Effect of hypoxia on the gulf fishery and implications for stock assessment

Amy M. Schueller, J. Kevin Craig, Kyle W. Shertzer, and Joseph W. Smith Beaufort Laboratory, Southeast Fisheries Science Center

Background: River-dominated coastal ecosystems have particularly productive fisheries due to external nutrient subsidies from coastal watersheds that enhance primary productivity at the base of marine food webs (Breitburg et al. 2009). However, nutrient over-enrichment often leads to low dissolved oxygen (DO), or hypoxia (DO ≤ 2.0 mg l-1), that can have a variety of negative consequences for marine species. The number of coastal ecosystems reporting hypoxia has doubled each decade since the 1960s (Diaz and Rosenberg 2008), reflecting a global increase in the severity of marine eutrophication, yet elucidating the consequences for fish populations and the implications for fisheries management has been difficult. Two fundamental pathways exist by which hypoxia can affect fisheries. First, hypoxia can influence biological production that determines the amount of a targeted species potentially available for harvest. Effects of hypoxia on processes underlying production (e.g., growth, survival, reproduction) have been extensively studied, though the population-level consequences are often unclear (Rose et al. 2009). Second, hypoxia can influence the fishery sector itself through effects on the behavior of fishermen and the dynamics of fishing fleets. These effects are less well known but potentially important, because the primary effect of hypoxia is often a shift in the spatial distribution of target species that can influence harvest. For example, short- term (e.g., within season) responses of a shrimp fleet to estuarine hypoxia led to annual declines in shrimp harvest of ~ 13% and induced growth of the stock (Huang et al. 2010ab). In general, there is a recognized need to incorporate information on fisher behavior and fleet dynamics into fisheries assessment models and management decisions, but the empirical basis to do so is typically lacking (Wilen et al. 2002, Branch et al. 2006). The northwestern Gulf of Mexico continental shelf currently experiences the largest seasonal hypoxic zone in the western hemisphere (Rabalais et al. 2002). The hypoxic zone is located at the terminus of the Mississippi- Atchafalaya river system, which drains 41% of the continental United States, and extends along the inner Louisiana shelf (< 30 m depth), sometimes reaching the north Texas DO ≤ 2 mg l-1 100 km shelf (Fig .1). Hypoxia is most Menhaden set pronounced in the bottom waters, but can sometimes extend over 80% of the water column, and it is most severe during summer (Jun-Aug). Mapping surveys since the mid-1980s indicate considerable annual variability in the spatial extent of Fig.1 (Top) Composite map of the hypoxic zone (1983-2010). 2 hypoxia, ranging from < 100 km to > (Bottom) Menhaden set locations (2006-2007). 2

22,000 km2 (Rabalais et al. 2002, Turner et al. 2008). Evidence from paleo-studies and hindcasting models indicates increasing oxygen stress since the early 1900s, with hypoxia becoming more severe beginning in the 1960s to 1970s (Justic et al. 2007, Rabalais et al. 2007a). The area of the Louisiana shelf that currently experiences hypoxia is within a region called the “fertile fishery crescent” that has historically supported the highest biomass of fish and crustaceans in the northwestern Gulf (Gunter 1963). The fishery operates within this region (from western Alabama to eastern Texas) with > 90% of the catch taken off the Louisiana coast within 10 miles of the shoreline (Fig. 1, Vanderkooy and Smith 2011). Annual recruitment of gulf menhaden is correlated with river discharge, indicating a coupling between processes in the watershed and menhaden production (Vaughan et al. 2011). The fishing season extends from mid-April to early November with peak landings from June to August, which is also the period when hypoxia is typically most severe. In terms of volume, the gulf menhaden fishery is the largest in the Gulf and among the largest in the United States, averaging about 447,000 metric tons annually during 2005−2009 with an ex-vessel value of about $58.5 million. Gulf menhaden, although susceptible to low DO, probably move out of hypoxic areas, resulting in displacement, rather than mortality. Based on long-term data from menhaden logbooks, Smith (2001) suggested that exceptionally low catches of gulf menhaden off the central Louisiana coast in some years may have been the result of hypoxic waters impinging on the shoreline. He further speculated that the hypoxic zone might force gulf menhaden into narrower “corridors” of normoxic waters nearshore where they could be more vulnerable to the fishery. Catchability, the proportion of a population harvested by a given unit of effort, is a key parameter in fisheries stock assessment models that links fishing mortality, fishing effort, and population abundance (Wilberg et al. 2010). Most stock assessment models commonly used to assess harvested populations assume constant catchability. However, this assumption is typically one of convenience, parsimony, or historical precedence. In reality, catchability varies over space and time due to a variety of factors (Crecco and Overholtz 1990, Ziegler et al. 2003, Erisman et al. 2011). Catchability for several fish stocks in the Gulf of Mexico has been shown to increase over time as a result of improved fishing technology, and to increase at low stock abundance (Thorson and Berkson 2010). Such density dependent catchability has been observed in many fisheries (Mackinson et al. 1997, Rose and Kulka 1999, Harley et al. 2001), including Atlantic menhaden (Ahrenholz et al. 1987), and can lead to hyperstability of CPUE, which can mask stock decline, as well as recovery (Erisman et al. 2011). Contraction in spatial distribution and aggregation near the edges of the Gulf hypoxic zone is another mechanism that can lead to high catchability, provided fishers are able to target these aggregations. Hypoxia-induced aggregations have been documented for several demersal species in the northwestern Gulf, including commercially important penaeid shrimp, suggesting hypoxia may influence catchability to the commercial shrimp trawl fishery (Craig and Crowder 2005, Craig et al. 2005, Craig 2011). Effects of hypoxia on the distribution of menhaden and the purse-seine fleet, and the associated implications for catchability to the menhaden fishery have not been investigated. The issue of variable catchability is not confined to fishery dependent data. Catchability of fishery independent surveys used to develop abundance indices is often assumed constant over time because of consistency of sampling gears and a statistical sampling design implemented across a broad area (Thorson and Berkson 2010). However, environmental factors that influence the spatial dynamics of a species can influence catchability to surveys and the associated abundance indices used in stock assessment models. This may be particularly important for surveys that use passive gear (e.g., gillnets) or cover only a portion of the geographic range of a 3 species. To the extent possible, variation in the sampling efficiency of surveys is mitigated when developing indices of abundance through the use of statistical standardization techniques (Maunder and Punt 2004, Maunder et al. 2006), though empirical information on the range of factors that potentially influence catchability is often lacking. The 2011 gulf menhaden assessment applied statistical catch-at-age, surplus production, and stochastic stock reduction models (Amy Schueller, lead analyst). The data used in the assessment included commercial fishery landings and age composition, a juvenile abundance index from state seine surveys, and an adult abundance index and length composition data from the Louisiana gillnet survey. An additional data source that received considerable attention was the commercial fishery CPUE, although this index was ultimately excluded due to concerns that it did not reflect adult abundance. As a result, fishing effort was not included and catchability to the fishery was not estimated in the most recent assessment. In addition, catchability was assumed constant for the fishery independent juvenile and adult abundance indices, even though a portion of these surveys occur in areas subject to hypoxia and none cover the entire geographic range of the stock. Much discussion during the 2011 assessment focused on what combination of indices to use and their utility, including potential biases induced by hypoxia. Hence, evaluating effects of hypoxia on gulf menhaden catchability would benefit the stock assessment. We propose to address the effects of hypoxia on the spatial and temporal dynamics of the gulf menhaden purse-seine fishery, the utility of fishery independent data for developing indices of menhaden abundance, and the associated consequences for the gulf menhaden stock assessment. If menhaden avoid hypoxia and aggregate in alternative habitats, as suggested by Smith (2001) and observed for demersal species, then catchability to the fishery may be enhanced. Alternatively, if the spatial distribution of menhaden shifts to areas less amenable to fishing (e.g., deeper or shallower water), then catchability may decline. Similarly, if hypoxia alters the distribution of menhaden then catchability to fishery-independent surveys may increase or decrease depending on how hypoxia alters availability to the survey. We propose a combination of empirical and modeling approaches to address the following research objectives:

1. Analyze spatial and temporal variation in menhaden fishing effort, landings, and CPUE in relation to variability in the severity of hypoxia over annual to decadal time scales. 2. Quantify the effects of hypoxia on abundances indices used or considered in the gulf menhaden stock assessment. 3. Estimate catchability to the gulf menhaden commercial fishery and determine how catchability has varied in relation to the severity of hypoxia. 4. Incorporate variable catchability into the current stock assessment to evaluate effects on estimates of abundance, fishing mortality, and management benchmarks.

Data Sources and Research Approach: We will assemble the following data sources— Fishery-dependent data: Commercial catch and nominal fishing effort from 1948−present represent one of the longest time series of fishery data in the US and are maintained at the NMFS Beaufort Laboratory. Annual logbook data of commercial landings and fishing effort for the gulf menhaden fleet are available from 1983−present (100% compliance since 1995). Weekly logbook data are spatially resolved into 10 x10 minute grids for the entire time series, with precise latitude and longitude recorded since 2005. These data are in the possession of Principal Investigator (PI) Smith. Fishery-independent data: Fishery independent survey data are available from trawls (1967−present), seines (1977−present), and gillnets (1986−present) across the Gulf coast states 4

from Texas to . These data include station locations and environmental variables (temperature, salinity, dissolved oxygen) and are in the possession of PI Schueller. Hypoxia data: Information on the seasonal and annual severity of hypoxia is available from systematic monitoring efforts by multiple groups. The Southeast Area Monitoring and Assessment Program (SEAMAP) database contains shelf-wide information on the distribution of summer and fall bottom DO from 1983−present. These data are in the possession of PI Craig and are publicly available (http://seamap.gsmfc.org/). Systematic mapping surveys of the hypoxic zone have been conducted during July since 1983 by Louisiana Universities Marine Consortium (N.N. Rabalais) and are available from the National Oceanographic Data Center (http://www.nodc.noaa.gov/). We will also use published hindcasting models (Justic et al. 2007) to examine the possibility of extending the times series of hypoxia severity to the early 1970s.

Analytical Approach—Our initial focus will be on mapping and analysis of geo-referenced fishery and environmental data from fishery-dependent and –independent sources (e.g., Fig. 1). We will develop two indices of the spatial concentration of the menhaden fleet, the spatial extent and the degree of spatial patchiness (sensu Salthaug and Aanes 2003). We anticipate generating maps at monthly time scales over the fishing season (Apr to Sept) prior to, during, and after the period of most severe hypoxia (Jun-Aug). A challenge in characterizing the spatial dynamics of the fleet will be the different degrees of spatial resolution (coordinates in latitude and longitude vs. 10x10 minute grids) over the available time series. We will evaluate this difference in two ways: (1) by aggregating to the lower resolution and (2) by distributing aggregated sets within geographic blocks based on a model of the degree of contagion derived from the disaggregated data. We will map the spatial locations of fishery independent survey CPUE and environmental variables in a similar manner. We will develop multiple metrics of hypoxia severity including the spatial extent of DO ≤ 2 mg l-1, the average nearshore and shelfwide bottom DO concentration off Louisiana, the geographic location of the inshore hypoxic edge, and the linear (alongshore and cross shelf) dimensions of the hypoxic zone. We expect that hypoxia alters the inshore-offshore and alongshore (east and west of the region of severe hypoxia) distribution of the menhaden fleet. The temporal dynamics of the fishery have possibly been altered as well, with increased effort and landings either before or after the period of severe summer hypoxia. We will develop statistical models relating the spatial concentration of the fishery to metrics of hypoxia using geostatistical and regression-based approaches (Guisan et al. 2002, Wood 2006, Cianelli et al. 2008) to test for these effects. We will also modify the current delta-GLM for gulf menhaden (Maunder and Punt 2004) to determine the effects of hypoxia on fishery- independent indices of abundance. These analyses will provide a flexible, mechanistic basis for evaluating hypoxia effects on the fishery. We will estimate the catchability coefficient, q, across years and locations that vary in the presence and severity of hypoxia as q = C/EB, where C = menhaden landings, E = fishing effort, and B = biomass. Logbook data will be used to estimate menhaden landings and fishing effort. Initially, we will use historical trends in menhaden biomass (B) from the current catch-at-age model. Because the current model does not use information on fishing effort or catchability to the fishery, these biomass estimates are not dependent on an estimate of q for the fishery. We will also examine the possibility of estimating biomass from the SEAMAP survey during summer (Jun-Jul) and available state survey data as alternative empirical estimates of annual menhaden biomass. Whereas SEAMAP is a bottom trawl survey, it does sample pelagic and vertically migrating species. Annual variation in the severity of hypoxia on the nearshore Louisiana shelf has varied considerably since the 1980s, suggesting hypoxia may induce time- 5

varying catchability across years differing in hypoxia severity. As an additional test of hypoxia effects on catchability we will explore spatial variation in q via comparisons east (where hypoxia is rare) and west (where hypoxia is most severe) of the Mississippi River delta (Fig. 1). We will relate these empirical estimates of q to previously calculated indices of spatial extent and aggregation of the fleet to test whether hypoxia is the underlying mechanism driving variability in catchability (aside from other annual effects). Empirically-based variation in catchability will be incorporated into the gulf menhaden stock assessment model to evaluate the constant catchability assumption of the current model. We will conduct simulation analyses comparing model outputs that assume constant catchability to those incorporating alternative, empirically- based estimates of catchability. We will explore two alternatives for incorporating variation in catchability: (1) estimating catchability as a function of environmental factors within the catch- at-age model itself, and (2) developing a priori relationships outside of the model that are then assumed fixed within the catch-at-age model. These alternative approaches involve tradeoffs associated with the strength of the relationship with environmental factors and the degree of autocorrelation in the environmental effect. These comparisons will provide an indication of the direction and magnitude of potential biases in the current assessment model, as well as a framework to improve the assessment methodology.

Timeline: Year 1: Hire post-doctoral associate, assemble datasets, and map the spatial distribution of effort, landings, fishery independent catch rates and hypoxia. Conduct statistical analyses of hypoxia effects on catchability and fishery independent CPUE. Year 2: Derive empirical estimates of annual catchability and quantify potential effects of hypoxia on fishery independent abundance indices. Conduct simulation analyses to quantify the effects of hypoxia-induced changes in catchability on the gulf menhaden stock assessment.

Benefits: The proposed research will provide an empirically-based analysis of hypoxia effects on the gulf menhaden stock assessment. If explicit incorporation of these effects into the assessment model is warranted, then historical estimates of abundance, fishing mortality, and management benchmarks could be improved. If this is not warranted, then a scientific basis will exist for excluding these effects rather than the current approach based on assumption. The results of this study may also indicate the need to address hypoxia effects on catchability of other economically important Gulf species. The training of a postdoctoral associate at the interface of fisheries ecology and stock assessment is an additional benefit.

Deliverables: • Maps of the spatial distribution of commercial fishing effort, landings, and CPUE relative to the distribution and severity of hypoxia over the available time series. • Empirically-based estimates of catchability of Gulf menhaden across time periods and locations that differ in the presence and severity of hypoxia. • Statistical models of hypoxia effects on fishery dependent and independent data used or considered for developing abundance indices. • Comparisons of historical trends in abundance, fishing mortality, and management benchmarks for models excluding and including hypoxia effects on catchability. • Peer-reviewed journal publications addressing the consequences of environmental variability on stock assessments. • Presentations at national scientific and regional conferences and to stakeholders in the gulf menhaden fishery, including managers. 6

Statement of Previous Results Bath-Martin, Shertzer, Buckel, Taylor. FY2006. Fishery indices for the Southeast Atlantic (FISEA): Biological indicators of coastal and estuary-dependent fishery production in the U.S. South Atlantic.

This previously funded project has produced, and continues to produce, peer-reviewed publications with the aim to improve stock assessments and ecosystem-based approaches to fishery management. Results reported in one of those publications (Taylor et al. 2009) were already used in a stock assessment of southern flounder (Moore and Taylor 2008), and results from another (Adamski et al. In press) will be considered for use in the next SEDAR benchmark assessment of gag grouper. Two affiliated manuscripts are still in preparation (listed below for completeness).

Completed Able, K, M Sullivan, J Hare, G Bath-Martin, JC Taylor, R Hagan. 2011. Fishery independent larval monitoring as a measure of summer flounder stock status: implications for management. Fishery Bulletin 109:68−78. Adamski, KM, JA Buckel, KW Shertzer, G Bath Martin, JC Taylor. 2011. Developing fishery- independent indices of abundance of larval and juvenile gag (Mycteroperca microlepis) in the southeast United States. Transactions of the American Fisheries Society (in press). Moore, T and JC Taylor. 2008. Juvenile and larval abundance indices working paper, 2008 Stock Assessment: Southern Flounder, North Carolina Division of Marine Fisheries, Morehead City, NC. Taylor, JC, J Miller, L Pietrafesa, D Dickey, S Ross. 2010. Winter winds and river discharge determine abundance and distribution of southern flounder in North Carolina estuaries. Journal of Sea Research 64:15−25. Taylor, JC, WA Mitchell, JA Buckel, HJ Walsh, KW Shertzer, GB Martin, JA Hare. 2009. Relationships between larval and juvenile abundance of winter-spawned fishes in North Carolina, USA. Marine and Coastal Fisheries 1:11−20.

In Preparation Adamski, KM, JA Buckel, D Ahrenholz, G Bath-Martin, and JA Hare. In prep. Use of otolith microstructure to determine early life history traits in post-larval and juvenile gag from North Carolina. Mitchell, WA, JC Taylor, JA Buckel, KW Shertzer, and G Bath Martin. In prep. Phenology of ingressing icthyoplankton assemblages at Beaufort inlet North Carolina, USA

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