several developmental novelties enhancing disparity. The bipartite life-cycle of damselfishes exemplifies a case where the variation of environmental factors, i.e. the transition from the more homogeneous oceanic environment to the coral reef offering a wide range of feeding habits, promotes increasing shape disparity of the head skeleton over the ontogeny of fishes.

Trophic Niche Width, Shift, and Specialization of Dascyllus aruanus in Toliara Lagoon, Madagascar

Abstract Intrapopulation diet specializations may result from the use of different dietary items or foraging tactics by individuals within a single population. The damselfish, Dascyllus aruanus, is a highly site-attached coral reef fish living in size hierarchies among branched corals. The trophic niche width and feeding specialization of this species were explored using stable isotopes and stomach content analyses. Intra-group niche variation was mainly related to fish size. Within social groups, D. aruanus gradually shifted its foraging tactics according to size; smaller fish fed on benthic prey such as isopods and copepods, and the larger fish foraged in the water column on planktonic copepods and larger-sized prey. Group density was found to explain some variation in trophic niche characteristics; greater specialization on prey size was observed in the colony having the highest density. All members of the largest colony foraged more frequently in the water column. Knowing that planktonic copepods are more energy-rich than benthic ones, a positive group-size effect facilitating access to preferred prey is suggested. Group size and group density effects on trophic specialization did not have any impact on body condition, suggesting that the behavioral plasticity of D. aruanus in its foraging strategies permits compensation for the maintenance of body conditions.

Mismatch between shape changes and ecological shifts during the post-settlement growth of the surgeonfish, Acanthurus triostegus

BackgroundMany coral reef fishes undergo habitat and diet shifts during ontogeny. However, studies focusing on the physiological and morphological adaptations that may prepare them for these transitions are relatively scarce. Here, we explored the body shape variation related to ontogenetic shifts in the ecology of the surgeonfish Acanthurus triostegus (Acanthuridae) from new settler to adult stages at Moorea Island (French Polynesia). Specifically, we tested the relationship between diet and habitat shifts and changes in overall body shape during the ontogeny of A. triostegus using a combination of geometric morphometric methods, stomach contents and stable isotope analysis.ResultsAfter reef settlement, stable isotope composition of carbon and nitrogen revealed a change from a zooplanktivorous to a benthic algae diet. The large amount of algae (> 75% of stomach contents) found in the digestive tract of small juveniles (25–30 mm SL) suggested the diet shift is rapid. The post-settlement growth of A. triostegus is highly allometric. The allometric shape changes mainly concern cephalic and pectoral regions. The head becomes shorter and more ventrally oriented during growth. Morphological changes are directly related to the diet shift given that a small mouth ventrally oriented is particularly suited for grazing activities at the adult stage. The pectoral fin is more anteriorely and vertically positioned and its basis is larger in adults than in juveniles. This shape variation had implications for swimming performance, manoeuvrability, turning ability and is related to habitat shift. Acanthurus triostegus achieves its main transformation of body shape to an adult-like form at size of 35–40 mm SL.ConclusionMost of the shape changes occurred after the reef colonization but before the transition between juvenile habitat (fringing reef) and adult habitat (barrier reef). A large amount of allometric variation was observed after diet shift from zooplankton to benthic algae. Diet shift could act as an environmental factor favouring or inducing morphological changes. On the other hand, the main shape changes have to be achieved before the recruitment to adult populations and start negotiating the biophysical challenges of locomotion and feeding in wave- and current-swept outer reef habitat.

Trait decoupling promotes evolutionary diversification of the trophic and acoustic system of damselfishes

Trait decoupling, wherein evolutionary release of constraints permits specialization of formerly integrated structures, represents a major conceptual framework for interpreting patterns of organismal diversity. However, few empirical tests of this hypothesis exist. A central prediction, that the tempo of morphological evolution and ecological diversification should increase following decoupling events, remains inadequately tested. In damselfishes (Pomacentridae), a ceratomandibular ligament links the hyoid bar and lower jaws, coupling two main morphofunctional units directly involved in both feeding and sound production. Here, we test the decoupling hypothesis by examining the evolutionary consequences of the loss of the ceratomandibular ligament in multiple damselfish lineages. As predicted, we find that rates of morphological evolution of trophic structures increased following the loss of the ligament. However, this increase in evolutionary rate is not associated with an increase in trophic breadth, but rather with morphofunctional specialization for the capture of zooplanktonic prey. Lineages lacking the ceratomandibular ligament also shows different acoustic signals (i.e. higher variation of pulse periods) from others, resulting in an increase of the acoustic diversity across the family. Our results support the idea that trait decoupling can increase morphological and behavioural diversity through increased specialization rather than the generation of novel ecotypes.

Diversification of the pectoral fin shape in damselfishes (Perciformes, Pomacentridae) of the Eastern Pacific

Fin shape strongly influences performance of locomotion across all swimming styles. In this study, we focused on the diversity of the pectoral fin morphology in damselfishes of the Eastern Pacific. Underwater observations and a review of literature allowed the characterization of ten behavioral groups. Territorial and non-territorial species were discriminated easily with traditional morphometrics. Five ecomorphological groups were recognized by geometric morphometric analyses. Geometric data segregated the outgroup from the damselfishes and allowed the distinction of mean morphologies from extreme ones within territorial and non-territorial species. Additionally, geometric morphometric data split Abudefduf into two groups: (1) A. troschelii is similar to C. atrilobata and (2) A. concolor and A. declivifrons are close to Stegastes. Solitary territorial species (e.g., Stegastes) show rounded and high fins whereas non-territorial species living in groups (e.g., Chromis) present long and curved pectoral fins. In the range of morphological variation, the morphologies of Microspathodon (elongate with highly curved hydrodynamic trailing edge) and Azurina (long, slender and angular) represent the extreme morphologies within territorial and non-territorial species, respectively. Our study revealed a strong relationship between the pectoral fin shape and the behavioral diversification in damselfishes.

Further insight into the sound-producing mechanism of clownfishes: what structure is involved in sound radiation?

SUMMARY It was recently demonstrated that clownfishes produce aggressive sounds by snapping their jaw teeth. To date, only the onset of the sound has been studied, which raises the question, what structure is involved in sound radiation? Here, a combination of different approaches has been used to determine the anatomical structure(s) responsible for the size-related variations observed in sound duration and frequency. Filling the swimbladder with physiological liquid specifically modified size-related acoustic features by inducing a significant decrease in pulse duration of approximately 3 ms and a significant increase in dominant frequency of approximately 105 Hz. However, testing the acoustics of the swimbladder by striking it with a piezoelectric impact hammer showed that this structure is a highly damped sound source prevented from prolonged vibrations. In contrast, the resonant properties of the rib cage seems to account for the size-related variations observed in acoustic features. For an equivalent strike on the rib cage, the duration and dominant frequency of induced sounds changed with fish size: sound duration and dominant frequency were positively and negatively correlated with fish size, respectively. Such relationships between sonic features and fish size are consistent with those observed in natural sounds emitted by fish. Therefore, the swimbladder itself does not act as a resonator; its wall just seems to be driven by the oscillations of the rib cage. This set of observations suggests the need for reassessment of the acoustic role of swimbladders in various fish species.

Triclosan exposure results in alterations of thyroid hormone status and retarded early development and metamorphosis in Cyprinodon variegatus

Thyroid hormones are critically involved in somatic growth, development and metamorphosis of vertebrates. The structural similarity between thyroid hormones and triclosan, an antimicrobial compound widely employed in consumer personal care products, suggests triclosan can have adverse effects on the thyroid system. The sheepshead minnow, Cyprinodon variegatus, is now used in ecotoxicological studies that have recently begun to focus on potential disruption of the thyroid axis by endocrine disrupting compounds. Here, we investigate the in vivo effects of exposure to triclosan (20, 50, and 100μgL-1) on the thyroid system and the embryonic and larval development of C. variegatus. Triclosan exposure did not affect hatching success, but delayed hatching time by 6-13h compared to control embryos. Triclosan exposure affected the ontogenetic variations of whole body thyroid hormone concentrations during the larval phase. The T3 peak around 12-15 dph, described to be indicative for the metamorphosis climax in C. variegatus, was absent in triclosan-exposed larvae. Triclosan exposure did not produce any deformity or allometric repatterning, but a delayed development of 18-32h was observed. We conclude that the triclosan-induced disruption of the thyroid system delays in vivo the start of metamorphosis in our experimental model. We observed a global developmental delay of 24-45h, equivalent to 4-7% prolongation of the developmental time in C. variegatus. The costs of delayed metamorphosis can lead to reduction of juvenile fitness and could be a determining factor in the outcome of competitive interactions.