Specialization in habitat use by coral reef damselfishes and their susceptibility to habitat loss

While it is generally assumed that specialist species are more vulnerable to disturbance compared with generalist counterparts, this has rarely been tested in coastal marine ecosystems, which are increasingly subject to a wide range of natural and anthropogenic disturbances. Habitat specialists are expected to be more vulnerable to habitat loss because habitat availability exerts a greater limitation on population size, but it is also possible that specialist species may escape effects of disturbance if they use habitats that are generally resilient to disturbance. This study quantified specificity in use of different coral species by six coral‐dwelling damselfishes (Chromis viridis, C. atripectoralis, Dascyllus aruanus, D. reticulatus, Pomacentrus moluccensis, and P. amboinensis) and related habitat specialization to proportional declines in their abundance following habitat degradation caused by outbreaks of the coral eating starfish, Acanthaster planci. The coral species preferred by most coral‐dwelling damselfishes (e.g., Pocillopora damicornis) were frequently consumed by coral eating crown‐of‐thorns starfish, such that highly specialized damselfishes were disproportionately affected by coral depletion, despite using a narrower range of different coral species. Vulnerability of damselfishes to this disturbance was strongly correlated with both their reliance on corals and their degree of habitat specialization. Ongoing disturbances to coral reef ecosystems are expected, therefore, to lead to fundamental shifts in the community structure of fish communities where generalists are favored over highly specialist species.     

From embryos to juveniles: morphogenesis in the spionid Boccardia proboscidea (Polychaeta)

Abstract. The polychaete Boccardia proboscidea has poecilogonous development that includes the production of both planktotrophic and adelphophagic young. In this study, we use scanning electron microscopy to analyse external morphogenesis of planktotrophic offspring with emphasis on early embryos, morphogenesis during metamorphosis, and the dynamic nature of larval structures during early ontogeny. Larval growth involves addition of terminal chaetigers and formation of segment-specific structures such as cilia and chaetae. Our observations reveal that most ciliary bands are reduced or incomplete relative to those found in larvae of other polychaete families. We describe a small metatroch (consisting of only a few trochoblasts) in early embryos, which has not previously been reported in the Spionidae. The presence of the metatroch does not imply a function in opposed-band feeding, as a food groove intermediate between the prototroch and metatroch is lacking. A neurotroch, inconsistently reported in the Spionidae, is also present and terminates in a ciliated pit. Many larval structures (e.g., presumptive sensory organs) are short-lived, implying a shift towards early functionality of adult traits in larvae. Metamorphosis is gradual and occurs over the latter half of the larval life. The reduction of larval structures, and early development of adult traits, suggests an overall shift in morphology facilitating settlement and juvenile development.     

Potential for adaptation to climate change in a coral reef fish

Predicting the impacts of climate change requires knowledge of the potential to adapt to rising temperatures, which is unknown for most species. Adaptive potential may be especially important in tropical species that have narrow thermal ranges and live close to their thermal optimum. We used the animal model to estimate heritability, genotype by environment interactions and nongenetic maternal components of phenotypic variation in fitness‐related traits in the coral reef damselfish, Acanthochromis polyacanthus. Offspring of wild‐caught breeding pairs were reared for two generations at current‐day and two elevated temperature treatments (+1.5 and +3.0 °C) consistent with climate change projections. Length, weight, body condition and metabolic traits (resting and maximum metabolic rate and net aerobic scope) were measured at four stages of juvenile development. Additive genetic variation was low for length and weight at 0 and 15 days posthatching (dph), but increased significantly at 30 dph. By contrast, nongenetic maternal effects on length, weight and body condition were high at 0 and 15 dph and became weaker at 30 dph. Metabolic traits, including net aerobic scope, exhibited high heritability at 90 dph. Furthermore, significant genotype x environment interactions indicated potential for adaptation of maximum metabolic rate and net aerobic scope at higher temperatures. Net aerobic scope was negatively correlated with weight, indicating that any adaptation of metabolic traits at higher temperatures could be accompanied by a reduction in body size. Finally, estimated breeding values for metabolic traits in F2 offspring were significantly affected by the parental rearing environment. Breeding values at higher temperatures were highest for transgenerationally acclimated fish, suggesting a possible role for epigenetic mechanisms in adaptive responses of metabolic traits. These results indicate a high potential for adaptation of aerobic scope to higher temperatures, which could enable reef fish populations to maintain their performance as ocean temperatures rise.     

Agriculture shapes the trophic niche of a bat preying on multiple pest arthropods across Europe: Evidence from DNA metabarcoding

The interaction between agricultural production and wildlife can shape, and even condition, the functioning of both systems. In this study, we i) explored the degree to which a widespread European bat, namely the common bent‐wing bat Miniopterus schreibersii, consumes crop‐damaging insects at a continental scale, and ii) tested whether its dietary niche is shaped by the extension and type of agricultural fields. We employed a dual‐primer DNA metabarcoding approach to characterize arthropod 16S and COI DNA sequences within bat faecal pellets collected across 16 Southern European localities, to first characterize the bat species’ dietary niche, second measure the incidence of agricultural pests across their ranges and third assess whether geographical dietary variation responds to climatic, landscape diversity, agriculture type and vegetation productivity factors. We detected 12 arthropod orders, among which lepidopterans were predominant. We identified >200 species, 44 of which are known to cause agricultural damage. Pest species were detected at all but one sampling site and in 94% of the analysed samples. Furthermore, the dietary diversity of M. schreibersii exhibited a negative linear relation with the area of intensive agricultural fields, thus suggesting crops restrict the dietary niche of bats to prey taxa associated with agricultural production within their foraging range. Overall, our results imply that M. schreibersii might be a valuable asset for biological pest suppression in a variety of agricultural productions and highlight the dynamic interplay between wildlife and agricultural systems.     

Evolution of a complex phenotype with biphasic ontogeny: Contribution of development versus function and climatic variation to skull modularity in toads

The theory of morphological integration and modularity predicts that if functional correlations among traits are relevant to mean population fitness, the genetic basis of development will be molded by stabilizing selection to match functional patterns. Yet, how much functional interactions actually shape the fitness landscape is still an open question. We used the anuran skull as a model of a complex phenotype for which we can separate developmental and functional modularity. We hypothesized that functional modularity associated to functional demands of the adult skull would overcome developmental modularity associated to bone origin at the larval phase because metamorphosis would erase the developmental signal. We tested this hypothesis in toad species of the Rhinella granulosa complex using species phenotypic correlation pattern (P‐matrices). Given that the toad species are distributed in very distinct habitats and the skull has important functions related to climatic conditions, we also hypothesized that differences in skull trait covariance pattern are associated to differences in climatic variables among species. Functional and hormonal‐regulated modules are more conspicuous than developmental modules only when size variation is retained on species P‐matrices. Without size variation, there is a clear modularity signal of developmental units, but most species have the functional model as the best supported by empirical data without allometric size variation. Closely related toad species have more similar climatic niches and P‐matrices than distantly related species, suggesting phylogenetic niche conservatism. We infer that the modularity signal due to embryonic origin of bones, which happens early in ontogeny, is blurred by the process of growth that occurs later in ontogeny. We suggest that the species differing in the preferred modularity model have different demands on the orbital functional unit and that species contrasting in climate are subjected to divergent patterns of natural selection associated to neurocranial allometry and T3 hormone regulation.     

Transition from larva to pupa: morphogenesis,cell proliferation and protein synthesis in Bombyx wing disc

Summary

In the present study, an attempt was made to clarify the timing of the transition from proliferation stage to pupal preparation stage of Bombyx wing discs and the correlation of its timing and ecdysteroid release. An histological study was carried out during the period of ecdysteroid increase in hemolymph in the last larval instar. The number of mitoses in wing discs from the feeding stage to the spinning stage was counted. During the feeding stage, the number of mitoses was about 200/disc, with the number increasing up to about 850/disc on the day of the beginning of spinning (S0); it then decreased to about 250/disc at the S1 stage, and finally mitotic figures were absent at S2. Comparing the mitotic number with hemolymph ecdysteroid titer, ecdysteroid during the high mitotic period is close to 100ng/ml, while ecdysteroid during the low mitotic period is about 10ng/ml at day 5 and 500ng/ml at S1, respectively. Two-dimensional gel electrophoresis was carried out to identify the ecdysone-induced polypeptides or the polypeptides synthesized during the spinning stage. Five ecdysteroid-inducible polypeptides were observed during the spinning stage or after 20-hydroxyecdysone (20E) treatment. From these findings, low concentrations of ecdysteroid induce cell proliferation, whereas high concentrations inhibit cell proliferation and induce new protein synthesis.     

Catastrophic regime shifts in coral communities exposed to physical disturbances: Simulation results from object-oriented 3-dimensional coral reef model

A 3-dimensional individual-based model, the ReefModel, was developed to simulate the dynamical structure of coral reef community using object-oriented techniques. Interactions among functional groups of reef organisms were simulated in the model. The behaviours of these organisms were described with simple mechanistic rules that were derived from their general behaviours (e.g. growing habits, competitive mechanisms, response to physical disturbance) observed in natural coral reef communities. The model was implemented to explore the effects of physical disturbance on the dynamical structure of a 3-coral community that was characterized with three functional coral groups: tabular coral, foliaceous coral and massive coral. Simulation results suggest that (i) the integration of physical disturbance and differential responses (disturbance sensitivity and growing habit) of corals plays an important role in structuring coral communities; (ii) diversity of coral communities can be maximal under intermediate level of acute physical disturbance; (iii) multimodality exists in the final states and dynamic regimes of individual coral group as well as coral community structure, which results from the influence of small random spatial events occurring during the interactions among the corals in the community, under acute and repeated physical disturbances. These results suggest that alternative stable states and catastrophic regime shifts may exist in a coral community under unstable physical environment.     

Habitat use and its implications to functional morphology: niche partitioning and the evolution of locomotory morphology in Lake Tanganyikan cichlids (Perciformes: Cichlidae)

Animal locomotory morphology, i.e. morphological features involved in locomotion, is under the influence of a diverse set of ecological and behavioral factors. In teleost fish, habitat choice and foraging strategy are major determinants of locomotory morphology. In this study, we assess the influence of habitat use and foraging strategy on important locomotory traits, namely the size of the pectoral and caudal fins and the weight of the pectoral fin muscles, as applied to one of the most astonishing cases of adaptive radiation: the species flock of cichlid fishes in East African Lake Tanganyika. We also examine the course of niche partitioning along two main habitat axes, the benthic vs. limnetic and the sandy vs. rocky substrate axis. The results are then compared with available data on the cichlid adaptive radiation of neighbouring Lake Malawi. We find that pectoral fin size and muscle weight correlate with habitat use within the water column, as well as with substrate composition and foraging strategies. Niche partitioning along the benthic–limnetic axis in Lake Tanganyikan cichlids seems to follow a similar course as in Lake Malawi, while the course of habitat use with respect to substrate composition appears to differ between the cichlid assemblages of these two lakes.     

Returns from matching management resolution to ecological variation in a coral reef fishery

When managing heterogeneous socioecological systems, decision-makers must choose a spatial resolution at which to define management policies. Complex spatial policies allow managers to better reflect underlying ecological and economic heterogeneity, but incur higher compliance and enforcement costs. To choose the most appropriate management resolution, we need to characterize the relationship between management resolution and performance. We parameterize a model of the commercial coral trout fishery in the Great Barrier Reef, Australia, which is currently managed by a single, spatially homogeneous management policy. We use this model to estimate how the spatial resolution of management policies affect the amount of revenue generated, and assess whether a more spatially complex policy can be justified. Our results suggest that economic variation is likely to be a more important source of heterogeneity than ecological differences, and that the majority of this variation can be captured by a relatively simple spatial management policy. Moreover, while an increase in policy resolution can improve performance, the location of policy changes also needs to align with ecological and socioeconomic variation. Interestingly, the highly complex process of larval dispersal, which plays a critical ecological role in coral reef ecosystem dynamics, may not demand equally complex management policies.     

Patch reef development in the florigemma-Bank Member (Oxfordian) from the Deister Mts (NW Germany): a type example for Late Jurassic coral thrombolite thickets

Small reefal bioconstructions that developed in lagoonal settings are widespread in a few horizons of the Late Jurassic (Oxfordian) succession of the Korallenoolith Formation, exposed southwest of Hannover, Northwest Germany. Especially the florigemma-Bank Member, “sandwiched” between oolite shoal deposits, exposes a high variety of build-ups, ranging from coral thrombolite patch reefs, to biostromes and to coral meadows. The reefs show a distribution with gradual facies variations along an outcrop belt that extends about 30 km from the Wesergebirge in the NW to the Osterwald Mts in the SE.The patch reefs from the Deister Mts locality at the “Speckhals” are developed as coral-chaetetid-solenoporid-microbialite reefs and represent a reef type that was hitherto unknown so far north of its Tethyan counterparts. They are mainly built up by coral thickets that are preserved in situ up to 1.5 m in height and a few metres in diameter. They contain up to 20 coral species of different morphotypes but are chiefly composed of phaceloid Stylosmilia corallina and Goniocora socialis subordinately. The tightly branched Stylosmilia colonies are stabilized by their anastomosing growth. The coral branches are coated with microbial crusts and micro-encrusters reinforcing the coral framework. Encrusters and other biota within the thicket show a typical community replacement sequence: Lithocodium aggregatum, Koskinobullina socialis and Iberopora bodeuri are pioneer organisms, whereas the occurrence of non-rigid sponges represents the terminal growth stage. The latter are preserved in situ and seem to be characteristic so far poorly known constituents of the Late Jurassic cryptobiont reef dweller community. The distance and overall arrangement of branches seems to be the crucial factor for the manifestation of a (cryptic) habitat promoting such community replacement sequences. Widely spaced branches often lack any encrusting and/or other reef dwelling organisms, whereas tightly branched corals, as is St. corallina, stimulate such biota. Hence, such reefs are well suited for research on coelobites and community sequences of encrusting and cavity dwelling organisms.     

Complex migration and the development of genetic structure in subdivided populations: an example from Caribbean coral reef ecosystems

A matrix‐based projection model is used in conjunction with the results of a coupled bio‐physical dispersal model to examine the spread of alleles through subdivided populations over time, and the associated development of genetic structural patterns. Applying this approach, it becomes possible to quantitatively evaluate the contribution of spatially explicit migration towards patterns of genetic structure observed in the field. To provide a concrete example, the model was used to examine genetic dispersal between coral reef patches of the Caribbean. Using generic life‐history parameters, the model shows the formation of a strong genetic break between eastern and western patches, as well as the development of a gradient along the length of the Bahamian archipelago, corresponding with evidence previously collected for coral and fish species. The data also suggest that Jamaica and the Cayman Islands are important stepping stones between the reefs of the northern Caribbean (Hispaniola and the Bahamas) and the Mesoamerican Barrier Reef. The model provides an effective means of evaluating regional‐scale genetic connectivity through time and identifying natural clusters of genetic exchange.     

Depth-dependant response to light of the reef building coral, Pocillopora verrucosa: Implication of oxidative stress

Several environmental factors have been described to trigger bleaching in cnidarian/dinoflagellate endosymbiosis. However, the molecular mechanisms underlying this process still need more investigations. Symbiosis breakdown is known to result from physiological damage to animal host cells and/or symbionts. Cellular oxidation appears to be an essential player in this damage. Indeed, oxidative stress is a direct consequence of increase in irradiance and temperature, the two main environmental factors involved in bleaching. In this study, we examined the role of irradiance in inducing dissociation and oxidative stress in cnidarians and dinoflagellates. We used the bleaching-sensitive scleractinian coral Pocillopora verrucosa in a field cross-transplantation experiment performed between 5 m and 20 m depth at Grande Glorieuse Island (Indian Ocean), a preserved area subject to minimal anthropogenic influence. Cellular damage and increase in antioxidant defense were correlated with bleaching in upward transplanted samples. Downward transplanted colonies presented no associated alterations similar to the controls. We therefore conclude that increasing light induced bleaching via a prooxidative period. Remarkably, the distribution of Symbiodinium over depth was invariant; all colonies were monomorph for clade C, suggesting that bleaching sensitivity of P. verrucosa might not be associated with clade specificity.     

To feed or to breed: morphological constraints of mouthbrooding in coral reef cardinalfishes

Functionally coupled biomechanical systems are widespread in nature and are viewed as major constraints on evolutionary diversification, yet there have been few attempts to explore the implications of performing multiple functions within a single anatomical structure. Paternally mouthbrooding cardinalfishes present an ideal system to investigate the constraints of functional coupling as the oral jaws of male fishes are directly responsible for both feeding and reproductive functions. To test the effects of (i) mouthbrooding on feeding and (ii) feeding on reproductive potential we compared the feeding apparatus between sexes of nine species of cardinalfish and compared brood characteristics among species from different trophic groups, respectively. Mouthbrooding was strongly associated with the morphology of the feeding apparatus in males. Male cardinalfishes possessed longer heads, snouts and jaws than female conspecifics irrespective of body size, trophic group or evolutionary history. Conversely, reproductive potential also appeared to be related to trophic morphology. Piscivorous cardinalfishes produced larger, but fewer eggs, and had smaller brood volumes than species from the two invertebrate feeding groups. These interrelationships suggest that feeding and reproduction in the mouth of cardinalfishes may be tightly coupled. If so this may, in part, have contributed to the limited morphological diversification exhibited by cardinalfishes.     

Left-right axis development: examples of similar and divergent strategies to generate asymmetric morphogenesis in chick and mouse embryos

Left-right asymmetry of internal organs is widely distributed in the animal kingdom. The chick and mouse embryos have served as important model organisms to analyze the mechanisms underlying the establishment of the left-right axis. In the chick embryo many genes have been found to be asymmetrically expressed in and around the node, while the same genes in the mouse show symmetric expression patterns. In the mouse there is strong evidence for an establishment of left-right asymmetry through nodal cilia. In contrast, in the chick and in many other organisms left-right asymmetry is probably generated by an early-acting event involving membrane depolarization. In both birds and mammals a conserved Nodal-Lefty-Pitx2 module exists that controls many aspects of asymmetric morphogenesis. This review also gives examples of divergent mechanisms of establishing asymmetric organ formation. Thus there is ample evidence for conserved and non-conserved strategies to generate asymmetry in birds and mammals.     

The phylogenetic affinities of Crossley's babbler (Mystacornis crossleyi): adding a new niche to the vanga radiation of Madagascar

Crossley's babbler (Mystacornis crossleyi) is a passerine endemic to Madagascar. Traditionally, it has been classified as a babbler (Timaliidae), although affinities with warblers and vangas have been suggested. We investigated the phylogenetic affinities of Crossley's babbler using sequence data from two nuclear introns (myoglobin intron 2 and beta-fibrinogen intron 5) and one mitochondrial gene (ND2). We present for the first time (to our knowledge) a molecular phylogeny that confidently places this enigmatic species within the vangas (Vangidae). The inclusion of Crossley's babbler within the vangas adds another foraging niche--gleaning small invertebrates from the ground-to this already large adaptive radiation of songbirds.     

Thinking and managing outside the box: coalescing connectivity networks to build region-wide resilience in coral reef ecosystems

As the science of connectivity evolves, so too must the management of coral reefs. It is now clear that the spatial scale of disturbances to coral reef ecosystems is larger and the scale of larval connectivity is smaller than previously thought. This poses a challenge to the current focus of coral reef management, which often centers on the establishment of no-take reserves (NTRs) that in practice are often too small, scattered, or have low stakeholder compliance. Fished species are generally larger and more abundant in protected reserves, where their reproductive potential is often greater, yet documented demographic benefits of these reproductive gains outside reserves are modest at best. Small reproductive populations and limited dispersal of larvae play a role, as does the diminished receptivity to settling larvae of degraded habitats that can limit recruitment by more than 50%. For “demographic connectivity” to contribute to the resilience of coral reefs, it must function beyond the box of no-take reserves. Specifically, it must improve nursery habitats on or near reefs and enhance the reproductive output of ecologically important species throughout coral reef ecosystems. Special protection of ecologically important species (e.g., some herbivores in the Caribbean) and size-regulated fisheries that capitalize on the benefits of NTRs and maintain critical ecological functions are examples of measures that coalesce marine reserve effects and improve the resilience of coral reef ecosystems. Important too is the necessity of local involvement in the management process so that social costs and benefits are properly assessed, compliance increased and success stories accrued.     

Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs

Design and decision-making for marine protected areas (MPAs) on coral reefs require prediction of MPA effects with population models. Modeling of MPAs has shown how the persistence of metapopulations in systems of MPAs depends on the size and spacing of MPAs, and levels of fishing outside the MPAs. However, the pattern of demographic connectivity produced by larval dispersal is a key uncertainty in those modeling studies. The information required to assess population persistence is a dispersal matrix containing the fraction of larvae traveling to each location from each location, not just the current number of larvae exchanged among locations. Recent metapopulation modeling research with hypothetical dispersal matrices has shown how the spatial scale of dispersal, degree of advection versus diffusion, total larval output, and temporal and spatial variability in dispersal influence population persistence. Recent empirical studies using population genetics, parentage analysis, and geochemical and artificial marks in calcified structures have improved the understanding of dispersal. However, many such studies report current self-recruitment (locally produced settlement/settlement from elsewhere), which is not as directly useful as local retention (locally produced settlement/total locally released), which is a component of the dispersal matrix. Modeling of biophysical circulation with larval particle tracking can provide the required elements of dispersal matrices and assess their sensitivity to flows and larval behavior, but it requires more assumptions than direct empirical methods. To make rapid progress in understanding the scales and patterns of connectivity, greater communication between empiricists and population modelers will be needed. Empiricists need to focus more on identifying the characteristics of the dispersal matrix, while population modelers need to track and assimilate evolving empirical results.