Gonad histology complements research on the life history of fish species and provides greater accuracy and precision than macroscopic characterization of the gonad for determining patterns of oogenesis at the cellular level and maturation at the individual level. In a fishery context, histology improves estimation of mature and spawning stock biomass, identification of spawning seasonality and grounds, and preselection of specimens for calculation of annual fecundity. However, in most studies, only a single staining method (hematoxylin and eosin) has been used. In this study on 3 taxonomically diverse species, using 4 different staining methods of varying complexity (degree of counterstaining), we compared confidence levels in identification of 8 stages of oogenesis, the presence and level of degradation for postovulatory follicles, and atretic (vitellogenic) germ cells. As anticipated, the method involving the least expensive, monochromatic stain provided the lowest level of confidence, whereas the most expensive and complex counterstaining method provided the highest confidence level, with hematoxylin and eosin staining and another simple counterstaining method in between them. The effect of staining method was most evident for identifying cortical alveoli, which can affect estimation of size or age at maturity, and for identifying postovulatory follicles, which can affect estimation of spawning frequency. These results are broadly applicable for determining best practices.
Anthropogenic warming is altering species abundance, distribution, physiology, and more. How changes observed at the species level alter emergent community properties is an active and urgent area of research. Trait-based ecology and regime shift theory provide complementary ways to understand climate change impacts on communities, but these two bodies of work are only rarely integrated. Lack of integration handicaps our ability to understand community responses to warming, at a time when such understanding is critical. Therefore, we advocate for merging trait-based ecology with regime shift theory. We propose a general set of principles to guide this merger and apply these principles to research on marine communities in the rapidly warming North Atlantic. In our example, combining trait distribution and regime shift analyses at the community level yields greater insight than either alone. Looking forward, we identify a clear need for expanding quantitative approaches to collecting and merging trait-based and resilience metrics in order to advance our understanding of climate-driven community change.
Ocean waters of the Northeast US continental shelf have warmed rapidly in recent years, with sea surface temperatures rising 2.5 times faster than those of the global oceans. With this strong warming trend, the frequency and duration of marine heatwaves have increased. These temperature changes stood out as a distinct warm temperature regime during the 2010s. During this decade, fish population characteristics also differed from the past. Species distribution shifts were detected for many species, demonstrating one way species could adapt to warming conditions. However, for most species, distribution shifts were insufficient to avoid warmer surface or bottom temperatures. As species occupied warmer habitats, growth patterns aligned with expectations for warming temperatures. Consistent with the temperature-size rule, some species exhibited faster growth at early life stages but plateaued at smaller body sizes; other species, however, experienced reduced growth across all ages, indicating thermal stress. Finally, population productivity indexed by the recruit-to-spawner ratio declined significantly during the 2010s for some populations. Changes in these three processes—distribution, growth, and productivity—indicate the emergence of climate change signals across multiple Northeast US fish populations. These effects create new challenges for fishery managers and industry participants operating in the context of non-stationarity and uncertainty.
Interactions between spatial dynamics and stock structure in marine fishes have largely focused on stocks in decline; stock structure is rarely re-visited for expanding species. Here, the spatial ecology of Atlantic halibut (Hippoglossus hippoglossus L.), managed as four stocks in the Northwest Atlantic, is reviewed. Halibut collapsed under high exploitation in the mid-19th century, but the Canadian fisheries value has increased seven-fold since the early 2000s. Atlantic halibut's thermal habitat has increased due to warming, possibly contributing to its expansion. Genomic evidence differentiates two populations in the four management units, whereas there is non-genetic spatial structure within each of the stock boundaries. There are different core juvenile areas and a diversity of spawning migration patterns influenced by timing, fish size, maturity state, and distance between summer-feeding and over-wintering habitats. From tagging studies, multiple estimates of median distance at recapture (similar to 3-90 km) are much less than the spatial domain of each stock. Growth rates are faster in the warmer south, as predicted by growing degree day. The current perspective of Atlantic halibut spatial structure is that there are two distinct populations, and within each, there are subpopulations composed of multiple migratory contingents. The level of mixing on common spawning grounds both among and within subpopulations is only partly understood.
The data-limited nature of Atlantic halibut (Hippoglossus hippoglossus) in U.S. waters hampers evaluation of what may be a slow but steady rebuilding pattern. Here, we collaborate with the commercial fishery to design and implement a multi-gear sampling program that collected 100s of biological samples from throughout the Gulf of Maine in a five-year period, 2014–2018. Examination of sectioned otoliths revealed a maximum age of 12 years (females) and 13 years (males); in comparison, Atlantic halibut as old as 40–50 years have been collected elsewhere in the western North Atlantic. Growth modeling confirmed sexual dimorphism, with a larger asymptotic length (L∞) for females (214 cm fork length [FL]) than males (195 cm FL). Estimates of median female length at maturity, L50, of 128 cm FL (124–132 cm, 95% confidence limits), and median female age at maturity, A50, of 9.6 years old (9.0–10.8 years), were longer and older than previous reports for the Gulf of Maine, likely resulting from our use of histological instead of macroscopic methods to classify maturity. Histology demonstrated that vitellogenesis initiated in individuals in spring, nearly a year prior to spawning, which allowed us to identify first-time (primiparous) spawners and provided the first potential evidence of skip spawning for this species. Finally, an index was developed to track the proportion of potentially mature females in the fishery, which showed an increasing trend; this qualitative tool may prove useful in a data-limited environment for evaluating the relative stock status of Atlantic halibut.
Stock assessments of U.S. Atlantic Wolffish Anarhichas lupus are hampered by a landings moratorium and low catches in fishery-independent surveys. Working with the commercial fishing industry, we collected hundreds of fish to overcome a lack of regionally specific life history information. Based on ages from sectioned otoliths, Atlantic Wolffish are long lived (maximum observed age: males = 31 years, females = 29 years). A Gompertz growth model showed that Atlantic Wolffish exhibit dimorphic growth-with larger males across all ages on average. Preliminary estimates of total mortality ranged from 0.15 to 0.21 and were lower than an estimate measured at the beginning of the moratorium. Based on gonad histology, a cohort of vitellogenic oocytes emerged in mature females by April and developed group synchronously to ovulate primarily in October. Skip spawning, which accounts for nonannual spawning, was observed in 5.6% of the mature females. Accounting for abortive maturation, a physiological event that delays functional maturation, improved precision and reduced bias of maturity estimates. The resulting median length at functional maturity was 53 cm total length (95% confidence interval = 49-56 cm), and the median age was 6.7 years old (6.2-7.2 years). These estimates are smaller and younger than elsewhere in the western North Atlantic Ocean, confirming that regionally specific maturity parameters are relevant when assessing reference points of the U.S. Atlantic Wolffish fishery.
Experiments examining fish sensitivities to future oceanic CO. levels have greatly expanded over past decades and identified many potentially affected traits. Curiously, data on reproductive trait responses to high CO. are still scarce, despite their strong link to Darwinian fitness and thus to population vulnerability to ocean acidification. We conducted two rearing experiments on the first broadcast-spawning marine fish model (Atlantic silverside, Menidia menidia) to examine how long-term and novel whole life-cycle exposures to predicted future CO2 levels (similar to 2,000 mu atm) affect laboratory spawning, temperature-specific reproductive investment, fecundity, and size distributions ofmaturing oocytes. At low temperatures (17 degrees C), female body size and therefore potential fecundity (FPot, oocytes/female) slightly increased with CO2, while relative fecundity (FRel, oocytes/g female) remained unaffected. At high temperatures (24 degrees C), high CO2 substantially reduced both F-Pot (-19%) and F-Rel (-28%) relative to control treatments. Irrespective of CO2, females at... C grewlarger and heavier than those at 17 degrees C, and although larger females produced larger oocytes at some developmental stages, they also had lower gonadosomatic indices and lower FRel. Our findings contrast with most previous studies and thus highlight the need to investigate reproductive impacts of increasing CO. on multiple fish specieswith contrasting life history strategies.
A 12-year time series (2005-2016) was examined to explore relationships between European anchovy density, growth, reproduction and habitat dynamics in an upwelling system. Specifically, data used for a daily egg production method were combined with oceanographic data, prey availability, as well as acoustic surveys of the anchovy stock in the Strait of Sicily, in the Central Mediterranean Sea. Variables typically used for evaluating habitat dynamics (i.e. water temperature, chlorophyll-a, zooplankton concentration, kinetic energy, mixed layer depth and upwelling index) indicated strong upwelling events during the summer, when anchovy spawns. A linear 'principal component' combination of environmental traits, associated with summer upwelling, was identified by step-wise regression as a driver for growth (length at the end of the first year; L1), reproductive investment (gonad-somatic index; GSI), as well as egg production (daily specific fecundity; DSF). These relationships are consistent with direct energy flow from the environment to both somatic growth and reproductive output, indicating an income breeding strategy by anchovy (i.e. surplus energy acquired during the summer breeding season is used directly for reproductive growth). Step-wise regression also identified three additional relationships: (1) a density-dependent mechanism reducing growth (L1) and fecundity (DSF) at higher fish densities; (2) higher fish condition (K-n) positively affecting growth (L1); (3) higher prey availability (mesozooplankton concentration) positively affecting GSI. This time series and approach are promising for exploring the abiotic and biotic mechanisms setting year class strength in advance of recruitment to the fishery.
AbstractConventional observations show spiny dogfish (Squalus acanthius Linnaeus) rarely eat Atlantic cod (Gadus morhua Linnaeus; 0.02% of stomachs) in the northwestern Atlantic Ocean. Critics express concern that digestion may limit species‐level prey identification, and with recovery from overfishing, dogfish populations may be suppressing cod by competition or predation. This study applied a real‐time PCR TaqMan assay to identify cod in dogfish stomachs collected by cooperating fishing boats during normal trawling operations (May 2014–May 2015; Gulf of Maine, Georges Bank). Conventional methods observed 51 different prey taxa and nearly 1,600 individual prey items, but no cod were observed. Cod DNA was detected in 31 (10.5%) of the dogfish stomachs, with a higher percentage of these from the homogenate of amorphous, well‐digested prey and stomach fluids (20 stomachs or 65%) than from discrete animal tissues (11 stomachs or 35%). Re‐examination of photographs of these 11 tissue samples revealed one whole, partially digested fish that could be recognized in hindsight as cod. Cod DNA was observed in dogfish stomachs year round: in January (1 of 1 trip), February (1 of 1), May (1 of 3), June (0 of 1), July (3 of 4), August (1 of 2), and October (3 of 3). Although these data suggest higher interaction rates between dogfish and cod than previously observed, addressing the population consequences of this predator–prey relationship requires a robust sampling design, estimates of digestion rates by dogfish to account for complete degradation of DNA sequences, and consideration for dogfish scavenging during fishing operations.
The circumglobal ocean sunfishes, Molidae (specifically Mola spp.), have long held the record for being the world's most fecund vertebrates. This record is based on one 1.5m individual whose ovary was estimated to contain 300 million "small and unripe" ova (Schmidt 1921). Few data have been available to assess this claim of reproductive prowess since large gravid sunfishes (>1.5m TL) are rarely encountered and ways of describing fecundity are not standardized. This chapter reviews our current knowledge of sunfish reproduction and proposes an assessment of fecundity in terms of productivity. It offers additional insight through the histological examination of samples collected from geographically disparate regions including California and Japan, the east coast of the USA, and the Mediterranean (Italy and Portugal). Ovaries at different stages of sexual maturity from two different species of molid are examined--M. mola (35.5cm - 2.9m TL) and M. tecta (2.15m TL). From Kamogawa Japan, three additional large female Mola spp. (2.10m, 2.43m and 2.72m TL) are described along with the first known molid egg release from a 1m TL captive female at Kamogawa SeaWorld. A new record of 847 million ova in a single female (2.2m total length) is presented. Lastly, future research directions are detailed and discussed.
Winter flounder, Pseudopleuronectes americanus, were collected from three fishery stocks in the United States (U.S.) during 2009-2013 to describe spermatogenesis. Spermatogenesis included rapid, synchronous transitions during autumn from mitotic spermatogonia to meiotic spermatocytes, then to haploid spermatids, and the release of spermatozoa into lobule lumen. As these transitions occurred several months prior to the spring spawning season, maturity of the testes are a poor indicator of spawning season, however, individuals can be readily evaluated prior to the spawning season for evidence of skipped spawning. Throughout this process, the gonad weight increased dramatically, with spawning-season maxima from 11 to 17% relative to individual somatic weight, suggesting considerable reproductive investment relative to other flatfishes. Fish condition also cycled seasonally, which indicated that males follow a capital breeding pattern that has been reported for female winter flounder. The timing of spermiogenesis was very similar in the fish among each U.S. stock (Southern New England [SNE], Georges Bank [GB], and the Gulf of Maine [GOM]) and published data from coastal Newfoundland, even though U.S. winter flounder spawned earlier in spring than fish in the Canadian stock. Male maturity varied in relation to both size and age, and over time, in patterns similar to those reported for female winter flounder, but at smaller and younger sizes than females. These intra-specific variations in reproductive seasonality, maturation, and skipped spawning suggest that winter flounder have the potential to adaptively respond to a dynamic environment in a region where ocean warming is occurring rapidly.
Measuring fish condition should link ecosystem drivers with population dynamics, if the underlying physiological basis for variations in condition indices are understood. We evaluated traditional (K, Kn, hepatosomatic index, gonadosomatic index, energy density, and percent dry weight of muscle (%DWM) and liver (%DWL)) and newer (bioelectrical impedance analysis (BIA) and scaled mass index (SMI)) condition indices to track seasonal cycles in three flatfishes — winter founder (Pseudopleuronectes americanus; three stocks), yellowtail flounder (Limanda ferruginea; three stocks), and summer flounder (Paralichthys dentatus; one stock) — with contrasting life histories in habitat, feeding, and reproduction. The %DWM and %DWL were good proxies for energy density (r2 > 0.96) and more strongly related to K, Kn, and SMI than to BIA metrics. Principal component analysis indicated many metrics performed similarly across species; some were confounded by size, sex, and maturity along PC1, while others effectively characterized condition along PC2. Stock differences were along PC1 in winter flounder, reflecting different sizes across stocks, whereas in yellowtail flounder differences occurred along PC2 related to condition. These comparisons, within and across species, highlight the broad applicability of some metrics and limitations in others.
Environmental DNA (eDNA) metabarcoding was used to characterize finfish communities in the nearshore estuarine environment. Monthly sampling was conducted June - August 2017 at two sites with structured habitats: a natural rock reef and a shellfish aquaculture farm within the same coastal embayment of Long Island Sound, CT, USA. Seventeen common and 25 rare finfish taxa were detected using eDNA metabarcoding. Incomplete status of reference sequence databases for finfish species was identified as a methodological challenge. Confidence in molecular identification was improved appreciably through the use of publicly-available data obtained from local trawling and seining surveys. Comparison between eDNA metabarcoding and trawling surveys on 6/27/2017, the only day when both data types were available, revealed more finfish species detected by eDNA metabarcoding. The high sensitivity of eDNA metabarcoding detected finfish species rarely observed in traditional surveys and showed the potential for this methodology to augment existing literature for finfish species distribution patterns and invasive species detection. Non-metric multidimensional scaling (NMS) analysis of finfish communities achieved a low-stress, 2D solution, and revealed greater variation between samples collected from different months than samples collected from the two habitats. Similarly, permutational analysis of variance (PERMANOVA) found both month and the interaction term (month x site) significant, with the latter identifying site as significant only in July and August. Different finfish assemblages were significantly associated with each axis, axes representing temporal and spatial variations, respectively. Additionally, polycarbonate and nylon filters were compared to optimize the sampling method; finfish communities retrieved using the 2 types of filters were statistically indistinguishable by NMS analysis, although the filtration time for nylon filters was shorter. If the objective is to detect rare species, nylon filters are recommended over polycarbonate filters because of higher capture rates of rare taxa. Our study demonstrates the potential for applying eDNA metabarcoding as a stand-alone method to conduct finfish surveys with high sensitivity.
Understanding drivers of fish maturity are essential to predict the productivity, stability, and resiliency of exploited populations. In terms of horse mackerel (Trachurus trachurus), in the eastern Atlantic Ocean and the Mediterranean Sea, size at maturity estimates date back to the 1940s and throughout its range. However, many older estimates may not reflect current maturity rates. This is because past methods were imprecise, or environmental or fishing effects may change maturity rates, and some stock areas have been overlooked. To address this data gap for the Central Mediterranean Sea, female horse mackerel size at maturity was estimated for two areas: the Strait of Sicily and the Tyrrhenian Sea. All ovaries were assigned a reproductive phase based on macroscopic methods, and the reliability of this method (94%) was validated with a microscopic method (i.e., gonad histology). Although the collected females exhibited similar condition, in terms of total body weight at a given length, as well as similar gonad-somatic indices, the size at median maturity in the Strait of Sicily was smaller (161 mm total length [TL]) than in the Tyrrhenian Sea (176 mm TL). Future sampling in a series of years with contrasting levels of productivity may help identify whether this is a broad latitudinal trend, or due to specific oceanographic drivers, such as estuarine outflow into the Tyrrhenian Sea or upwelling in the Strait of Sicily. Meanwhile, resource assessments should consider that these two areas represent two phenotypic stocks.
The black sea bass (Centropristis striata) is extending its range northward, into a warming Gulf of Maine. Here, we plot the geographic distribution of specific life stages to examine whether spawning and settlement, and therefore productivity, are extending northward. In order to align these life stages with the correct sampling season, we first resolve confusion about the spawning seasonality of this species, by collecting age-0 individuals from coastal waters of southeastern Massachusetts (Buzzards Bay and Nantucket Sound) and aging them by using daily otolith microincrements. Wild-caught age-0 fish (n=381), ranged in size from 32 to 88 mm total length (mean: 53 mm [standard deviation (SD) 11]), and in age from 50 to 129 d old (84 d [SD 16]). They hatched from May 2 to July 21 (June 6 [SD 14 d]), and grew at linear rates from 0.32 to 1.22 mm/d (0.65 mm/d [SD 0.15]). The literature and two 40-year trawl surveys confirm that black sea bass have spawned in Buzzards Bay and Nantucket Sound since the 1880s. Farther north, in the southern Gulf of Maine, spawning has likely occurred in the last 15 years. Settlement has increased about 1 degrees N latitude over the recent 4 decades in association with warming sea temperatures in the southern Gulf of Maine.
The spotted seatrout, Cynoscion nebulosus (Cuvier, 1830), lives almost entirely within natal estuaries, and although many genetic studies identify fine-scale population structure, they do not provide a consensus as to the number of stocks, the stock boundaries, or their connectivity. Two perceived limitations of previous studies were addressed. To address a presumption of limited sampling, we assembled a large sample size with broad geographic range: 547 specimens from 18 sampling areas (mean inter-area distance = 270 km) between Texas and North Carolina, representing the majority of this species' range. To address the presumptive limitations of genetic markers, two genetic marker types were compared: a 335-base-pair segment of the mitochondrial DNA (mtDNA) control region and 38 microsatellite loci. MtDNA haplotype frequencies were different only between populations of the Gulf of Mexico (GoM) and the Atlantic Ocean, but not between the western GoM and the eastern GoM. In contrast, the microsatellite loci characterized the species' range-wide population structure as three geographically non-overlapping clusters. These clusters were defined by two genetic breaks: one at the Apalachicola River, on Florida's Gulf Coast, and another in the Atlantic Ocean between Miami and Palm Beach on Florida's east coast. Moreover, within each genetic cluster (identified by microsatellite markers), a pattern of isolation by distance was evident. This new characterization of spotted seatrout population structure supports assessment and management of the species by individual states and defines distinct stock boundaries in Florida, the only state with multiple genetic stocks, as defined by either genetic marker type.
Sheepshead, Archosargus probatocephalus (Walbaum, 1792), have long been separated into three subspecies based on meristic traits, particularly counts of pigmented bars on the sides of the body. Here, we evaluate sheepshead genetic variation both mtDNA and microsatellite in the domain of the two morphologically defined subspecies, Archosargus probatocephalus probatocephalus and Archosargus probatocephalus oviceps. Sheepshead were collected in coastal habitats of the southeastern United States, from North Carolina (Atlantic Ocean) to Texas (Gulf of Mexico). Significant variations in the mtDNA control region data indicated that the sheepshead is divided into two populations by a genetic break originating somewhere between Apalachicola (Florida gulf coast) and Indian River (Florida Atlantic coast), leaving a wide margin of uncertainty as to the exact area of the division. However, use of species-specific microsatellite markers revealed that the sheepshead is geographically structured by two genetic breaks into three population clusters. The first genetic break occurs at Apalachee Bay, close to the boundary between the two morphologically defined subspecies (i.e., between Apalachicola and Steinhatchee, on Florida's gulf coast). The second genetic break occurs off south Florida (Atlantic Ocean), where it coincided with a discontinuity of estuarine habitat between Miami and Palm Beach that likely impedes gene flow between populations. This second genetic boundary had been unrecognized for sheepshead, although it has been widely recognized as a genetic boundary for many other nearshore fish species in the southeastern United States.