A general pattern of trade-offs between ecosystem resistance and resilience to tropical cyclones.

Tropical cyclones drive coastal ecosystem dynamics, and their frequency, intensity, and spatial distribution are predicted to shift with climate change. Patterns of resistance and resilience were synthesized for 4138 ecosystem time series from n = 26 storms occurring between 1985 and 2018 in the Northern Hemisphere to predict how coastal ecosystems will respond to future disturbance regimes. Data were grouped by ecosystems (fresh water, salt water, terrestrial, and wetland) and response categories (biogeochemistry, hydrography, mobile biota, sedentary fauna, and vascular plants). We observed a repeated pattern of trade-offs between resistance and resilience across analyses. These patterns are likely the outcomes of evolutionary adaptation, they conform to disturbance theories, and they indicate that consistent rules may govern ecosystem susceptibility to tropical cyclones.

The importance of spawning behavior in understanding the vulnerability of exploited marine fishes in the U.S. Gulf of Mexico.

The vulnerability of a fish stock to becoming overfished is dependent upon biological traits that influence productivity and external factors that determine susceptibility or exposure to fishing effort. While a suite of life history traits are traditionally incorporated into management efforts due to their direct association with vulnerability to overfishing, spawning behavioral traits are seldom considered. We synthesized the existing biological and fisheries information of 28 fish stocks in the U.S. Gulf of Mexico to investigate relationships between life history traits, spawning behavioral traits, management regulations, and vulnerability to fishing during the spawning season. Our results showed that spawning behavioral traits were not correlated with life history traits but improved identification of species that have been historically overfished. Species varied widely in their intrinsic vulnerability to fishing during spawning in association with a broad range of behavioral strategies. Extrinsic vulnerability was high for nearly all species due to exposure to fishing during the spawning season and few management measures in place to protect spawning fish. Similarly, several species with the highest vulnerability scores were historically overfished in association with spawning aggregations. The most vulnerable species included several stocks that have not been assessed and should be prioritized for further research and monitoring. Collectively, the results of this study illustrate that spawning behavior is a distinct aspect of fish ecology that is important to consider for predictions of vulnerability and resilience to fisheries exploitation.

Reproductive behaviour and concurrent sound production of Gulf grouper Mycteroperca jordani (Epinephelidae) at a spawning aggregation site.

The reproductive and acoustic behaviours of Gulf grouper Mycteroperca jordani were studied at a spawning aggregation site in the southern Gulf of California, México. In May 2015-2017, divers located and surveyed a spawning aggregation site within Cabo Pulmo National Park. Adult M. jordani conformed to a lek mating system in which large males formed territories over sand adjacent to a rocky reef that were spatially segregated from smaller females outside of courtship and spawning periods. Females moved into male territories during evening hours to spawn. Male courtship behaviours targeted a single female, included head shakes and burst rises and preceded pair spawning prior to sunset. Males and females displayed three shared colour phases, but four phases were sex-specific. During evening hours, courtship and spawning, both sexes exhibited sexual dichromatism concurrent with reproductive behaviours. The pair-spawning mating system and observations of bimodal size distributions by sex support previous claims of protogyny in the species. Males produced sounds during territorial patrols, courtship and spawning rushes, which corroborated the importance of acoustic communication within the behavioural repertoire associated with spawning. Long-term acoustic monitoring revealed increases in total sounds detected day-1 from March through June with diel increases (e.g., evenings) that may be indicative of the spawning season. Observations of spawning on 12 consecutive evenings in May 2017 coupled with extended periods of sound production suggest that spawning does not follow a lunar rhythm. This first description of the mating system and sounds of the endangered M. jordani facilitates future development of seasonal and areal protections to restore and manage the species.

Reproductive resilience of an estuarine fish in the eye of a hurricane.

Spatial and temporal patterns of spawning activity are important measures of resilience in fishes that directly link environmental disturbances with reproductive success. We acoustically monitored spawning in spotted seatrout (Cynoscion nebulosus) from April through September 2017 at 15 sites near Port Aransas, Texas, which coincided with the landfall of a category 4 hurricane (Harvey) on 25 August. Spawning sounds were recorded every day of the study across all sites and were also confirmed during the hurricane at two sites located within the eye of the storm. Daily spawning continued after the hurricane, but the onset of spawning shifted 2.12 h earlier for 5 days, after which it returned to the pre-storm schedule. These results illustrate the resilience of seatrout to intense, episodic disturbances and offer insights on the phenotypic plasticity of estuarine fishes to cope with projected increases in environmental variability.

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.

The influence of sample distribution on growth model output for a highly-exploited marine fish, the Gulf Corvina (Cynoscion othonopterus).

Estimating the growth of fishes is critical to understanding their life history and conducting fisheries assessments. It is imperative to sufficiently sample each size and age class of fishes to construct models that accurately reflect biological growth patterns, but this may be a challenging endeavor for highly-exploited species in which older fish are rare. Here, we use the Gulf Corvina (Cynoscion othonopterus), a vulnerable marine fish that has been persistently overfished for two decades, as a model species to compare the performance of several growth models. We fit the von Bertalanffy, Gompertz, logistic, Schnute, and Schnute-Richards growth models to length-at-age data by nonlinear least squares regression and used simple indicators to reveal biased data and ensure our results were biologically feasible. We then explored the consequences of selecting a biased growth model with a per-recruit model that estimated female spawning-stock-biomass-per-recruit and yield-per-recruit. Based on statistics alone, we found that the Schnute-Richards model described our data best. However, it was evident that our data were biased by a bimodal distribution of samples and underrepresentation of large, old individuals, and we found the Schnute-Richards model output to be biologically implausible. By simulating an equal distribution of samples across all age classes, we found that sample distribution distinctly influenced model output for all growth models tested. Consequently, we determined that the growth pattern of the Gulf Corvina was best described by the von Bertalanffy growth model, which was the most robust to biased data, comparable across studies, and statistically comparable to the Schnute-Richards model. Growth model selection had important consequences for assessment, as the per-recruit model employing the Schnute-Richards model fit to raw data predicted the stock to be in a much healthier state than per-recruit models employing other growth models. Our results serve as a reminder of the importance of complete sampling of all size and age classes when possible and transparent identification of biased data when complete sampling is not possible.

Author Correction: Prioritizing monitoring and conservation efforts for fish spawning aggregations in the U.S. Gulf of Mexico.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has not been fixed in the paper.

Prioritizing monitoring and conservation efforts for fish spawning aggregations in the U.S. Gulf of Mexico.

In the U.S. Gulf of Mexico (U.S. GOM), the identification and characterization of transient fish spawning aggregation (FSA) sites is recognized as a regional priority for conservation, but progress is hindered by a lack of understanding of FSA distributions for most exploited species. We employed information compiled in regional databases on FSAs and monitoring for the U.S. GOM to fit species distribution models and produce maps showing the areas likely to host single- and multi-species transient FSA sites. Our results revealed two distinct regions of the U.S. GOM for prioritizing monitoring and conservation efforts for transient FSAs: the coastal waters surrounding major bay systems, particularly those of Texas and Louisiana, and portions of the continental shelf edge (the Flower Garden Banks area and the West Florida shelf edge). The next step would be to locate and characterize actual transient FSA sites in the U.S. GOM by surveying within the areas we identified.

A sound worth saving: acoustic characteristics of a massive fish spawning aggregation.

Group choruses of marine animals can produce extraordinarily loud sounds that markedly elevate levels of the ambient soundscape. We investigated sound production in the Gulf corvina (Cynoscion othonopterus), a soniferous marine fish with a unique reproductive behaviour threatened by overfishing, to compare with sounds produced by other marine animals. We coupled echosounder and hydrophone surveys to estimate the magnitude of the aggregation and sounds produced during spawning. We characterized individual calls and documented changes in the soundscape generated by the presence of as many as 1.5 million corvina within a spawning aggregation spanning distances up to 27 km. We show that calls by male corvina represent the loudest sounds recorded in a marine fish, and the spatio-temporal magnitude of their collective choruses are among the loudest animal sounds recorded in aquatic environments. While this wildlife spectacle is at great risk of disappearing due to overfishing, regional conservation efforts are focused on other endangered marine animals.

Estimating fish abundance at spawning aggregations from courtship sound levels.

Sound produced by fish spawning aggregations (FSAs) permits the use of passive acoustic methods to identify the timing and location of spawning. However, difficulties in relating sound levels to abundance have impeded the use of passive acoustics to conduct quantitative assessments of biomass. Here we show that models of measured fish sound production versus independently measured fish density can be generated to estimate abundance and biomass from sound levels at FSAs. We compared sound levels produced by spawning Gulf Corvina (Cynoscion othonopterus) with simultaneous measurements of density from active acoustic surveys in the Colorado River Delta, Mexico. During the formation of FSAs, we estimated peak abundance at 1.53 to 1.55 million fish, which equated to a biomass of 2,133 to 2,145 metric tons. Sound levels ranged from 0.02 to 12,738 Pa2, with larger measurements observed on outgoing tides. The relationship between sound levels and densities was variable across the duration of surveys but stabilized during the peak spawning period after high tide to produce a linear relationship. Our results support the use of active acoustic methods to estimate density, abundance, and biomass of fish at FSAs; using appropriately scaled empirical relationships, sound levels can be used to infer these estimates.

Correction: A spatial method to calculate small-scale fisheries effort in data poor scenarios.

[This corrects the article DOI: 10.1371/journal.pone.0174064.].

A spatial method to calculate small-scale fisheries effort in data poor scenarios.

To gauge the collateral impacts of fishing we must know where fishing boats operate and how much they fish. Although small-scale fisheries land approximately the same amount of fish for human consumption as industrial fleets globally, methods of estimating their fishing effort are comparatively poor. We present an accessible, spatial method of calculating the effort of small-scale fisheries based on two simple measures that are available, or at least easily estimated, in even the most data-poor fisheries: the number of boats and the local coastal human population. We illustrate the method using a small-scale fisheries case study from the Gulf of California, Mexico, and show that our measure of Predicted Fishing Effort (PFE), measured as the number of boats operating in a given area per day adjusted by the number of people in local coastal populations, can accurately predict fisheries landings in the Gulf. Comparing our values of PFE to commercial fishery landings throughout the Gulf also indicates that the current number of small-scale fishing boats in the Gulf is approximately double what is required to land theoretical maximum fish biomass. Our method is fishery-type independent and can be used to quantitatively evaluate the efficacy of growth in small-scale fisheries. This new method provides an important first step towards estimating the fishing effort of small-scale fleets globally.

Operationalizing the social-ecological systems framework to assess sustainability.

Environmental governance is more effective when the scales of ecological processes are well matched with the human institutions charged with managing human-environment interactions. The social-ecological systems (SESs) framework provides guidance on how to assess the social and ecological dimensions that contribute to sustainable resource use and management, but rarely if ever has been operationalized for multiple localities in a spatially explicit, quantitative manner. Here, we use the case of small-scale fisheries in Baja California Sur, Mexico, to identify distinct SES regions and test key aspects of coupled SESs theory. Regions that exhibit greater potential for social-ecological sustainability in one dimension do not necessarily exhibit it in others, highlighting the importance of integrative, coupled system analyses when implementing spatial planning and other ecosystem-based strategies.

Asymmetric connectivity of spawning aggregations of a commercially important marine fish using a multidisciplinary approach.

Understanding patterns of larval dispersal is key in determining whether no-take marine reserves are self-sustaining, what will be protected inside reserves and where the benefits of reserves will be observed. We followed a multidisciplinary approach that merged detailed descriptions of fishing zones and spawning time at 17 sites distributed in the Midriff Island region of the Gulf of California with a biophysical oceanographic model that simulated larval transport at Pelagic Larval Duration (PLD) 14, 21 and 28 days for the most common and targeted predatory reef fish, (leopard grouper Mycteroperca rosacea). We tested the hypothesis that source-sink larval metapopulation dynamics describing the direction and frequency of larval dispersal according to an oceanographic model can help to explain empirical genetic data. We described modeled metapopulation dynamics using graph theory and employed empirical sequence data from a subset of 11 sites at two mitochondrial genes to verify the model predictions based on patterns of genetic diversity within sites and genetic structure between sites. We employed a population graph describing a network of genetic relationships among sites and contrasted it against modeled networks. While our results failed to explain genetic diversity within sites, they confirmed that ocean models summarized via graph and adjacency distances over modeled networks can explain seemingly chaotic patterns of genetic structure between sites. Empirical and modeled networks showed significant similarities in the clustering coefficients of each site and adjacency matrices between sites. Most of the connectivity patterns observed towards downstream sites (Sonora coast) were strictly asymmetric, while those between upstream sites (Baja and the Midriffs) were symmetric. The best-supported gene flow model and analyses of modularity of the modeled networks confirmed a pulse of larvae from the Baja Peninsula, across the Midriff Island region and towards the Sonoran coastline that acts like a larval sink, in agreement with the cyclonic gyre (anti-clockwise) present at the peak of spawning (May-June). Our approach provided a mechanistic explanation of the location of fishing zones: most of the largest areas where fishing takes place seem to be sustained simultaneously by high levels of local retention, contribution of larvae from upstream sites and oceanographic patterns that concentrate larval density from all over the region. The general asymmetry in marine connectivity observed highlights that benefits from reserves are biased towards particular directions, that no-take areas need to be located upstream of targeted fishing zones, and that some fishing localities might not directly benefit from avoiding fishing within reserves located adjacent to their communities. We discuss the implications of marine connectivity for the current network of marine protected areas and no-take zones, and identify ways of improving it.

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.

Long-term effectiveness of a multi-use marine protected area on reef fish assemblages and fisheries landings.

The Loreto Bay National Park (LBNP) is a large, multi-use marine protected area in the Gulf of California, Mexico, where several types of small-scale commercial and recreational fishing are allowed, but where less than 1% of the park is totally protected from fishing. The LBNP was created in 1996; its management plan was completed in 2000, but it was not effectively implemented and enforced until 2003. Between 1998 and 2010, we monitored reef fish populations annually at several reefs inside and outside the LBNP to measure the effects of the park on fish assemblages. We also evaluated reported fisheries landings within the LBNP for the same time series. Our results show that reef fish biomass increased significantly after protection at a small no-take site at LBNP relative to the rest of the park. However, the multi-use part of LBNP where fishing is allowed (99% of its surface) has had no measurable effect on reef fish biomass relative to open access sites outside the park boundaries. Reported fisheries landings have decreased within the park while increasing in nearby unprotected areas. Although the current partial protection management regime has not allowed for reef fish populations to recover despite 15 years as a "protected area," we conclude that LBNP's regulations and management have maintained the conditions of the ecosystem that existed when the park was established. These results suggest that community livelihoods have been sustained, but a re-evaluation of the multi-use management strategy, particularly the creation of larger no-take zones and better enforcement, is needed to improve the reef fish populations in the park in order to ensure sustainable fisheries far into the future. These recommendations can be applied to all multi-use MPAs in Mexico where ecosystem recovery is not occurring despite maintenance of fish stocks.

Spatio-temporal dynamics of a fish spawning aggregation and its fishery in the Gulf of California.

We engaged in cooperative research with fishers and stakeholders to characterize the fine-scale, spatio-temporal characteristics of spawning behavior in an aggregating marine fish (Cynoscion othonopterus: Sciaenidae) and coincident activities of its commercial fishery in the Upper Gulf of California. Approximately 1.5-1.8 million fish are harvested annually from spawning aggregations of C. othonopterus during 21-25 days of fishing and within an area of 1,149 km(2) of a biosphere reserve. Spawning and fishing are synchronized on a semi-lunar cycle, with peaks in both occurring 5 to 2 days before the new and full moon, and fishing intensity and catch are highest at the spawning grounds within a no-take reserve. Results of this study demonstrate the benefits of combining GPS data loggers, fisheries data, biological surveys, and cooperative research with fishers to produce spatio-temporally explicit information relevant to the science and management of fish spawning aggregations and the spatial planning of marine reserves.

Large recovery of fish biomass in a no-take marine reserve.

No-take marine reserves are effective management tools used to restore fish biomass and community structure in areas depleted by overfishing. Cabo Pulmo National Park (CPNP) was created in 1995 and is the only well enforced no-take area in the Gulf of California, Mexico, mostly because of widespread support from the local community. In 1999, four years after the establishment of the reserve, there were no significant differences in fish biomass between CPNP (0.75 t ha(-1) on average) and other marine protected areas or open access areas in the Gulf of California. By 2009, total fish biomass at CPNP had increased to 4.24 t ha(-1) (absolute biomass increase of 3.49 t ha(-1), or 463%), and the biomass of top predators and carnivores increased by 11 and 4 times, respectively. However, fish biomass did not change significantly in other marine protected areas or open access areas over the same time period. The absolute increase in fish biomass at CPNP within a decade is the largest measured in a marine reserve worldwide, and it is likely due to a combination of social (strong community leadership, social cohesion, effective enforcement) and ecological factors. The recovery of fish biomass inside CPNP has resulted in significant economic benefits, indicating that community-managed marine reserves are a viable solution to unsustainable coastal development and fisheries collapse in the Gulf of California and elsewhere.

A phylogenetic test of the size-advantage model: evolutionary changes in mating behavior influence the loss of sex change in a fish lineage.

The size-advantage model asserts that mating behavior influences the incidence and direction of sex change in animals. Selection for protogyny (female to male sex change) occurs in mating systems in which large males monopolize and pair spawn with females; however, gonochorism (no sex change) is favored when adults spawn in groups and sperm competition is present. Despite widespread empirical and theoretical support for the model, these predictions have not been tested within a phylogenetic context. Here we show that the loss of sex change within a lineage of reef fishes is influenced by evolutionary changes in two traits related to their mating behavior: mating group structure and sperm competition intensity. Phylogenetic reconstructions of the reproductive evolution of groupers (Epinephelidae) indicate that protogyny and paired spawning are the ancestral conditions for the lineage; both gonochorism and group spawning evolved independently at least four times in three different genera. Evolutionary transformations from protogyny to gonochorism (loss of sex change) are associated with equivalent transformations in mating group structure from paired to group spawning, and sperm competition is considerably higher in gonochoric species than in protogynous species. These results provide explicit phylogenetic support for predictions of the size-advantage model, demonstrating that selection for protogynous sex change decreases as mating group size and sperm competition intensity increase.