Fake spawns and floating particles: a rebuttal of Karkarey et al. "Alternative reproductive tactics and inverse size-assortment in a high-density fish spawning aggregation".

Courtship and spawning behaviors of coral reef fishes are very complex, and sufficient sampling effort and proper methods are required to draw informed conclusions on their mating systems that are grounded in contemporary theories of mate choice and sexual selection. We reviewed the recent study by Karkarey et al. (BMC Ecol 17:10, 2017) on the spawning behavior of Squaretail coralgrouper (Plectropomus areolatus) from India and found no evidence to support their findings of alternative reproductive tactics, unique school-spawning involving a single male with multiple females, or inverse size-assortment. The study lacks scientific credibility due to a lack of rigor in the methodology used, misinterpretation of observed behaviors, misinterpretation of the literature, and insufficient data. Their approach led the authors to produce spurious results and profound, invalid conclusions that violate the most basic assumptions of mate choice and sexual selection theory as applied to mating systems in marine fishes.

Protection of large predators in a marine reserve alters size-dependent prey mortality.

Where predator-prey interactions are size-dependent, reductions in predator size owing to fishing has the potential to disrupt the ecological role of top predators in marine ecosystems. In southern California kelp forests, we investigated the size-dependence of the interaction between herbivorous sea urchins and one of their predators, California sheephead (Semicossyphus pulcher). Empirical tests examined how differences in predator size structure between reserve and fished areas affected size-specific urchin mortality. Sites inside marine reserves had greater sheephead size and biomass, while empirical feeding trials indicated that larger sheephead were required to successfully consume urchins of increasing test diameter. Evaluations of the selectivity of sheephead for two urchin species indicated that shorter-spined purple urchins were attacked more frequently and successfully than longer-spined red urchins of the same size class, particularly at the largest test diameters. As a result of these size-specific interactions and the higher biomass of large sheephead inside reserves, urchin mortality rates were three times higher inside the reserve for both species. In addition, urchin mortality rates decreased with urchin size, and very few large urchins were successfully consumed in fished areas. The truncation of sheephead size structure that commonly occurs owing to fishing will probably result in reductions in urchin mortality, which may reduce the resilience of kelp beds to urchin barren formation. By contrast, the recovery of predator size structure in marine reserves may restore this resilience, but may be delayed until fish grow to sizes capable of consuming larger urchins.

Human activities change marine ecosystems by altering predation risk.

In ocean ecosystems, many of the changes in predation risk - both increases and decreases - are human-induced. These changes are occurring at scales ranging from global to local and across variable temporal scales. Indirect, risk-based effects of human activity are known to be important in structuring some terrestrial ecosystems, but these impacts have largely been neglected in oceans. Here, we synthesize existing literature and data to explore multiple lines of evidence that collectively suggest diverse human activities are changing marine ecosystems, including carbon storage capacity, in myriad ways by altering predation risk. We provide novel, compelling evidence that at least one key human activity, overfishing, can lead to distinct, cascading risk effects in natural ecosystems whose magnitude exceeds that of presumed lethal effects and may account for previously unexplained findings. We further discuss the conservation implications of human-caused indirect risk effects. Finally, we provide a predictive framework for when human alterations of risk in oceans should lead to cascading effects and outline a prospectus for future research. Given the speed and extent with which human activities are altering marine risk landscapes, it is crucial that conservation and management policy considers the indirect effects of these activities in order to increase the likelihood of success and avoid unfortunate surprises.

Predicting evolutionary responses to climate change in the sea.

An increasing number of short-term experimental studies show significant effects of projected ocean warming and ocean acidification on the performance on marine organisms. Yet, it remains unclear if we can reliably predict the impact of climate change on marine populations and ecosystems, because we lack sufficient understanding of the capacity for marine organisms to adapt to rapid climate change. In this review, we emphasise why an evolutionary perspective is crucial to understanding climate change impacts in the sea and examine the approaches that may be useful for addressing this challenge. We first consider what the geological record and present-day analogues of future climate conditions can tell us about the potential for adaptation to climate change. We also examine evidence that phenotypic plasticity may assist marine species to persist in a rapidly changing climate. We then outline the various experimental approaches that can be used to estimate evolutionary potential, focusing on molecular tools, quantitative genetics, and experimental evolution, and we describe the benefits of combining different approaches to gain a deeper understanding of evolutionary potential. Our goal is to provide a platform for future research addressing the evolutionary potential for marine organisms to cope with climate change.

Does fish larval dispersal differ between high and low latitudes?

Several factors lead to expectations that the scale of larval dispersal and population connectivity of marine animals differs with latitude. We examine this expectation for demersal shorefishes, including relevant mechanisms, assumptions and evidence. We explore latitudinal differences in (i) biological (e.g. species composition, spawning mode, pelagic larval duration, PLD), (ii) physical (e.g. water movement, habitat fragmentation), and (iii) biophysical factors (primarily temperature, which could strongly affect development, swimming ability or feeding). Latitudinal differences exist in taxonomic composition, habitat fragmentation, temperature and larval swimming, and each difference could influence larval dispersal. Nevertheless, clear evidence for latitudinal differences in larval dispersal at the level of broad faunas is lacking. For example, PLD is strongly influenced by taxon, habitat and geographical region, but no independent latitudinal trend is present in published PLD values. Any trends in larval dispersal may be obscured by a lack of appropriate information, or use of 'off the shelf' information that is biased with regard to the species assemblages in areas of concern. Biases may also be introduced from latitudinal differences in taxa or spawning modes as well as limited latitudinal sampling. We suggest research to make progress on the question of latitudinal trends in larval dispersal.

Postsettlement survival linked to larval life in a marine fish.

There is a growing realization that the scale and degree of population connectivity are crucial to the dynamics and persistence of spatially structured populations. For marine organisms with complex life cycles, experiences during larval life may influence phenotypic traits, performance, and the probability of postsettlement survival. For a Caribbean reef fish (Thalassoma bifasciatum) on an oceanic island, we used otolith (ear stone) elemental profiles of lead (Pb) to assign recent settlers to a group that developed in waters elevated in Pb concentrations throughout larval life (i.e., nearshore signature) and a group that developed in waters depleted in Pb (i.e., offshore signature), potentially dispersing from upstream sources across oceanic waters. Larval history influenced early life history traits: offshore developers initially grew slowly but compensated with fast growth upon entering nearshore waters and metamorphosed in better condition with higher energy reserves. As shown in previous studies, local production contributed heavily to settlement: at least 45% of settlers developed nearshore. However, only 23% of survivors after the first month displayed a nearshore otolith profile. Therefore, settlers with different larval histories suffered differential mortality. Importantly, selective mortality was mediated by larval history, in that the postsettlement intensity of selection was much greater for fish that developed nearshore, potentially because they had developed in a less selectively intense larval environment. Given the potential for asymmetrical postsettlement source-based survival, successful spatial management of marine populations may require knowledge of "realized connectivity" on ecological scales, which takes into account the postsettlement fitness of individuals from different sources.

Fishing indirectly structures macroalgal assemblages by altering herbivore behavior.

Fishing has clear direct effects on harvested species, but its cascading, indirect effects are less well understood. Fishing disproportionately removes larger, predatory fishes from marine food webs. Most studies of the consequent indirect effects focus on density-mediated interactions where predator removal alternately drives increases and decreases in abundances of successively lower trophic-level species. While prey may increase in number with fewer predators, they may also alter their behavior. When such behavioral responses impact the food resources of prey species, behaviorally mediated trophic cascades can dramatically shape landscapes. It remains unclear whether this pathway of change is typically triggered by ocean fishing. By coupling a simple foraging model with empirical observations from coral reefs, we provide a mechanistic basis for understanding and predicting how predator harvest can alter the landscape of risk for herbivores and consequently drive dramatic changes in primary producer distributions. These results broaden trophic cascade predictions for fisheries to include behavioral changes. They also provide a framework for detecting the presence and magnitude of behaviorally mediated cascades. This knowledge will help to reconcile the disparity between expected and observed patterns of fishing-induced cascades in the sea.

Field evidence for pervasive indirect effects of fishing on prey foraging behavior.

The indirect, ecosystem-level consequences of ocean fishing, and particularly the mechanisms driving them, are poorly understood. Most studies focus on density-mediated trophic cascades, where removal of predators alternately causes increases and decreases in abundances of lower trophic levels. However, cascades could also be driven by where and when prey forage rather than solely by prey abundance. Over a large gradient of fishing intensity in the central Pacific's remote northern Line Islands, including a nearly pristine, baseline coral reef system, we found that changes in predation risk elicit strong behavioral responses in foraging patterns across multiple prey fish species. These responses were observed as a function of both short-term ("acute") risk and longer-term ("chronic") risk, as well as when prey were exposed to model predators to isolate the effect of perceived predation risk from other potentially confounding factors. Compared to numerical prey responses, antipredator behavioral responses such as these can potentially have far greater net impacts (by occurring over entire assemblages) and operate over shorter temporal scales (with potentially instantaneous response times) in transmitting top-down effects. A rich body of literature exists on both the direct effects of human removal of predators from ecosystems and predators' effects on prey behavior. Our results draw together these lines of research and provide the first empirical evidence that large-scale human removal of predators from a natural ecosystem indirectly alters prey behavior. These behavioral changes may, in turn, drive previously unsuspected alterations in reef food webs.

The relationship between maternal phenotype and offspring quality: do older mothers really produce the best offspring?

Maternal effects are increasingly recognized as important drivers of population dynamics and determinants of evolutionary trajectories. Recently, there has been a proliferation of studies finding or citing a positive relationship between maternal size/age and offspring size or offspring quality. The relationship between maternal phenotype and offspring size is intriguing in that it is unclear why young mothers should produce offspring of inferior quality or fitness. Here we evaluate the underlying evolutionary pressures that may lead to a maternal size/age-offspring size correlation and consider the likelihood that such a correlation results in a positive relationship between the age or size of mothers and the fitness of their offspring. We find that, while there are a number of reasons why selection may favor the production of larger offspring by larger mothers, this change in size is more likely due to associated changes in the maternal phenotype that affect the offspring size-performance relationship. We did not find evidence that the offspring of older females should have intrinsically higher fitness. When we explored this issue theoretically, the only instance in which smaller mothers produce suboptimal offspring sizes is when a (largely unsupported) constraint on maximum offspring size is introduced into the model. It is clear that larger offspring fare better than smaller offspring when reared in the same environment, but this misses a critical point: different environments elicit selection for different optimal sizes of young. We suggest that caution should be exercised when interpreting the outcome of offspring-size experiments when offspring from different mothers are reared in a common environment, because this approach may remove the source of selection (e.g., reproducing in different context) that induced a shift in offspring size in the first place. It has been suggested that fish stocks should be managed to preserve these older age classes because larger mothers produce offspring with a greater chance of survival and subsequent recruitment. Overall, we suggest that, while there are clear and compelling reasons for preserving older females in exploited populations, there is little theoretical justification or evidence that older mothers produce offspring with higher per capita fitness than do younger mothers.

Evolutionary biology: sex change and relative body size in animals.

Organisms that change sex during their lifetime use a variety of strategies--they may be female first, male first or even repetitive sex changers. Natural selection should favour those individuals that change sex at a time when it increases their reproductive value. Allsop and West claim that the relative timing of sex change is invariant across all animals, with individuals changing sex at 72% of their maximum body size, and infer that natural selection for sex change must therefore be fundamentally similar across animals. Here we explain why we believe that Allsop and West's claims are not supported by their analysis or by their empirical data.

Markov chain Monte Carlo methods for assigning larvae to natal sites using natural geochemical tags.

Geochemical signatures deposited in otoliths are a potentially powerful means of identifying the origin and dispersal history of fish. However, current analytical methods for assigning natal origins of fish in mixed-stock analyses require knowledge of the number of potential sources and their characteristic geochemical signatures. Such baseline data are difficult or impossible to obtain for many species. A new approach to this problem can be found in iterative Markov Chain Monte Carlo (MCMC) algorithms that simultaneously estimate population parameters and assign individuals to groups. MCMC procedures only require an estimate of the number of source populations, and post hoc model selection based on the deviance information criterion can be used to infer the correct number of chemically distinct sources. We describe the basics of the MCMC approach and outline the specific decisions required when implementing the technique with otolith geochemical data. We also illustrate the use of the MCMC approach on simulated data and empirical geochemical signatures in otoliths from young-of-the-year and adult weakfish, Cynoscion regalis, from the U.S. Atlantic coast. While we describe how investigators can use MCMC to complement existing analytical tools for use with otolith geochemical data, the MCMC approach is suitable for any mixed-stock problem with a continuous, multivariate data.

Safety in numbers and the spatial scaling of density-dependent mortality in a coral reef fish.

In coral reef fishes, density-dependent population regulation is commonly mediated via predation on juveniles that have recently settled from the plankton. All else being equal, strong density-dependent mortality should select against the formation of high-density aggregations, yet the juveniles of many reef fishes aggregate. In light of this apparent contradiction, we hypothesized that the form and intensity of density dependence vary with the spatial scale of measurement. Individual groups might enjoy safety in numbers, but predators could still produce density-dependent mortality at larger spatial scales. We investigated this possibility using recently settled juvenile bluehead wrasse, Thalassoma bifasciatum, a small, aggregating reef fish. An initial caging experiment demonstrated that juvenile bluehead wrasse settlers suffer high predation, and spatial settlement patterns indicated that bluehead wrasse juveniles preferentially settle in groups, although they are also found singly. We then monitored the mortality of recently settled juveniles at two spatial scales: microsites, occupied by individual fish or groups of fish and separated by centimeters, and sites, consisting of approximately 2400-m2 areas of reef and separated by kilometers. At the microsite scale, we measured group size and effective population density independently and found that per capita mortality decreased with group size but was not related to density. At the larger spatial scale, however, per capita mortality increased with settler density. This shift in the form of density dependence with spatial scale could reconcile the existence of small-scale aggregative behavior typical of many reef fishes with the population-scale density dependence that is essential to population stability and persistence.

A social basis for the development of primary males in a sex-changing fish.

An example of alternative male strategies is seen in diandric protogynous (female first) hermaphrodites, where individuals either mature directly as male (primary males) or first reproduce as female and then change sex to male (secondary males). In some sex-changing fishes, the testes of primary males appear anatomically similar to those of non-sex-changing species, whereas the testes of secondary males have anatomical evidence of their former ovarian function. Here, we provide evidence that in the bluehead wrasse, Thalassoma bifasciatum, these strikingly different male phenotypes arise from differences in the ontogenetic timing of environmental sex determination, timing that can be experimentally altered through changes in the social circumstances. Juveniles differentiated almost exclusively as females when reared in isolation, regardless of whether they were collected from a reef with a high proportion of primary males or from a reef with a low proportion of primary males. In contrast, one individual usually differentiated as a primary male when reared in groups of three. Our results indicate that primary males of the bluehead wrasse are an environmentally sensitive developmental strategy that has probably evolved in response to variation in the reproductive success of primary males in populations of different sizes.

Current shifts and kin aggregation explain genetic patchiness in fish recruits.

The scales of population structure in marine species depend on the degree to which larvae from different populations are mixed in the plankton. There is an intriguing trend in marine population genetic studies of significant genetic structure for larvae, recruits, or populations at fine scales that is unpatterned across space and changes through time. This "chaotic genetic patchiness" suggests that larval pools are not well mixed in the plankton. However, few studies have been able to distinguish among potential causes of spatial and temporal genetic heterogeneity: changes in larval migration patterns, changes in environmental selection, or stochasticity caused by "sweepstakes" reproductive success of spawners creating detectable family structure. Here we use microsatellite markers to show that significant allele frequency shifts occurred sporadically in space and time for cohorts of recruits of Paralabrax clathratus (kelp bass) collected once every two weeks over two years from five sites in the Santa Barbara Channel, California, USA. We found that the pattern of genetic differentiation among cohorts was explained by a combination of (1) family structure in some cohorts, evidenced by half and full siblings, and (2) an indication of changes in larval delivery. It is unlikely but possible that environmental selection also plays a role. Although sampling of potential source populations was incomplete, cohorts arriving during western current flows show most genetic similarity with a population sample collected in the west, and cohorts arriving during current flows from the southeast show similarity with population samples collected in the south and east. Despite the family structure apparent in some cohorts, these "sweepstakes" events occur on too fine a scale to create lasting year class genetic structure. The results corroborate oceanographic models of larval dispersal, which suggest that larval mixing in the plankton is less extensive than previously believed.

Habitat size, recruitment, and longevity as factors limiting population size in stage-structured species.

Surprisingly little research has evaluated how habitat size may limit the population size of species that use different habitats at different stages of their lives. Here we develop simple discrete-time models to describe the population dynamics of species that use separate juvenile and adult habitats. Analytic solutions, model simulations, and elasticity and sensitivity analyses show that adult abundance is only limited by the size of the juvenile habitat when both adult habitat size and recruitment are much larger than juvenile habitat size. Juvenile habitat plays a marginally greater role in limiting population size for species with closed populations, where recruitment is proportional to adult abundance, versus open populations. Because adult populations often accumulate pulses of juveniles, adult habitat size can strongly limit population size over a broad range of parameter values, an effect that increases as the longevity of a species increases. Limited empirical research from a range of taxa supports these model predictions, although few studies were designed to actually test the limiting role of juvenile versus adult habitat. Future research must carefully evaluate whether and how processes at the juvenile stage affect adult abundance, and conservation efforts may be able to use this model to evaluate the cost-effectiveness, vis-a-vis increasing adult abundance, of time and money allocated to protecting juvenile habitats.

Recovery trajectories of kelp forest animals are rapid yet spatially variable across a network of temperate marine protected areas.

Oceans currently face a variety of threats, requiring ecosystem-based approaches to management such as networks of marine protected areas (MPAs). We evaluated changes in fish biomass on temperate rocky reefs over the decade following implementation of a network of MPAs in the northern Channel Islands, California. We found that the biomass of targeted (i.e. fished) species has increased consistently inside all MPAs in the network, with an effect of geography on the strength of the response. More interesting, biomass of targeted fish species also increased outside MPAs, although only 27% as rapidly as in the protected areas, indicating that redistribution of fishing effort has not severely affected unprotected populations. Whether the increase outside of MPAs is due to changes in fishing pressure, fisheries management actions, adult spillover, favorable environmental conditions, or a combination of all four remains unknown. We evaluated methods of controlling for biogeographic or environmental variation across networks of protected areas and found similar performance of models incorporating empirical sea surface temperature versus a simple geographic blocking term based on assemblage structure. The patterns observed are promising indicators of the success of this network, but more work is needed to understand how ecological and physical contexts affect MPA performance.

Marine defaunation: animal loss in the global ocean.

Marine defaunation, or human-caused animal loss in the oceans, emerged forcefully only hundreds of years ago, whereas terrestrial defaunation has been occurring far longer. Though humans have caused few global marine extinctions, we have profoundly affected marine wildlife, altering the functioning and provisioning of services in every ocean. Current ocean trends, coupled with terrestrial defaunation lessons, suggest that marine defaunation rates will rapidly intensify as human use of the oceans industrializes. Though protected areas are a powerful tool to harness ocean productivity, especially when designed with future climate in mind, additional management strategies will be required. Overall, habitat degradation is likely to intensify as a major driver of marine wildlife loss. Proactive intervention can avert a marine defaunation disaster of the magnitude observed on land.

Allocation to Mate Guarding or Increased Sperm Production in a Mediterranean Wrasse.

An excellent body of literature exists that examines sperm expenditure when males allocate only to sperm production. However, in many species, males can also allocate energy to behaviors that influence sperm competition. We model whether males in sperm competition should allocate energy to mate guarding or additional sperm production. Mate guarding is predicted to lead to greater reproductive success than increased sperm output, and mate-guarding males are not predicted to alter their allocation to sperm production with increasing sperm competition. Only when mate guarding is ineffective or greatly reduces sperm production are males predicted to allocate to sperm production. In a Mediterranean wrasse Symphodus ocellatus, three male alternative reproductive behaviors coexist. While nesting males and satellites guard mates to decrease sperm competition, sneaker males only compete via sperm production. Sneakers produce four times as much sperm per spawn as either nesting males or satellites. As predicted by the model, mate guarding but not sperm production increased with increased risk of sperm competition in nesting males. We argue that this can be explained by nesting males allocating to mate guarding rather than sperm production. Considering allocation among behaviors that affect sperm competition enhances our ability to explain and to predict sperm allocation patterns.

Matching marine reserve design to reserve objectives.

Recent interest in using marine reserves for marine resource management and conservation has largely been driven by the hope that reserves might counteract declines in fish populations and protect the biodiversity of the seas. However, the creation of reserves has led to dissension from some interested groups, such as fishermen, who fear that reserves will do more harm than good. These perceived differences in the effect of marine reserves on various stakeholder interests has led to a contentious debate over their merit. We argue here that recent findings in marine ecology suggest that this debate is largely unnecessary, and that a single general design of a network of reserves of moderate size and variable spacing can meet the needs and goals of most stakeholders interested in marine resources. Given the high fecundity of most marine organisms and recent evidence for limited distance of larval dispersal, it is likely that reserves can both maintain their own biodiversity and service nearby non-reserve areas. In particular, spillover of larger organisms and dispersal of larvae to areas outside reserves can lead to reserves sustaining or even increasing local fisheries. Ultimately, the success of any reserve network requires attention to the uncertainty and variability in dispersal patterns of marine organisms, clear statements of goals by all stakeholder groups and proper evaluation of reserve performance.

Phylogenetic perspectives on the evolution of functional hermaphroditism in teleost fishes.

Hermaphroditism is taxonomically widespread among teleost fishes and takes on many forms including simultaneous, protogynous, and protandrous hermaphroditism, bidirectional sex change, and androdioecy. The proximate mechanisms that influence the timing, incidence, and forms of hermaphroditism in fishes are supported by numerous theoretical and empirical studies on their mating systems and sexual patterns, but few have examined aspects of sex-allocation theory or the evolution of hermaphroditism for this group within a strict phylogenetic context. Fortunately, species-level phylogenetic reconstructions of the evolutionary history of many lineages of fishes have emerged, providing opportunities for understanding fine-scale evolutionary pathways and transformations of sex allocation. Examinations of several families of fishes with adequate data on phylogeny, patterns of sex allocation, mating systems, and with some form of hermaphroditism reveal that the evolution and expression of protogyny and other forms of sex allocation show little evidence of phylogenetic inertia within specific lineages but rather are associated with particular mating systems in accordance with prevalent theories about sex allocation. Transformations from protogyny to gonochorism in groupers (Epinephelidae), seabasses (Serranidae), and wrasses and parrotfishes (Labridae) are associated with equivalent transformations in the structure of mating groups from spawning of pairs to group spawning and related increases in sperm competition. Similarly, patterns of protandry, androdioecy, simultaneous hermaphroditism, and bidirectional sex change in other lineages (Aulopiformes, Gobiidae, and Pomacentridae) match well with particular mating systems in accordance with sex-allocation theory. Unlike other animals and plants, we did not find evidence that transitions between hermaphroditism and gonochorism required functional intermediates. Two instances in which our general conclusions might not hold include the expression of protandry in the Sparidae and the distribution of simultaneous hermaphroditism. In the Sparidae, the association of hypothesized mating systems and patterns of sex allocation were not always consistent with the size-advantage model (SAM), in that certain protandric sparids show evidence of intense sperm competition that should favor the expression of gonochorism. In the other case, simultaneous hermaphroditism does not occur in some groups of monogamous fishes, which are similar in ecology to the hermaphroditic serranines, suggesting that this form of sex allocation may be more limited by phylogenetic inertia. Overall, this work strongly supports sexual lability within teleost fishes and confirms evolutionary theories of sex allocation in this group of vertebrates.