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Emaciated black drum (Pogonias cromis) in the upper Laguna Madre, Texas: tracking the recovery of the population over two years.

Abstract.--Black drum (Pogonias cromis), are the focus of a major commercial and recreational fishery in Texas coastal waters within the Upper Laguna Madre (ULM) producing the greatest proportion of commercial landings. During Fall 2012, the black drum population in the Baffin Bay area of the ULM experienced an emaciation event. Individuals exhibited gelatinous fillets with reduced white muscle along the dorsal region, little-to-no digestate in the gut, and in some cases, atrophy of the internal organs. These individuals were found to be underweight compared to those in the northern ULM. After this initial emaciation event, Texas Parks and Wildlife Department-Coastal Fisheries Division staff continued to quantitatively monitor the health of this population using condition factor analysis through Spring 2014. This analysis suggests that the Baffin Bay area population of black drum demonstrated improving condition factor values from the emaciation event of Fall 2012 (0.94 [+ or -] 0.07; median [+ or -] interquartile range) by Spring 2013 (1.00 [+ or -] 0.08) and had completely recovered by Spring 2014 (0.98 [+ or -] 0.08) as compared to condition factor values of a control group in the northern ULM (fall 2012: 1.06 [+ or -] 0.08; spring 2014: 0.97 [+ or -] 0.09). Anecdotal reports from both recreational and commercial anglers also suggest a decline in the prevalence of emaciated fish in the Baffin Bay area.

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Black drum (Pogonias cromis Linnaeus 1776), occur along inshore marine waters from New England in the western Atlantic to Argentina (Hoese & Moore 1998). These large benthic sciaenids (Perciformes: Sciacnidae) are the focus of multiple commercial and recreational fisheries in the Gulf of Mexico and the Atlantic coasts. The Upper Laguna Madre (ULM) is the ccnter of the commercial black drum fishery along the Texas coast in the Gulf of Mexico. Coast-wide, the fishery has an annual mean ex-vessel value of $1,484,545 (2007-2012) with greater than half of these landings (by weight) generally coming from the ULM (TPWD, unpublished data). Throughout much of their range, black drum are known to feed extensively on benthic mollusks, most notably the economically important Eastern oyster (Crassostrea virginica) (Cave 1978; Dugas 1986). In the hypersaline ULM where salinities are too high to support viable oyster populations, black drum feed primarily on a suite of smaller benthic mollusks such as the dwarf surf clam (Mulinia lateralis) and Atlantic paper mussel (Amygdalum papyrium) (Martin 1979). However, populations of these benthic mollusks are known to be extremely variable, presumably as a result of the highly variable salinity regimes of this ecosystem (Montagna & Kalke 1995).

During the fall of 2012 Texas Parks and Wildlife Department-Coastal Fisheries Division (TPWD-CF) staff received numerous reports from commercial fish houses and recreational anglers of underweight and emaciated black drum from the Baffin Bay region of the ULM. Such fish exhibited gelatinous fillets with reduced white muscle along the dorsal region, little to no digestate in the gut and, in some cases, atrophied internal organs. Using condition factor analysis (Froese 2006), Olsen et al. (2014) determined that the black drum population in the Baffin Bay region was significantly underweight compared to those in the northern ULM.

Methods of tracking emaciation and condition have varied among researchers. Uphoff (2003) examined variation in length-weight regression coefficients and confidence intervals as suggested by Cone (1989). Uphoff (2003) cited increased variability in the relationship between length-weight (i.e., decreasing r2) as evidence for emaciation. Other researchers have suggested that the use of regression coefficients as a replacement for condition factors is often uninformative (Springer & Murphy 1990). Froese (2006) gives an excellent review of condition factor analysis in addition to a number of recommendations to ensure sound use of this analytic technique. Among these recommendations is the necessity to assess and allow for natural changes in condition with length (form) and season. Diets and feeding behavior of other scieanids are known to vary ontogenetically and seasonally (Martin 1979; Scharf & Schlicht 2000) which could result in a natural impact on condition. Additionally, seasonal reproductive cycles could have an impact on condition with changes in body weight related to gonad development artificially inflating condition factor values. Therefore, if condition factors are to be compared across time, season and length specific changes in condition must be taken into account.

In the months following the initial emaciation event, TPWD-CF staff received fewer reports of emaciated fish from commercial fish houses and recreational anglers. The recovery of the Baffin Bay population of black drum in the years following the 2012 emaciation event is reported here.

Materials & Methods

Sample Collection-TPWD-CF has conducted routine fisheries independent sampling in the upper Laguna Madre region since the late 1970s. This includes collection of both gill net catch rate data and physical parameters throughout this bay system (see Martinez-Andrade et al. 2005 for a full description of sampling protocols). Black drum were collected (live and fresh dead) from routine fishery independent gill net surveys, stored on ice, and transported to the laboratory for analysis in the same manner as Olsen et al. (2014). As gill net surveys are only conducted during the spring and fall months, sample collection for condition factor analysis occurred during the following seasons: Fall 2012 (September-November), Spring 2013 (April-June), Fall 2013 (September-November), and Spring 2014 (April-June). For purposes of the condition factor analysis, fish were collected from the Baffin Bay area and from the northern ULM. The latter was considered a control site due to reports of healthy black drum from commercial fishermen and its location (approximately 35 kilometers north) compared to Baffin Bay (Fig. 1). This control site was slightly expanded from Olsen et al. (2014) to allow for greater flexibility in sample collection, though the stipulations for this region still hold true (i.e., healthy black drum and distance from Baffin Bay).

Condition Factor Calculations and Statistical Analysis.--Individual black drum lengths and weights were recorded in laboratory and a relative condition factor ([K.sub.rel]) calculated for each individual fish:

[K.sub.rel] = W / a x [TL.sup.b],

where W is wet weight (g), TL is total length (mm), and a (-5.05) and b (3.06) are regression coefficients from performing simple linear regression on log-transformed length and weight for fish from all seasons combined (i.e., Fall 2012, Spring 2013, Fall 2013, and Spring 2014). The relative condition factor accounts for changes in form with length (i.e., b < or > 3) which is often observed as a fish grows. Regression coefficients from simple linear regression on log-transformed length and weight conducted separately for each season were found to be very similar and so season specific values were deemed unnecessary.

Changes in condition with length were assessed by regressing [K.sub.rel] on TL separately for each site. Changes in [K.sub.rel] across season and site were assessed using Analysis of Covariance (ANCOVA) procedures. For both the simple linear regression and ANCOVA models, plotted residuals were examined to assess normality. For the ANCOVA models, [K.sub.rel] values were log-transformed to better fit this assumption. Multicollinearity was assessed by both examination of plotted explanatory variables and calculation of variance inflation factors. All statistical procedures were implemented in R (R Core Team 2014) and deemed significant at a = 0.05.

Results

Sample size and size range of fish collected are given in Table 1. The relationship between [K.sub.rel] and TL was found to be very limited and in most cases non-existent (Fig. 2). During the fall of 2012 this relationship for Baffin Bay fish was found to be negative (t = 3.42; df= 35; P = 0.002) and during the spring 2014, this relationship for control site fish was found to be positive (f = 4.18; df= 54; P< 0.001) though model fit was quite poor in both cases (Fall 2012: F = 11.7; df= 1, 35; P = 0.002; [r.sup.2] =0.25; Spring 2014: F= 17.49; df= 1, 54; P < 0.001 ; [r.sup.2] =0.23).

Residuals of the ANCOVA model utilizing log-transformed [K.sub.rel] values were found to be normally distributed and multicollinearity was not observed among independent variables. Transformed [K.sub.rel] values were found to vary significantly with the interaction of season*site (Table 2). This suggests that the regression lines for the two sites differ in both the intercept and the slope (i.e., sites represent differing regression lines that vary at differing rates across seasons). Therefore, interpretation of the site and season terms is unnecessary. The disparity of median [K.sub.rel] values between sites was greatest during the Fall 2012 emaciation event and decreased in each successive season with Fall 2013 and Spring 2014 showing very similar[K.sub.rel] values between sites (Fig. 3).

Monthly mean surface salinity from both the Baffin Bay area and the ULM (designated as the primary bay system running from Corpus Christi Bay south to the southern portion of the landcut; Fig. 1) collected during TPWD-CF's routine monitoring are presented from 2004-2014 (Fig. 4). During this time period, peak salinities are observed during the timeframe of this study. Additionally, black drum catch rates (catch/hour) from TPWD-CF's routine fisheries independent gill net surveys are also presented by season from 2004-2014 in order to assess black drum abundance patterns in these two bay systems surrounding the 2012 emaciation event (Fig. 5). Catch rates are consistently greater in the Baffin Bay system for all seasons except Spring 2013 and Spring 2014, which seems to be a result of increasing ULM catch rates and decreasing Baffin Bay catch rates in the years surrounding the emaciation event.

Discussion

Based on condition factor values reported in this study, the population of black drum in the Baffin Bay area began recovery from the Fall 2012 emaciation event by Spring 2013, and had completely recovered by Fall 2013 and Spring 2014. This finding coincided with decreased reports of emaciated fish from both recreational and commercial anglers. The potential cause(s) of the black drum emaciation event reported here are detailed in Olsen et al. (2014) and so are only discussed briefly. The variable nature of the benthic community in Baffin Bay (Martin 1979; Montagna & Kalke 1995; Nicolau & Nunez 2006) combined with large populations of black drum (Olsen 2014) in the system may have resulted in a shortage of forage. The Baffin Bay system experienced some of the highest mean annual salinities on record in 2012 and 2013 (56.2 and 62.3 practical salinity units (psu) respectively; Fig. 4). Such conditions could have presumably aided in such a shortage and resultant lack of resources. Nonetheless, improvement in black drum condition seems to have begun while salinities remained fairly high in the Baffin Bay area. Increased fishery independent gillnet catch rates in the adjacent ULM and decreased catch rates in the Baffin Bay area during Spring 2013 and Spring 2014 do, however, coincide with decreasing disparity of [K.sub.rel] values between sites and suggests that black drum may be moving out of the area resulting in decreased population density and less competition for resources. However, as migratory patterns are difficult to ascertain without appropriate tagging studies and limited benthic data are available for this system, such conclusions are strictly speculative for the time being.

Emaciation in black drum populations has also been observed in Louisiana waters. In 2009, Louisiana Department of Wildlife and Fisheries (LDWF) received reports of underweight and emaciated fish from commercial fish houses in the Barataria basin. After examination of the fish, LDWF staff speculated the emaciation was caused by increased levels of domoic acid and microcystin in the diet of the fish though this was never verified (pers. comm. Jason Adriance, LDWF). Uphoff (2003) described an emaciation event in northern Chesapeake Bay striped bass, Morone saxatilis (Walbaum), that occurred from 1997-2000. It was speculated that this striped bass emaciation event was the result of a decrease in Atlantic menhaden (Brevooria tyrannus) populations, the primary forage of striped bass, and increasing striped bass abundance following a harvest moratorium in the early 1990s (Uphoff 2003). Costantini et al. (2008) found that decreasing dissolved oxygen could have resulted in increased feeding efficiency of striped bass further resulting in decreased forage. While these emaciation events occurred under very different circumstances compared to the present situation, it underscores the potential impact of environmental parameters on forage organisms and the food webs they support.

The present study confirms that the greatest disparity of black drum condition between the northern ULM control site and the Baffin Bay area was observed during Fall 2012, coinciding with the described emaciation event. In each subsequent season, the difference in condition between sites decreased. This event highlights the need to further understand trophic relationships, movement patterns, and the impacts of hypersalinity on Baffin Bay residence. Further work is necessary to fully elucidate the causes of this event and to better understand the dynamics of this unique system.

Acknowledgments

I would like to thank F. Grubbs, A. Leiva, M. Voorhees, J. Garcia, J. Ferguson, and C. Witherell for aiding in the collection of this length-weight data. I would also like to thank J. Tolan for helpful discussion and guidance with the condition factor analysis and J. Adriance (Louisiana Department of Wildlife and Fisheries) for discussion regarding black drum emaciation in Louisiana.

Literature Cited

Cave, N. 1978. Predator-prey relationships involving the American oyster, Crassostrea virginica, and the black drum, Pogonias cromis, in Mississippi Sound. Unpublished M.S. Thesis. Southeastern Louisiana Univ., Hammond. 43 pp.

Cone, R. S. 1989. The need to reconsider the use of condition indices in fishery science. Trans. Am. Fish. Soc. 118: 510-514.

Costantini. M., S. A. Ludsin, D. M. Mason, X. Zhang, W. C. Boicourt & S. B. Brandt. 2008. Effect of hypoxia on habitat quality of striped bass (Morons saxatilis) is Chesapeake Bay. Can. J. of Fish. Aquat. Sci. 65: 989-1002.

Dugas, C. N. 1986. Food habits of black drum. Pogonias cromis, in southeast Louisiana with emphasis on their predation of the American oyster, Crassostrea virginica. Contributions of the Marine Research Laboratory pp. 32-38. Louisiana Department of Wildlife and Fisheries.

Froese, R. 2006. Cube law, condition factor and weight-length relationships: history, meta-analysis and recommendations. J. Appl. Ichthyol. 22: 241-253.

Hoese. H. D. & R. H. Moore. 1998. Fishes of the Gulf of Mexico Texas, Louisiana, and Adjacent Waters. Texas A&M University Press, College Station.

Martin, J.H. 1979. A study of the feeding habits of black drum (Pogonias cromis Linnaeus) in Alazan Bay and the Laguna Salada, Texas. Unpublished M.S. Thesis, Texas A&I Univ., Kingsville, 104 pp.

Martinez-Andrade, F., P. Campbell & B. Fuls. 2005. Trends in relative abundance and size of selected finfish and shellfish along the Texas coast: November 1975-December 2003. Texas Parks and Wildlife Department-Coastal Fisheries Management Data Series Number 232. Austin.

Montagna, P. A. & R. D. Kalke. 1995. Ecology of infaunal Mollusca in south Texas estuaries. Am. Malacol. Bull. 11: 163-175.

Nicolau. B. A. & A. X. Nunez. 2006. Coastal Bend Bays and Estuaries Program, Regional Coastal Assessment Program (RCAP): RCAP 2004 Annual Report. Center for Coastal Studies, Texas A&M University--Corpus Christi. TAMU-CC-0603-CCS.

Olsen, Z. T., F. P. Grubbs, A. D. Morris & J. M. Tolan. 2014. Reports of Emaciated black drum, Pogonias cromis, in the Upper Laguna Madre, Texas. Tex. J. Sci. 66(3):75-81.

Olsen, Z. T. 2014. Potential impacts of extreme salinity and surface temperature events on population dynamics of black drum, Pogonias cromis, in the Upper Laguna Madre, Texas. Gulf Mex. Sci. 1-2: 60-68

R Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org/.

Scharf, F. S. & K. K. Schlicht. 2000. Feeding habits of red drum (Sciaenops ocellatus) in Galveston Bay, Texas: seasonal diet variation and predator-prey size relationships. Estuaries 23: 128-139.

Springer, T. A. & B. R. Murphy. 1990. Comments: Properties of relative weight and other condition indices. Trans. Am. Fish. Soc. 119:1048-1058.

Uphoff. J. H. 2003. Predator-prey analysis of striped bass and Atlantic menhaden in upper Chesapeake Bay. Fish. Manage. Ecol. 10: 313-322.

ZTO at: zachary.olsen@tpwd.texas.gov

Zachary T. Olsen

Texas Parks and Wildlife Department--Coastal Fisheries Division 6300 Ocean Drive, Suite 2500, Corpus Christi, Texas 78412

Caption: Figure 1. Map of the Upper Laguna Madre with collection locations (Baffin Bay area and the northern Upper Laguna Madre control site).

Caption: Figure 2. Simple linear regression of relative condition factors ([K.sub.rel]) and total length for black drum (Pogonias cromis) from Baffin Bay (hollow; dashed line) and the northern Upper Laguna Madre control site (solid; solid line). Fish were collected during Fall 2012 (a). Spring 2013 (b). Fall 2013 (c), and Spring 2014 (d).

Caption: Figure 3. Median relative condition factors ([K.sub.rel]) plotted with first and third quartiles for black drum (Pogonias cromis) collected in the Baffin Bay area (hollow) and northern Upper Laguna Madre control site (solid) across season. Fitted values from the ANCOVA model are also given for both the Baffin Bay area (dashed line) and the northern Upper Laguna Madre control site (solid line).

Caption: Figure 4. Monthly mean surface salinity (practical salinity units, psu) collected during Texas Parks and Wildlife Department-Coastal Fisheries Division's routine fisheries independent monitoring in the Baffin Bay area (dashed line) and the Upper Laguna Madre (solid line).

Caption: Figure 5. Gill net catch rates (catch/hour [+ or -] SE) for black drum (Pogonias cromis) from Texas Parks and Wildlife Department-Coastal Fisheries Division's routine fisheries independent monitoring program collected in the Baffin Bay area (dashed line) and the Upper Laguna Madre (solid line).
Table 1 .Sample size (n) and size range (Total length, mm) of black
drum (Pogonias cromis) collected for condition factor analysis for
each season and site combination.

Season           Site       n      Size range (TL, mm)

Fall 2012       Baffin     37            219-596
Fall 2012      Control     30            295-592
Spring 2013     Baffin     72            235-487
Spring 2013    Control     34            300-566
Fall 2013       Baffin     107           210-531
Fall 2013      Control     65            217-667
Spring 2014     Baffin     111           213-634
Spring 2014    Control     56            293-550

Table 2. Output from the ANCOVA model of log-transformed relative
condition factors ([K.sub.rel]) of black drum (Pogonias cromis) on
site (Baffin Bay area and northern Upper Laguna Madre control site),
season (Fall 2012-Spring 2014), and the interaction of site*season.
Due to the fact that the interaction term is significant, the
interpretation of the site and season terms is unnecessary.

Independent Variables      F      df (factor, model error)       P

Site*Season              27.96             1, 508              <0.001
Site                     18.36             1, 508              <0.001
Season                   7.39              1, 508              0.006
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Author:Olsen, Zachary T.
Publication:The Texas Journal of Science
Article Type:Report
Geographic Code:1USA
Date:Feb 1, 2016
Words:3078
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