Applications of SABRE to research and management

In this paper, we highlight the major results from the SABRE programme and applications to research and management. In particular, SABRE provided new scientific insights into the fisheries oceanography of the estuarine-dependent fishes of the South Atlantic Bight. Although we concentrated our efforts on Atlantic menhaden, we also gained insights on the coupling of physics to biology in the early life history of a number of marine fishes. Larval transport from spawning sites to and through barrier island inlets is now better understood. Analysis of menhaden population dynamics suggests survival in the late larval/early juvenile stage is particularly important to population growth. This phase of the life history appears likely to present a bottleneck to recruitment for Atlantic menhaden. We also made a number of technological breakthroughs which are already being applied elsewhere in research and assessments including the Continuous, Underway Egg Sampler (CUFES), enzyme-based approaches to evaluating condition of individual larvae and various physical and biological modelling innovations. Our experiences establishing and managing the SABRE research team also provide insights into one model for promoting multidisciplinary research in fisheries oceanography. Throughout SABRE, we have sought an open exchange of information and insights from a wide variety of researchers and environmental managers. We hope the synthesis provided here continues that dialogue.     

Atlantic menhaden recruitment to a southern estuary: defining potential spawning regions

Atlantic menhaden ( Brevoortia tyrannus ) is an estuarine-dependent fish that spawns in coastal waters of the Middle and South Atlantic Bights. Circulation modelling studies of larval transport suggest that recruitment of larvae into the Albemarle-Pamlico Estuarine System, North Carolina, is linked to dynamics on the shelf from New York to South Carolina. Field-collected menhaden egg data (from MARMAP and SABRE) define a range of temperatures within which menhaden eggs have been found. In this study we refine the transport model-predicted spawning grounds for the 1994–95 season by using satellite-derived sea surface temperature data to highlight regions that are outside the observed spawning temperature range. We also use transport pathways leading from source locations to the estuarine system to characterize the temperature field experienced by particles/larvae during their spawning-ground to inlet transit. The modelled nearshore location of source regions agrees well with MARMAP and SABRE egg data, and points to the importance of understanding biological and physical linkages between the Middle and South Atlantic Bights. The combination of modelled transport and synoptic temperature maps can provide useful guidance to future sampling efforts as well as help refine our understanding of menhaden ecology.     

From spawning grounds to the estuary: using linked individual-based and hydrodynamic models to interpret patterns and processes in the oceanic phase of Atlantic menhaden Brevoortia tyrannus life history

Present theory suggests that population regulation in marine fishes cannot be resolved until an understanding of the processes involved in shaping the overall distribution (the number of populations, geographical extent, mean abundance and temporal changes in abundance) is developed. Here, we present a step toward understanding Atlantic menhaden population patterns, by studying processes in the Middle and South Atlantic Bights, which shape those patterns. We use individual-based and hydrodynamic models to reinterpret the 'mechanics' of the menhaden life history, and put forward several potentially testable hypotheses. The success of the menhaden reproductive strategy seems to depend on the seasonal changes in the mean flow field of the Middle and South Atlantic Bights, suggesting that their life history may have been strongly structured by the regional physics of the system. Because the annual menhaden migration is size-based and spawning occurs throughout the population's range, the size distribution of the adult population may influence the supply of larvae to particular estuaries along the coast. Recruitment of larvae into Delaware and Chesapeake Bays may be dependent on spawning to the north of the bays' mouths, owing to coastline shape and orientation in the vicinity of the bays. Our results suggest that management of this resource might be improved by consideration of the spatial and temporal variability in both the biological and the physical system.     

Ecosystem‐based forecasts of recruitment in two menhaden species

Gulf (Brevoortia patronus, Clupeidae) and Atlantic menhaden (Brevoortia tyrannus, Clupeidae) support large fisheries that have shown substantial variability over several decades, in part, due to dependence on annual recruitment. Nevertheless, traditional stock–recruitment relationships lack predictive power for these stocks. Current management of Atlantic menhaden explicitly treats recruitment as a random process. However, traditional methods for understanding recruitment variability carry the very specific hypothesis that the effect of adult biomass on subsequent recruitment occurs independently of other ecosystem factors such as food availability and predation. Here, we evaluate the predictability of menhaden recruitment using a model‐free approach that is not restricted by these strong assumptions. We find that menhaden recruitment is predictable, but only when allowing for interdependence of stock with other ecological factors. Moreover, while the analysis confirms the presence of environmental effects, the environment alone does not readily account for the complexity of menhaden recruitment dynamics. The findings set the stage for revisiting recruitment prediction in management and serve as an instructive example in the ongoing debate about how to best treat and understand recruitment variability across species and fisheries.     

Physical oceanography of the North Carolina continental shelf during the fall and winter seasons: implications for the transport of larval menhaden

The circulation over the continental shelf off the southern Middle Atlantic Bight (MAB) and northern South Atlantic Bight (SAB) is examined for the fall and winter periods. Observational data are compared with results from a three-dimensional numerical model to identify the dominant processes on the shelf. By considering wind-forcing, tides, and a specified upstream inflow (into the MAB), the observed and modelled flow fields are in close agreement in the mid- and inner shelf regions. The resulting larval drift indicates a seasonal dependence of transport pathways from spawning grounds to estuarine nursery areas for menhaden larvae and other offshore-spawning estuarine-dependent fish. Specifically, the physical oceanography of the MAB and SAB during the fall and winter months suggests a north-to-south shift in spawning areas providing recruits to the Carolina estuaries, in agreement with the observed migration of the spawning populations.     

Physical oceanography of the North Carolina continental shelf during the fall and winter seasons: implications for the transport of larval menhaden

The circulation over the continental shelf off the southern Middle Atlantic Bight (MAB) and northern South Atlantic Bight (SAB) is examined for the fall and winter periods. Observational data are compared with results from a three-dimensional numerical model to identify the dominant processes on the shelf. By considering wind-forcing, tides, and a specified upstream inflow (into the MAB), the observed and modelled flow fields are in close agreement in the mid- and inner shelf regions. The resulting larval drift indicates a seasonal dependence of transport pathways from spawning grounds to estuarine nursery areas for menhaden larvae and other offshore-spawning estuarine-dependent fish. Specifically, the physical oceanography of the MAB and SAB during the fall and winter months suggests a north-to-south shift in spawning areas providing recruits to the Carolina estuaries, in agreement with the observed migration of the spawning populations.     

Atlantic coast feeding habits of striped bass: a synthesis supporting a coast-wide understanding of trophic biology

The recent increase in the Atlantic coast population of striped bass, Morone saxatilis (Walbaum), prompted managers to re‐evaluate their predatory impact. Published and unpublished diet data for striped bass on the Atlantic Coast of North America were examined for geographical, ontogenetic and seasonal patterns in the diet and to assess diet for this species. Diets of young‐of‐the‐year (YOY) striped bass were similar across the Upper Atlantic (UPATL), Chesapeake and Delaware Bays (CBDEL) and North Carolina (NCARO) areas of the Atlantic coast where either fish or mysid shrimp dominate the diet. For age one and older striped bass, cluster analysis partitioned diets based on predominance of either Atlantic menhaden, Brevoortia tyrannus (Latrobe), characteristic of striped bass from the CBDEL and NCARO regions, or non‐menhaden fishes or invertebrates, characteristic of fish from the UPATL, in the diet. The predominance of invertebrates in the diets of striped bass in the UPATL region can be attributed to the absence of several important species groups in Northern waters, particularly sciaenid fishes, and to the sporadic occurrences of Atlantic menhaden to UPATL waters. In all regions, across most seasons and in most size classes of striped bass, the clupeiod fishes; menhaden, anchovies (Anchoa spp.) and river herrings (Alosa spp,) and Atlantic herring, Clupea harengus L., dominated the diets of striped bass above the first year of life.     

Searching for sensitivity in the life history of Atlantic menhaden: inferences from a matrix model

We used modified Leslie matrix models to explore the life history of Atlantic menhaden ( Brevoortia tyrannus ). By examining the sensitivity of long-term population growth rates to changes in vital rates, we identified those life history components which can cause large population level responses. Our models subdivide the first year of life into five stages (eggs, early larvae, late larvae, juveniles, and 'peanuts' or subadults), and population growth rate responds most strongly to changes in juvenile and late larval stages. The relative ranking between these stages is dependent on the magnitude of mortality during the prejuvenile stages relative to juvenile mortality. An examination of low-level model parameters indicates that the population growth rate is influenced by the growth and mortality rates during the time when young-of-the-year menhaden are gaining access to and residing in the estuaries. Sensitivity to changes in many adult metrics, such as fishing mortality, were relatively low. We conclude that a better understanding of biotic and abiotic factors that influence the late larval and juvenile stages will further our understanding of population dynamics in this species.     

Vertical distribution of larval Atlantic menhaden (Brevoortia tyrannus) and Atlantic croaker (Micropogonias undulatus): Implications for vertical migratory behaviour and transport

Understanding the interactions among biological and physical processes is essential to determining how the environment affects transport and survival of fishes. We examined vertical distribution in larval Atlantic menhaden (Brevoortia tyrannus) and Atlantic croaker (Micropogonias undulatus) using 126 depth stratified tows in Delaware Bay, USA, during two cruises, in December 2007 and February 2008. Menhaden larvae were 16.8–24.6 and 20.5–26.2 mm standard length in December and February. Corresponding lengths for croaker were 9.3–17.9 and 8.6–19.6 mm. Using empirical observations, and statistically derived models, we explored larval concentration for both species as a function of location, depth, diel period, tidal period, size, and pairwise interactions. Menhaden concentration was best modeled as a function of station, cruise, and interactions between depth and size as well as between station and cruise. No significant differences in larval menhaden concentration were present among tidal and diel periods. Croaker concentration was best modeled as a function of size and interactions between station and diel period, depth and size, cruise and size. Despite tidal period not emerging as a significant model parameter, we observed larger croaker larvae during nighttime flood tides. Our statistical models are consistent with processes of up‐estuary transport for both species, suggesting larvae are increasingly affected by behavioral responses as larvae grow, exhibiting stronger patterns in vertical distribution. The results refine our understanding of the potential importance of size‐related differences in vertical distribution for larval transport in these species. Future research should examine the interactions among size‐specific vertical migratory capabilities, vertical distribution, transport, and retention.     

Common trends in recruitment dynamics of north‐east Atlantic fish stocks and their links to environment,ecology and management

Recruitment dynamics are challenging to assess or predict because of the many underlying drivers that vary in their relevance over time and space. Stock size, demographic and trait composition, condition and distribution of spawning fish and the spatio‐temporal dynamics of trophic and environmental interactions all influence recruitment processes. Exploring common patterns among stocks and linking them to potential drivers may therefore provide insights into key mechanisms of recruitment dynamics. Here, we analysed stock‐recruitment data of 64 stocks from the north‐east Atlantic Ocean for common trends in variation and synchrony among stocks using correlation, cluster and dynamic factor analyses. We tested common trends in recruitment success for relationships with large‐scale environmental processes as well as stock state indicators, and we explored links between recruitment success and demographic, environmental and ecological variables for a subset of individual stocks. The results revealed few statistically significant correlations between stocks but showed that underlying common trends in recruitment success are linked to environmental indices and management indicators. Statistical analyses confirmed previously suggested relationships of environmental–ecological factors such as the subpolar gyre and Norwegian coastal current with specific stocks, and indicated a large relevance of spawning stock biomass and demographics, as well as predation, whereas other suggested relationships were not supported by the data. Our study shows that despite persistent challenges in determining drivers of recruitment due to poor data quality and unclear mechanisms, combining different data analysis techniques can improve our understanding of recruitment dynamics in fish stocks.     

Spawning and transport dynamics of Atlantic menhaden: inferences from characteristics of immigrating larvae and predictions of a hydrodynamic model

We examined patterns of abundance, age and spawning date distributions of Atlantic menhaden Brevoortia tyrannus larvae immigrating during two seasons through three North Carolina inlets—Oregon, Ocracoke and Beaufort—to elucidate their spawning and transport dynamics. These patterns were examined in conjunction with corresponding predictions from a three-dimensional, wind-and tide-driven hydrodynamic model. Larvae immigrating through different inlets showed consistent similarities as well as marked differences in temporal patterns of abundance, spawning dates and transport times. Intraseasonal patterns in abundance and spawning date distributions among inlets suggest that, in both study years, the spatio-temporal dynamics of menhaden immigration were driven by large-scale patterns along the Atlantic coast, rather than by localized variation in spawning activity. Interannual differences in the temporal patterns of spawning dates and larval immigration indicate interannual differences in transport dynamics and/or the spatial-temporal distribution of spawning. When the spawning locations predicted by the hydrodynamic model are interpreted in conjunction with advanced very high resolution radiometer sea-surface temperature information, the results are consistent with the limited historical information available on spatio-temporal distribution of Atlantic menhaden eggs and larvae. The transport model also predicted distributions of arrival times for immigrating larvae that were comparable in range and variability with observed patterns. Our use of data from immigrating larvae, coupled with a hydrodynamic transport model and sea-surface temperatures, allowed us to uncover relationships between spatio-temporal patterns of Atlantic menhaden spawning and transport dynamics that could not have been identified by either approach alone.     

A viral aetiology for the annual spring epizootics of Atlantic menhaden Brevoortia tyrannus (Latrobe) in Chesapeake Bay

Abstract. Virus was isolated from the brain and pancreatic tissues of Atlantic menhaden with 'spinning' disease. The biological, physical and chemical properties of the isolate were similar to those of infectious pancreatic necrosis virus. Inoculation of the virus into healthy menhaden resulted in the characteristic signs and mortality associated with the natural disease.     

Predator–prey analysis of striped bass and Atlantic menhaden in upper Chesapeake Bay

Between 1997 and 2000, an outbreak of skin lesions and observations of emaciated striped bass, Morone saxatilis (Walbaum), in upper Chesapeake Bay were attributed to a perceived shortage of its main prey, Atlantic menhaden, Brevoortia tyrannus Latrobe. Abundance estimates, Atlantic menhaden consumption per recruit analysis (modified yield‐per‐recruit), bioenergetics analysis and predator–prey theory were combined to explore whether an imbalance between striped bass and Atlantic menhaden in upper Chesapeake Bay was plausible. Reduced fishing mortality and higher size limits that underpinned the effort to restore striped bass during the 1980s and 1990s lead to more abundant and larger striped bass in upper Chesapeake Bay, increasing predatory demand for forage‐sized Atlantic menhaden, the abundance of which declined to a historic low. Nominal losses of age 0–2 Atlantic menhaden to harvest and potential striped bass predation exceeded supply after 1998. The outbreak of lesions in upper Chesapeake Bay striped bass coincided with increased variation in weight‐at‐length, decreased length‐at‐age, and decreased presence of Atlantic menhaden in diets. Decreased attack success, inferred from a 97% decline in ratios of forage‐sized Atlantic menhaden to striped bass between 1983 and 1998, would have expected to have been followed by a deterioration of striped bass nutritional state. Transmission of disease would have been aided by high density of striped bass in poor nutritional condition residing in degraded habitat (Chesapeake Bay was the most hypoxic estuary in the mid‐Atlantic region in the late 1990s). These problems suggest that striped bass exceeded their carrying capacity in Chesapeake Bay during the late 1990s.     

Evidence for atmosphere–ocean forcing of yellowtail flounder (Limanda ferruginea) recruitment in the Middle Atlantic Bight

We investigated the relationship between large-scale climate variability (the North Atlantic Oscillation, NAO), continental shelf hydrography, and year-class strength of yellowtail flounder (Limanda ferruginea) in the Middle Atlantic Bight. Using long-term environmental time series (1963–98), dominant winter NAO phase in the northeast region of the United States was correlated with local air temperature records from Block Island, Rhode Island (December–March). Air temperature also influenced the characteristics of a pool of remnant winter cold water on the continental shelf, such that negative NAO winters produced a colder-than-average summer cold pool, and vice versa. Smoothed data sets of L. ferruginea recruitment over the 36-yr period (using Southern New England VPA and hindcast data) were highly correlated with the NAO and air temperature, highlighting the influence of multi-year variability. Although less robust, the relationship with the NAO remained significant after removing equal-but-opposite long-term linear trends from the series. Surprisingly, recruitment and cold pool bottom temperature were only marginally correlated. Data from independent 2-m beam trawl and submersible sampling in the region (1994, 1996–2000) indicated a strong relationship between the abundance of recent settlers and cold pool temperature; however, this pattern was often modified by subsequent changes in cold pool stratification (fall overturn). These results underscore the dynamic role thermal habitats play in the lives of early stage benthic fishes. For yellowtail flounder, the generation of recruitment variability represents one endpoint of a complex interaction between large-scale phenomena (climate) and more localized, event-scale features (cold pool).     

Tracking shifts in Atlantic mackerel (Scomber scombrus) larval habitat suitability on the Northeast U.S. Continental Shelf

Climate change has altered the oceanographic environment and subsequently the habitats of marine species. Fish and invertebrate populations’ responses to habitat include movement with latitude and depth to remain within their fundamental niches. The northwest Atlantic mackerel (Scomber scombrus) population has fluctuated over the last century due in part to changes in the environment. We used species distribution models to understand the influence of the physical (temperature) and biological (zooplankton) environment on mackerel larval abundance, and how such relations have determined larval habitat suitability in the Northeast U.S. Shelf. Atlantic mackerel larval presence and abundance correlated with sea temperature and copepod abundances, suggesting that larval survival may be sensitive to specific temperatures and zooplankton prey. Predicted abundances were spatially interpolated to estimate Atlantic mackerel larval suitable habitat. Metrics for habitat quality indicate that the Mid‐Atlantic Bight has become less suitable over time. Since the 1970s, the proportion of Northeast U.S. Shelf suitable habitat located in the Mid‐Atlantic Bight has decreased, as southern New England and the western Gulf of Maine regions have become more suitable. Habitat suitability within the Northeast U.S. Shelf has shifted northeast: from the Mid‐Atlantic Bight‐southern New England border towards the northeast portion of southern New England. While total Northeast U.S. Shelf habitat suitability has decreased since the 1970s, the decline in the time series trend was not statistically significant. Thus, while select ecoregions have decreased in habitat suitability, larval habitat does not appear to be the only contributor to decreases in the U.S. Atlantic mackerel contingent.     

Oocyte recruitment and fecundity type in fishes: Refining terms to reflect underlying processes and drivers

Only with new technology and the ability to simulate systems are we beginning to understand fish reproductive processes at the individual scale over time. Traditionally, oocyte recruitment and fecundity type in fishes have been based on a “snapshot” approach, that is a histological micrograph and/or oocyte size frequency distribution of a spawning capable female has been assumed to indicate oocyte recruitment processes over time. This has important implications as the asynchronous and group‐synchronous oocyte recruitment patterns are associated with indeterminate and determinate fecundity types, respectively, and thus affect estimates of reproductive potential and spawning biomass (if using egg production methods). However, a historic review of these terms revealed that they are not applied consistently, with the same oocyte recruitment pattern often assigned to both of these by different scientists. The intent of this study is to develop a conceptual model of oocyte recruitment processes over time, key drivers, and resulting “snapshots” to refine oocyte recruitment terms, definitions, and the methods needed to identify them.     

The diet of Chesapeake Bay striped bass in the late 1950s

The diet of Chesapeake Bay striped bass, (Morone saxatilis) Walbaum, based on unpublished stomach content data from 916 fish collected between 1955 and 1959 was described. The diet in the late 1950s, quantified using an index of relative importance (IRI), was dominated by Atlantic menhaden, Brevoortia tyrannus Latrobe. Atlantic menhaden (66%) and bay anchovy, Anchoa mitchilli Valenciennes, (19%) had the highest IRI value overall. Small striped bass (<600 mm total length) ate predominantly bay anchovy (IRI = 67%). Large striped bass (≥ 600 mm total length) ate predominantly Atlantic menhaden (IRI = 93%). Since 1990 small striped bass rely more on invertebrate prey and larger fish now rely more on small pelagic prey, such as bay anchovy and 0‐age clupeids. Analysis of historical data using current techniques provided a valuable tool for comparison to help in understanding the current striped bass predator–prey relationship in Chesapeake Bay.     

Seasonal dynamics of fish assemblage in a pond canal

The annual dynamics of fish assemblage in a pond-connecting canal of a South Moravian pond aquaculture facility was studied to reveal potential assemblage effects on pond stocks and vice versa. The species richness of fish assemblage and seasonal dynamics of its development were predominantly dependent upon the fish stock of the interconnected ponds (particularly due to escapees during the period of pond harvesting), which contributed to a considerable increase of commercial fish species occurrence. Using a seasonal parameter, the season proved to have a major impact on fish assemblage dynamics (r = −0.71, P < 0.001). Spring samples were dominated by commercial fishes of aquaculture origin (mainly Cyprinus carpio). Occurrence of several fish species originating from the wild (bleak, Alburnus alburnus, chub, Leuciscus cephalus and roach, Rutilus rutilus) was also reported. The pond canal was found to be an important reservoir site of persistent survival and potential subsequent spreading of some undesirable alien fishes such as topmouth gudgeon (Pseudorasbora parva) and gibel carp (Carrasius auratus). Moreover, more attention should be paid to the potential negative impacts of all fishes of aquaculture origin upon the natural ecosystem and to the adverse effects due to the immigration of wild fish into aquaculture pond farming units.     

Eulerian views of layered water currents, vertical distribution of some larval fishes, and inferred advective transport over the continental shelf off North Carolina, USA, in winter

Currents that effect the shoreward transport of the larvae of estuarine-dependent fishes spawned in winter in Onslow Bay, North Carolina, USA, were driven by winds and pressure gradients, and influenced by the Gulf Stream. Aside from storms, winds over the continental shelf in Onslow Bay blew predominantly alongshore with velocities approaching 14 m s^-1 during February and March 1986, and January and February 1989. Water masses and currents observed at two current-meter moorings, one at mid-shelf and the other on the outer shelf, reflected the onshore (or offshore) advection of interior water in compensation for the offshore (or onshore) advection of wind-driven surface water. Winds and currents reversed direction approximately every 4 to 6 days. The larvae of Atlantic menhaden, Brevoortia tyrannus , spot, Leiostomus xan- thurus, and Atlantic croaker, Micropogonias undulatus , were most abundant in 17–19^oC and 20–21^oC water of the outer shelf and Gulf Stream fronts. There was little indication of diel vertical migration; larval Atlantic menhaden were most abundant in mid- and surface water, while spot and Atlantic croaker were most abundant in mid- and deep water. Given this distribution, the inferred advective transport of larvae was at times onshore, but at other times it was offshore. Within a spawning season, the prevalence of either reciprocation could determine the number of larvae that reach coastal inlets.     

A continuous, underway fish egg sampler

We describe a method to sample the highly contagious distribution of pelagic fish eggs. CUFES, the continuous, underway fish egg sampler, consists of a submersible pump, concentrator, electronics and sample collector. This system operates continuously and under nearly all sea conditions, providing a real-time estimate of the volumetric abundance of pelagic fish eggs at pump depth, usually 3 m. CUFES-derived estimates of volumetric abundance agree well with those from nets towed at pump depth and with areal abundance estimated from vertically integrated plankton tows. CUFES has been used successfully to sample the eggs of menhaden, pinfish, sardine, and anchovy off the coasts of the eastern and western United States and South Africa. Two large patches of eggs of the Atlantic menhaden were sampled off North Carolina in winter 1993–94, had a linear scale of 5–10 km, and were found in waters between the Gulf Stream and mid-shelf front. Spawning location may be related to bathymetry. CUFES is now being used to estimate spawner biomass by the daily egg production method. An optical plankton counter provided accurate estimates of the number of Atlantic menhaden eggs sample by CUFES.