Experimental evaluation of diversity–productivity relationships in a coral reef fish assemblage

The global decline in biodiversity is causing increasing concern about the effects of biodiversity loss on ecosystem services such as productivity. Biodiversity has been hypothesised to be important in maintaining productivity of biological assemblages because niche complementarity and facilitation among the constituent species can result in more efficient use of resources. However, these conclusions are primarily based on studies with plant communities, and the relationship between diversity and productivity at higher trophic levels is largely unknown, especially in the marine environment. Here, we used a manipulative field experiment to test the effects of species richness and species identity on biomass accumulation in coral reef fish assemblages at Lizard Island. Small patch reefs were stocked with a total of 30 juveniles belonging to three planktivorous damselfish (genus Pomacentrus) according to three different levels of fish species richness (one, two and three species) and seven different combinations of fish species. Species richness had no effect on the relative growth in this assemblage after 18 days, but relative growth differed among individual fish species and the different combinations of species. Patterns of increase in biomass were best explained by species-specific differences and variable effects of intra- and interspecific competition on growth. These results suggest that niche complementarity and facilitation are not the most influential drivers of total productivity within this guild of planktivorous fishes. Total productivity may be resilient to declining reef fish biodiversity, but this will depend on which species are lost and on the life-history traits of remaining species.     

Moorea BIOCODE barcode library as a tool for understanding predator–prey interactions: insights into the diet of common predatory coral reef fishes

Identifying species involved in consumer–resource interactions is one of the main limitations in the construction of food webs. DNA barcoding of prey items in predator guts provides a valuable tool for characterizing trophic interactions, but the method relies on the availability of reference sequences to which prey sequences can be matched. In this study, we demonstrate that the COI sequence library of the Moorea BIOCODE project, an ecosystem-level barcode initiative, enables the identification of a large proportion of semi-digested fish, crustacean and mollusks found in the guts of three Hawkfish and two Squirrelfish species. While most prey remains lacked diagnostic morphological characters, 94% of the prey found in 67 fishes had >98% sequence similarity with BIOCODE reference sequences. Using this species-level prey identification, we demonstrate how DNA barcoding can provide insights into resource partitioning, predator feeding behaviors and the consequences of predation on ecosystem function.     

The aftermath of coral bleaching on a Maldivian reef—a quantitative study

Since the bleaching event of 1998, the development of the reef flat and upper reef slope on a Maldivian reef (the Komandoo house reef; Komandoo Island, Lhaviyani atoll or Fadiffolu atoll) is under detailed observation. We quantitatively recorded specific losses, re-colonisation by coral larvae on transects on the reef flat and on dead Acropora tables at the reef slope and regeneration of partly damaged large Porites and Diploastrea—colonies over the period from 1999 to 2004. The detrimental effects on the reef structure by bioerosion and hydrodynamics, as well as the overall status of the reef community were qualitatively assessed. Recruitment soon after the bleaching was more pronounced than in the following years, Pavona varians being a main constituent. The temporal re-colonisation pattern points at an emergency spawning of local Scleractinia just prior to the bleaching, whereas a sharp decrease of young settlers in 2001 and 2002 confirms a reduction of fertile colonies. The dominant species in the coral community shifted from acroporids and pocilloporids to agariciids. The skeletal deposition of recovering Diploastrea heliopora was equivalent to that before the bleaching, but much less than that of neighbouring Porites lobata colonies. The slow and scattered formation of new reef substance, which would structurally strengthen the reef, is however outweighed by the collapse of dead protruding and spacious colonies (e.g., Acropora tables). Six years after the bleaching, the formerly three-dimensional structure of the reef flat and upper reef slope presents as a levelled field of rubble, only partly consolidated by incrusting corals. Considering the recurrence of bleaching events (1987, 1998) and the results of the present study, one may assume a cascading deterioration of the status of the reef for the future.     

Coexistence of coral reef fishes — a lottery for living space

Synopsis Data are summarised from studies of two reef fish communities — pomacentrids territorial on rubble patches, and fishes resident in small isolated colonies of coral. In each case there is evidence that availability of living sites limits numbers of fishes, and that similar species of fish use the same kinds of spaces. Priority of arrival as recruits, rather than subtle differences in requirements or competitive abilities of adults, appears to determine which species holds each site. Faced with a limited and patchy supply of living space, most reef fishes are sedentary as adults, and produce frequent clutches of pelagic larvae over extended breeding seasons In this way they maximise their chances of getting offspring into suitable living sites as such sites appear. It is argued that by adopting this strategy, reef fishes are preadapted for forming inter-specific lotteries for living space if several species with similar requirements occur together. Such lotteries among similar species may be a feature common to many reef fish communities, and may explain the typically high within-site diversity found in them.This paper forms part of the proceedings of a mini-symposium convened at Cornell University, Ithaca, N.Y., 18–19 May 1976, entitled Patterns of Community Structure in Fishes (G. S. Helfman, ed.).     

Determinants of the steep species–area relationship of coral reef fishes

The increase in species richness with area is known as the species–area relationship (SPAR). Although several mutually non-exclusive processes may produce the SPAR, the null, often ignored, hypothesis states that a SPAR can be generated by random placement alone. The log–log-transformed SPAR of coral reef fishes on small patch-reefs revealed a steep slope of 0.55. However, this slope was dependent on the cumulative area of the reef examined and was therefore affected by random placement. After statistically removing the contribution of random placement from the SPAR, the slope was estimated to be 0.21. This is consistent with estimates from other, mostly terrestrial, systems. Furthermore, a randomization procedure, where the probability of fishes to reach a patch was proportional to reef area, showed that the field measured SPAR did not differ from random placement. In addition, fish assemblages on species poor reefs did not form subsets of species rich reefs (i.e., no nestedness) beyond that expected from random placement. Steep log–log-transformed SPARs can be formed by random placement alone, indicating that caution should be used when assigning an ecological meaning to SPARs generated from small spatial scales.     

Alloparental care in the sea: Brood parasitism and adoption within and between two species of coral reef Altrichthys damselfish?

The evolution of parental care opens the door for the evolution of brood parasitic strategies that allow individuals to gain the benefits of parental care without paying the costs. Here we provide the first documentation for alloparental care in coral reef fish and we discuss why these patterns may reflect conspecific and interspecific brood parasitism. Species‐specific barcodes revealed the existence of low levels (3.5% of all offspring) of mixed interspecific broods, mostly juvenile Amblyglyphidodon batunai and Pomacentrus smithi damselfish in Altrichthys broods. A separate analysis of conspecific parentage based on microsatellite markers revealed that mixed parentage broods are common in both species, and the genetic patterns are consistent with two different modes of conspecific brood parasitism, although further studies are required to determine the specific mechanisms responsible for these mixed parentage broods. While many broods had offspring from multiple parasites, in many cases a given brood contained only a single foreign offspring, perhaps a consequence of the movement of lone juveniles between nests. In other cases, broods contained large numbers of putative parasitic offspring from the same parents and we propose that these are more likely to be cases where parasitic adults laid a large number of eggs in the host nest than the result of movements of large numbers of offspring from a single brood after hatching. The evidence that these genetic patterns reflect adaptive brood parasitism, as well as possible costs and benefits of parasitism to hosts and parasites, are discussed.     

Revealing the role of predator interference in a predator–prey system with disease in prey population

Predation on a species subjected to an infectious disease can affect both the infection level and the population dynamics. There is an ongoing debate about the act of managing disease in natural populations through predation. Recent theoretical and empirical evidence shows that predation on infected populations can have both positive and negative influences on disease in prey populations. Here, we present a predator–prey system where the prey population is subjected to an infectious disease to explore the impact of predator on disease dynamics. Specifically, we investigate how the interference among predators affects the dynamics and structure of the predator–prey community. We perform a detailed numerical bifurcation analysis and find an unusually large variety of complex dynamics, such as, bistability, torus and chaos, in the presence of predators. We show that, depending on the strength of interference among predators, predators enhance or control disease outbreaks and population persistence. Moreover, the presence of multistable regimes makes the system very sensitive to perturbations and facilitates a number of regime shifts. Since, the habitat structure and the choice of predators deeply influence the interference among predators, thus before applying predators to control disease in prey populations or applying predator control strategy for wildlife management, it is essential to carefully investigate how these predators interact with each other in that specific habitat; otherwise it may lead to ecological disaster.     

The role of noise in a predator–prey model with Allee effect

The existence and implications of alternative stable states in ecological systems have been investigated extensively within deterministic models. However, it is known that natural systems are undeniably subject to random fluctuations, arising from either environmental variability or internal effects. Thus, in this paper, we study the role of noise on the pattern formation of a spatial predator–prey model with Allee effect. The obtained results show that the spatially extended system exhibits rich dynamic behavior. More specifically, the stationary pattern can be induced to be a stable target wave when the noise intensity is small. As the noise intensity is increased, patchy invasion emerges. These results indicate that the dynamic behavior of predator–prey models may be partly due to stochastic factors instead of deterministic factors, which may also help us to understand the effects arising from the undeniable susceptibility to random fluctuations of real ecosystems.     

Reconstruction of coral reef fisheries catches in American Samoa, 1950–2002

Fisheries catches from Pacific Island coral reefs are rarely recorded in official statistics. Reconstruction of catch estimates with limited hard data requires interpolation and assumptions, justifiable only by the unsatisfactory alternative of continued substitution of zero catches, a common policy interpretation for ‘no data’. Uncertainties associated with reconstructions are high, requiring conservative estimation. American Samoan domestic fisheries consist of an artisanal, small-boat sector, whose commercial catches are reported, and a shore-based subsistence sector, with no regular reporting. Our catch reconstruction (with large pelagic species removed) suggested a 79% decrease in catches between 1950 (752 t) and 2002 (155 t). Accounting for rapid human population growth on the main island, the per capita catch rate may have declined from 36.3 kg·person⁻¹ year⁻¹ in 1950 to 1.3 kg·person⁻¹ year⁻¹ by 2002, while the catch rate for the inhabited outer islands has been independently reported as 58.6 kg·person⁻¹ year⁻¹. Catch per area of coral reef (to 50-m depth) may have declined from 5.5 to 0.7 t km⁻² year⁻¹ for the main island, and from 9.1 to 4.9 t km⁻² year⁻¹ for the outer islands, for 1950 and 2002, respectively. Summed for 1950–2002, our reconstruction suggested a 17-fold difference between reconstructed estimates and reported statistics.     

Background level of risk and the survival of predator-naive prey: can neophobia compensate for predator naivety in juvenile coral reef fishes?

Neophobia—the generalized fear response to novel stimuli—provides the first potential strategy that predator-naive prey may use to survive initial predator encounters. This phenotype appears to be highly plastic and present in individuals experiencing high-risk environments, but rarer in those experiencing low-risk environments. Despite the appeal of this strategy as a ‘solution’ for prey naivety, we lack evidence that this strategy provides any fitness benefit to prey. Here, we compare the relative effect of environmental risk (high versus low) and predator-recognition training (predator-naive versus predator-experienced individuals) on the survival of juvenile fish in the wild. We found that juveniles raised in high-risk conditions survived better than those raised in low-risk conditions, providing the first empirical evidence that environmental risk, in the absence of any predator-specific information, affects the way naive prey survive in a novel environment. Both risk level and experience affected survival; however, the two factors did not interact, indicating that the information provided by both factors did not interfere or enhance each other. From a mechanistic viewpoint, this indicates that the combination of the two factors may increase the intensity, and hence efficacy, of prey evasion strategies, or that both factors provide qualitatively separate benefits that would result in an additive survival success.     

Structural sensitivity and resilience in a predator–prey model with density-dependent mortality

Numerous formulations with the same mathematical properties can be relevant to model a biological process. Different formulations can predict different model dynamics like equilibrium vs. oscillations even if they are quantitatively close (structural sensitivity). The question we address in this paper is: does the choice of a formulation affect predictions on the number of stable states? We focus on a predator–prey model with predator competition that exhibits multiple stable states. A bifurcation analysis is realized with respect to prey carrying capacity and species body mass ratio within range of values found in food web models. Bifurcation diagrams built for two type-II functional responses are different in two ways. First, the kind of stable state (equilibrium vs. oscillations) is different for 26.0–49.4% of the parameter values, depending on the parameter space investigated. Using generalized modelling, we highlight the role of functional response slope in this difference. Secondly, the number of stable states is higher with Ivlev's functional response for 0.1–14.3% of the parameter values. These two changes interact to create different model predictions if a parameter value or a state variable is altered. In these two examples of disturbance, Holling's disc equation predicts a higher system resilience. Indeed, Ivlev's functional response predicts that disturbance may trap the system into an alternative stable state that can be escaped from only by a larger alteration (hysteresis phenomena). Two questions arise from this work: (i) how much complex ecological models can be affected by this sensitivity to model formulation? and (ii) how to deal with these uncertainties in model predictions?     

Global analysis of a predator–prey model with variable predator search rate

We consider a modified Holling-type II predator–prey model, based on the premise that the search rate of predators is dependent on the prey density, rather than constant. A complete analysis of the global behavior of the model is presented, and shows that the model exhibits a dichotomy similar to the classical Holling-type II model: either the coexistence steady state is globally stable; or it is unstable, and then a unique, globally stable limit cycle exists. We discuss the similarities, but also important differences between our model and the Holling-type II model. The main differences are that: 1. The paradox of enrichment which always occurs in the Holling-type II model, does not always occur here, and 2. Even when the paradox of enrichment occurs, predators can adapt by lowering their search rate, and effectively stabilize the system.

     

Feeding by coral reef mesograzers: algae or cyanobacteria?

Marine studies on herbivory have addressed the role of algae as food and shelter for small consumers, but the potential of benthic cyanobacteria to play similar roles is largely unknown. Here, feeding preferences were measured for eight invertebrate consumers from Guam, offered four common macroalgae and two cyanobacteria. The survivorship of another consumer raised on either macroalgae or cyanobacteria was also assessed. From the choices offered, the sacoglossans Elysia rufescens and E. ornata consumed the green macroalga Bryopsis pennata. The crab Menaethius monoceros preferred the red alga Acanthophora spicifera. The amphipods Parhyale hawaiensis and Cymadusa imbroglio consumed macroalgae and cyanobacteria in equivalent amounts, with C. imbroglio showing less selectivity among diets. In contrast to these patterns, in these assays the gastropods Stylocheilus striatus, Haminoea cymbalum, H. ovalis, and Haminoea sp. fed exclusively, or survived only, on cyanobacteria. Preferences for different cyanobacteria varied. Field surveys of cyanobacteria-associated species yielded 34 different invertebrate taxa and suggested different degrees of specificity in these associations. Tropical mesograzers exploit considerably different food resources, with some species adapted to consume cyanobacterial mats. Benthic cyanobacteria may play important roles as food and shelter for marine consumers and may indirectly influence local biodiversity through their associated fauna.     

Effects of the probability of a predator catching prey on predator–prey system stability

To understand the effect of the probability of a predator catching prey, P_catch, on the stability of the predator–prey system, a spatially explicit lattice model consisting of predators, prey, and grass was constructed. The predators and prey randomly move on the lattice space, and the grass grows according to its growth probability. When a predator encounters prey, the predator eats the prey in accordance with the probability P_catch. When a prey encounters grass, the prey eats the grass. The predator and prey give birth to offspring according to a birth probability after eating prey or grass, respectively. When a predator or prey is initially introduced or newly born, its health state is set at a high given value. This health state decreases by one with every time step. When the state of an animal decreases to less than zero, the individual dies and is removed from the system. Population densities for predator and prey fluctuated significantly according to P_catch. System stability was characterized by the standard deviation ? of the fluctuation. The simulation results showed that ? for predators increased with an increase of P_catch; ? for prey reached a maximum at P_catch = 0.4; and ? for grass fluctuated little regardless of P_catch. These results were due to the tradeoff between P_catch and the predator–prey encounter rate, which represents the degree of interaction between predator and prey and the average population density, respectively.     

Length–weight relationships to quantify biomass for motile coral reef cryptofauna

Coral Reefs - Length–weight relationships (LWRs) are a fundamental tool for the non-intrusive determination of biomass, a unit of measure that facilitates the quantification of ecosystem and...     

Chemically cued suppression of coral reef resilience: Where is the tipping point?

Coral reefs worldwide are shifting from high-diversity, coral-dominated communities to low-diversity systems dominated by seaweeds. This shift can impact essential recovery processes such as larval recruitment and ecosystem resilience. Recent evidence suggests that chemical cues from certain corals attract, and from certain seaweeds suppress, recruitment of juvenile fishes, with loss of coral cover and increases in seaweed cover creating negative feedbacks that prevent reef recovery and sustain seaweed dominance. Unfortunately, the level of seaweed increase and coral decline that creates this chemically cued tipping point remains unknown, depriving managers of data-based targets to prevent damaging feedbacks. We conducted flume and field assays that suggest juvenile fishes sense and respond to cues produced by low levels of seaweed cover. However, the herbivore species we tested was more tolerant of degraded reef cues than non-herbivores, possibly providing some degree of resilience if these fishes recruit, consume macroalgae, and diminish negative cues.     

Functional responses and predator–prey models: a critique of ratio dependence

Arditi and Ginzburg (2012) propose ordinary differential equations (ODEs) with ratio-dependent functional responses as the new null model for predation, based on their earlier work on ratio-dependent food chains and a number of functional response measurements. Here, I discuss some of their claims, arguing for a flexible and problem-driven approach to predator–prey modeling. Models to understand population cycles and models to predict the effect of basal enrichment on food chains need not be the same. While ratio-dependent functional responses in ODE models might sometimes be useful as limit cases for food chains, they are not intrinsically more useful than prey-dependent models to understand the effect of a given predator on prey population dynamics—and sometimes less useful, given the small temporal scales considered in many models. “Instantism” is showed to be an invalid criticism when ODEs are interpreted as describing average trajectories of stochastic birth–death processes. Moreover, other modeling frameworks with strong ties to time series statistics, such as stochastic difference equations, should be promoted to improve the feedback loop between field and theoretical research. The main problems of current trophic ecology do not lie in a wrong null model, as ecologists have already several at their disposal. The loose connection of ODE models with empirical data and spatial/temporal scaling up of empirical measurements constitute more serious challenges to our understanding of trophic interactions and their consequences on ecosystem functioning.