Effects of the 2004 Hurricanes on the Fish ...

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seatrout (Cynoscion nebulosus)). There was relative stability in both estuaries' fish assemblages from. 1996 to 2005, as was indicated by no serial change.
Estuaries and Coasts

Vol. 29, No. 6A, p. 985–996

December 2006

Effects of the 2004 Hurricanes on the Fish Assemblages in Two Proximate Southwest Florida Estuaries: Change in the Context of Interannual Variability MARIN F. D. GREENWOOD1,*, PHILIP W. STEVENS2, and RICHARD E. MATHESON JR.1 1

2

Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, 100 8th Avenue SE, St. Petersburg, Florida 33701 Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, Charlotte Harbor Field Lab, 1481 Market Circle Unit 1, Port Charlotte, Florida 33953

ABSTRACT: We examined interannual differences in fish assemblage structure in Tampa Bay and Charlotte Harbor, Florida, from 1996 to 2005 to reveal the extent of hurricane-induced changes in relation to multiannual variability for five different assemblages in each estuary: small-bodied fishes (, generally 80-mm standard length) along river shorelines, in river channels, along bay shorelines, and on the bay shelf (, 1.5-m water depth); and large-bodied fishes (. generally 100-mm standard length) along bay shorelines. Fish assemblages tended to differ between estuaries, as did interannual variability in assemblage structure. In the lower portions of tributary rivers to Tampa Bay, the small-bodied shoreline fish assemblage during August 2004 to July 2005, i.e., during and after the multiple hurricanes, was different from assemblages of August to July in previous years. This may have been a result of physical displacement of fish or suboptimal salinities caused by increased freshwater inflow. The small-bodied shoreline fish assemblage in Charlotte Harbor also differed between prehurricane and hurricane periods, possibly because damage to vegetated shorelines affected fish survival through a decrease in feeding and refuge habitats. In the remaining habitats, fish assemblage structure from August 2004 to July 2005 were within the range of variability exhibited over the 9-yr study period. There were several unusual fish assemblages that appeared to be attributable to drought conditions (1996, 1999–2000), suggesting that other major environmental perturbations may be as important as hurricanes in influencing assemblage structure. We conclude that although the 2004 hurricane season affected some of the fish assemblages of Tampa Bay and Charlotte Harbor, these assemblages generally appeared quite resilient to natural environmental perturbations from a decadal perspective.

that decrease salinity, increase nutrient input, reduce vertical mixing of the water column, and facilitate the formation of areas of bottom hypoxia (Paerl et al. 2001). As a consequence, fishes in estuaries may suffer mass mortality or impaired health (Tabb and Jones 1962; Paerl et al. 2001). Although short-term effects of hurricanes on fishes may be substantial, the relatively high frequency of hurricane events in tropical and subtropical areas may result in fish assemblages being reasonably resistant to long-term change (Adams and Ebersole 2004; Burkholder et al. 2004). Because fish assemblages are composed of diverse species, each with unique environmental tolerances, long-term studies of changes in assemblage structure are desirable to indicate multiple species’ responses to acute or chronic environmental variability (e.g., Wolfe et al. 1987; Jan et al. 2001). This allows apparently great short-term changes to be judged in the context of long-term variability (Adams 2001). We examined changes in southwest Florida estuarine fish assemblages following multiple hurricanes in 2004 (see Sallenger et al. 2006) in relation

Introduction Estuarine fish assemblages typically undergo predictable annual cycles in structure that are largely attributable to discrete recruitment periods of marine species (e.g., Tsou and Matheson 2002; Maes et al. 2005), but extreme environmental conditions may disrupt these cycles (Potter et al. 1986). Extreme environmental conditions may result from factors such as sudden temperature changes (Gilmore et al. 1978), large annual variations in rainfall or river discharge (e.g., due to climatic fluctuations; Garcia et al. 2001), excessive contaminant loading (Marchand et al. 2002), or catastrophic natural events such as hurricanes. In the case of hurricanes, the wind and storm surge may cause sediment inundation or removal of submerged aquatic vegetation (SAV), which may adversely affect fish assemblages (Tabb and Jones 1962; Rozas and Reed 1994). The rainfall associated with hurricanes leads to elevated inflows to estuaries * Corresponding author; tele: 727/896-8626; fax: 727/8931271; e-mail: [email protected] ß 2006 Estuarine Research Federation

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to assemblage variability observed during the previous 8 yr (1996–2003). We compared and contrasted assemblage changes in Tampa Bay and Charlotte Harbor, two proximate (, 100 km apart) estuaries with relatively similar fish assemblages (Springer and Woodburn 1960; Poulakis et al. 2004), which received varying levels of rainfall, contaminant loading, and physical damage to mangroves during the 2004 hurricane season. We addressed three main questions in this study: were fish assemblages found in these two estuaries during and after the 2004 hurricanes notably different from pre-hurricane assemblages; if so, which species were principally responsible for the observed differences; and did fish assemblages in Tampa Bay and Charlotte Harbor show evidence of serial change over the 1996 to 2005 period, i.e., was there evidence of overall long-term faunal change? Materials and Methods STUDY AREAS AND HURRICANE EFFECTS Tampa Bay and Charlotte Harbor are located in southwestern Florida and have surface areas of about 1,030 and 700 km2, respectively (Galperin et al. 1991; McPherson et al. 1996). Both systems are shallow (generally , 4 m), drowned-river-valley estuaries (Galperin et al. 1991; Sheng 1998). A shallow shelf , 1.5 m deep extends 500 to 1,200 m from the shoreline (Lewis and Estevez 1988), beyond which deeper, unvegetated habitats predominate. Tidal range is typically , 0.7 m (see National Oceanographic and Atmospheric Administration/National Ocean Service Center for Operational Oceanographic Products and Services benchmarks website http://tidesandcurrents.noaa. gov). Principal freshwater inflow is from several rivers (Tampa Bay: Hillsborough, Manatee, Alafia, and Little Manatee; Charlotte Harbor: Peace, Myakka, and Caloosahatchee). Tampa Bay is the more urbanized of the two estuaries, with substantial amounts of altered shoreline (e.g., seawall and rip-rap), but both estuaries contain considerable areas of vegetated habitat, including seagrass (predominantly turtle grass, Thalassia testudinum, and shoal grass, Halodule wrightii), mangrove (principally red mangrove, Rhizophora mangle), and salt marsh (mostly black needlerush, Juncus roemerianus). More detailed descriptions of the study areas are available from (Lewis and Estevez 1988) and (McPherson et al. 1996). Tampa Bay and Charlotte Harbor experienced fluctuating environmental conditions in recent years, including unusually wet and warm periods attributable to the El Nin ˜ o portion of ENSO (1997– 1998) followed by very dry and cool conditions coinciding with La Nin ˜ a (1998–2000; Schmidt et al.

2004). High rainfall in December 1997 caused an acid spill into the Alafia River, resulting in release of 189–211 3 106 l of wastewater that killed more than 1.3 3 106 fish (Iliff et al. 2001). Four hurricanes greatly elevated rainfall in the region during the summer of 2004, but Hurricane Charley, a category 4 storm that made landfall on 13 August, also produced considerable physical damage (defoliation and uprooting of mangroves and other wetland vegetation) in Charlotte Harbor. The resultant pulse of organic material greatly elevated microbial activity and caused an enlarged area of bottom hypoxia reaching 15 km into Charlotte Harbor (Tomasko personal communication). A short-term change in fish assemblage was apparent, with a predominance of low-oxygen-tolerant species; the fish assemblage returned to pre-hurricane structure within 4 wk of the storm’s passage (Stevens et al. 2006). In Tampa Bay, heavy rainfall from September’s Hurricane Frances caused a breach in a phosphate facility’s acidic waste reservoir, releasing approximately 155,000 m3 of wastewater into northeastern Tampa Bay via Archie Creek. In addition to these events, various fishery regulations have been changed (for complete history see State of Florida Marine Fisheries Management Commission Approved Rules Summary, http://marinefisheries. org/history/index.html). The most important of these changes was an entangling net restriction in July 1995 that led to a 65% decrease in commercial landings of inshore finfishes (Adams et al. 2002). SAMPLING METHODS This paper is derived from data collected by the State of Florida, Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute’s Fisheries-Independent Monitoring Program, with the essential features described here (McMichael unpublished data). To ensure adequate representation of the primary ichthyofaunal habitats within Tampa Bay and Charlotte Harbor and the lower portions of several of their main tributaries, sampling sites were selected in a stratified random manner. Each bay was divided into zones based on hydrographic and logistic considerations (Fig. 1), with effort allocated to each zone in proportion to the area of the zone. Within each zone, we further stratified shoreline habitat by dividing sites into two groups: overhanging (. 10% of shoreline with vegetation overhanging the water) and nonoverhanging. Bay habitats away from the shoreline on the estuarine shelf were stratified into vegetated ($ 25% SAV coverage) or unvegetated (, 25% SAV coverage) categories. Detailed descriptions of gear deployment techniques and field procedures are available from Kuspschus and Tremain (2001), Paperno et al. (2001), Tsou and Matheson

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Fig. 1. Study areas, with stratified random sampling zones indicated by letters.

(2002), and Idelberger and Greenwood (2005). Five habitat-gear combinations were employed in each estuary, and we treat each of the combinations as representing a particular fish assemblage. Smallbodied fishes (generally , 80-mm standard length [SL]) along river shorelines (water depth , 1.8 m), bay shorelines, and shallow bay shelves away from the shore (, 1.5-m depth) were sampled with 21.3-m seines (3.2-mm stretched mesh). Typical effort (samples month21) ranged from five (bay shorelines in Tampa Bay) to twenty (bay shelves in Tampa Bay). Small-bodied fishes in river channels (depth 1.8–7.6 m) were sampled with 6.1-m otter trawls (3.2-mm cod-end liner; eleven and six samples? month21 in Tampa Bay and Charlotte Harbor, respectively). Larger fish (usually . 100-mm SL) in bay shoreline habitats were collected with 183-m haul seines (38-mm stretched mesh; 20 and 17 samples?month21 in Tampa Bay and Charlotte Harbor, respectively). Sampling effort was reasonably consistent over time and there were no substantial interannual biases of spatial or seasonal coverage, so we assumed that valid comparisons of assemblage structure could be made despite minor differences in effort between some years. Fish were identified to lowest practical taxon (generally species); nomenclature follows (Nelson et al. 2004). A subsample of # 40 individuals was measured for length; any remaining individuals were counted. Following data collection, fish were returned to the water, except in cases when laboratory identification was necessary. Additionally, three representative specimens of each species

collected in 21.3-m seines and 6.1-m otter trawls on each sampling day were identified in the laboratory to confirm field-based identifications. Physical (temperature) and chemical (salinity and dissolved oxygen) characteristics of the water at each site were recorded at surface, bottom, and 1-m intervals between surface and bottom with Hydrolab or YSI probes. DATA ANALYSIS The 2004 hurricane season began with Hurricane Charley on 13 August. The main objective of the study was to compare the fish assemblages in the 12 mo including and following the multiple hurricanes (August 2004 to July 2005) with fish assemblages over the July to August period for all years preceding the hurricanes (August 1996 to July 2004). We grouped data into annual periods commencing in August and ending in July. We refer to each 12-mo period by the first year in the period, e.g., August 1996 to July 1997 is referred to as 1996. Data for river inflow in both estuaries’ watersheds were obtained from the United States Geological Survey’s National Water Information System (http://waterdata.usgs.gov/nwis/). Sites used to indicate inflows to Tampa Bay included the Little Manatee River at Wimauma (site # 2300500) and the Alafia River at Lithia (# 2301500). Sites chosen to characterize inflow to Charlotte Harbor were the Peace River at Arcadia (# 2296750) and the Myakka River near Sarasota (# 2298830). Mean daily inflow for each of the 9 study

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years was plotted in relation to median, 5th, 25th, 75th, and 95th percentile flows for the 1955–1995 period. We also assessed water column averaged mean temperature, salinity, and dissolved oxygen using General Linear Models (PROC GLM in SAS; SAS Institute Inc. 1999) by testing for differences in these variables between bay, year, and the bay 3 year interaction, for each of the five habitat-gear combinations. Statistical significance was considered to be p , 0.05. We conducted separate sets of biotic analyses for each of the five habitat-gear combinations, with data for Tampa Bay and Charlotte Harbor included in the same analysis. Data for trawls were standardized to number of fish per 720 m2 (i.e., the average area sampled by a typical trawl) to account for differences in sampling area resulting from different tow speeds. Data for shoreline 21.3-m seines set in bay habitats were standardized to number of fish per 338 m2 to offset the change in deployment technique that was initiated in January 1998 (Matheson et al. 2005). These standardizations eliminated small fractions that would have been included in the data set had it been standardized to an arbitrary area of 100 m2, for example. In each set of analyses, relative abundance was natural-logarithm-transformed (ln [x+1]) to lessen the influence of highly abundant taxa, in particular bay anchovy (Anchoa mitchilli). All fish-assemblage analyses were conducted with Plymouth Routines in Multivariate Ecological Research (PRIMER v.6) software (Clarke and Warwick 2001). Bray-Curtis similarity matrices (Bray and Curtis 1957) were calculated on data averaged by year and estuary to assess interannual fish assemblage similarities. The resulting matrices facilitated arrangement of samples into two-dimensional ordination space by nonmetric multidimensional scaling (MDS; Clarke 1993), which allowed us to visually explore whether hurricane-year conditions were unusual in relation to other interannual variability in fish assemblage structure. The MDS analysis was undertaken in conjunction with hierarchical agglomerative clustering (Kaufman and Rousseeuw 1990) because MDS plots were of only reasonable representation (i.e., stress [5 goodness of fit] between 0.1 and 0.2; Clarke and Warwick 2001). We concentrated our description of interannual assemblage differences at the levels of BrayCurtis similarity that resulted in division of individual, outlying years from remaining years in each estuary. This allowed us to examine whether the hurricane-influenced assemblage structures from August 2004 to July 2005 were notably different from assemblages in other years. Notable interannual differences in fish assemblage structure that were apparent from MDS and cluster analyses were assessed for discriminating taxa with Similarity

Percentage Analysis (SIMPER; Clarke 1993), based on data averaged by estuary, year, and month. We defined discriminating taxa as the ten taxa that contributed most to average dissimilarity, both in terms of percentage contribution to overall average dissimilarity and consistency of contribution to overall dissimilarity (judged by a high ratio of average dissimilarity to standard deviation of dissimilarity; Clarke 1993). Species with a high percentage contribution to overall average dissimilarity are often highly abundant but very aggregated in distribution and are inconsistent discriminating taxa; consistent discriminating taxa are often lower in abundance but have less variability between samples. Because these two groups are important in discriminating samples, it is important to consider both when interpreting results. Note that the two groups are not mutually exclusive, e.g., a species with high abundance and high contribution to overall dissimilarity may also be a consistent contributor to differences between samples. We tested the null hypothesis of no significant serial change in fish assemblage structure within each estuary over the 9-yr study period using the PRIMER RELATE routine, which computes an Index of Multivariate Seriation (IMS; Brown et al. 2002) that ranges from 21 to 1 based on Mantel test-like comparisons between actual Bray-Curtis similarity matrices and theoretical distance matrices. Maximal distances in theoretical matrices are between the first and last years of the study period (Somerfield et al. 2002), and high positive IMS values indicate greater conformance with a serial change in assemblage structure over time. Results ENVIRONMENTAL CONDITIONS Annual patterns of river inflow in Tampa Bay and Charlotte Harbor were similar; patterns for both were starkly different between years. Mean daily river inflow from August 2004 to July 2005 was extremely high; both estuaries experienced conditions above the 95th percentile of 1955 to 1995 inflows (Fig. 2). This was also true of 1997 (i.e., August 1997 to July 1998). The high 2004 inflows were attributable to hurricane-related rainfall in summer, whereas the high inflow in 1997 was related to El Nin ˜ o-associated weather patterns in autumn and winter (Schmidt et al. 2001). High inflows, close to the 95th percentile of historic flows, were also evident in 2002. Very low inflows, at or below the 5th percentile of historic inflows, occurred during 1996, 1999, and 2000; some of these were attributable to La Nin ˜ a conditions. The remaining years had inflows that were closer to

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generally occurred in the 1997–1998 and 2002– 2004 periods. OVERVIEW OF FISHES SAMPLED We collected 16,154 samples from August 1996 to July 2005. The ten most abundant taxa in each habitat-gear constituted a large proportion of the catch, ranging from 80.8% in 183-m haul seines to 94.7% in 6.1-m otter trawls in rivers (Greenwood et al. unpublished data). Estuary-resident taxa dominated the assemblages collected in the small-mesh gear, including A. mitchilli and silversides (Menidia spp.). Offshore-spawning, estuary-dependent taxa tended to be most abundant in the large-mesh gear, e.g., pinfish (Lagodon rhomboides), silver jenny (Eucinostomus gula), tidewater mojarra (Eucinostomus harengulus), and ladyfish (Elops saurus). LONG-TERM FISH ASSEMBLAGE STRUCTURE River Shoreline (21.3-m Seine)

Fig. 2. Trends in mean daily river inflow from Tampa Bay (sum of gauges on Little Manatee and Alafia rivers) and Charlotte Harbor (sum of gauges on Peace and Myakka rivers) for the 1996 to 2005 period. Years are grouped from August 1st to July 31st, i.e., 1996 represents August 1st 1996 to July 31st 1997. The median and various percentile inflows for the 1955 to 1995 period are indicated.

historic medians and mostly between 25th and 75th percentiles of 1955–1995 values. Mean water temperatures followed similar trends in both estuaries (all bay 3 year interactions were statistically insignificant in GLM; Fig. 3). There was no significant difference in the mean water temperature between estuaries in river channels, but Charlotte Harbor had significantly warmer temperatures in other habitats. Significant interannual temperature differences were found in river shoreline and bay shelf habitats; low mean temperatures were generally apparent in 2000. Interannual salinity and dissolved oxygen patterns tended to differ between estuaries (four of five bay 3 year interactions were statistically significant in GLM for each variable). Unsurprisingly, salinity was low in high inflow years and vice versa; higher salinities were typically found in Tampa Bay. Dissolved oxygen was relatively low in 1999 (both estuaries); relative highs for Tampa Bay were in 2000, 2002, and 2004, whereas highs for Charlotte Harbor

Small-bodied fish assemblages inhabiting the shoreline of the lower reaches of the main tributary rivers generally differed between Tampa Bay and Charlotte Harbor (Fig. 4). The MDS ordination suggested greater interannual variability in Charlotte Harbor, but this may be due to the different sampling intensities between the two estuaries (18 samples month21 in Tampa Bay, eight samples month 21 in Charlotte Harbor). In Tampa Bay, the 2004 fish assemblage was different from all other years at the 71% Bray-Curtis similarity level. The 2004 assemblage differed from assemblages of other years because of a relatively even division of species that were either more or less abundant in this year compared with other years (Table 1). In Charlotte Harbor, the 2004 assemblage was somewhat different from assemblages in other years, but not markedly so; the 1996 assemblage was notably different from the other years’ assemblages and grouped with assemblages collected in Tampa Bay during all years at 66% similarity (Fig. 4). Taxa that discriminated the 1996 Charlotte Harbor assemblage from the two groups collected during the remaining Charlotte Harbor years (at 71% similarity) included more taxa with higher abundances in 1996 than taxa with lower abundances in this year (Table 1). The structure of fish assemblages in both estuaries did not change linearly over the 9-yr study period (IMS from RELATE test: Tampa Bay: 0.232, Charlotte Harbor: 0.294, both p . 0.05), indicating relative stability from 1996 to 2005. River Channel (6.1-m Otter Trawl) As with the river shoreline assemblage, fishes in the river channel habitat tended to differ between estuaries (Fig. 4). There was complete estuarine

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Fig. 3. Annual mean temperature, salinity, and dissolved oxygen (6 SE) based on data collected from various habitats in Tampa Bay (%) and Charlotte Harbor (&). Years are grouped from August 1st to July 31st, i.e., 1996 represents August 1, 1996 to July 31, 1997.

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Fig. 4. Multivariate analyses of fish assemblages of Tampa Bay and Charlotte Harbor. Ordination plots based on nonmetric multidimensional scaling (MDS) of year-averaged data. Each point represents bay (T 5 Tampa Bay, C 5 Charlotte Harbor) and 12-mo period from August of labeled year to July of following year (i.e., 96 5 August 1996 to July 1997, 97 5 August 1997 to July 1998, etc.). BrayCurtis similarity percentages from hierarchical agglomerative cluster analysis are included as ellipses.

separation at 65% similarity. At the 72% similarity level, the years 2000 (both estuaries) and 2002 (Tampa Bay) were the first to separate from the remaining years in each estuary; hurricane-year assemblages were not notably different from assemblages found in most other years. In Tampa Bay, the 2000 assemblage largely differed from the other 72% similarity assemblages (i.e., 2002 and the remaining years combined) because of many taxa having higher abundances in 2000 (Table 1). Charlotte Harbor’s 2000 assemblage was generally discriminated from the assemblages of other years because of lower abundance of the principal taxa. Fish assemblages in both estuaries showed longterm stability over the 9-yr study period (IMS: Tampa Bay: 0.038, Charlotte Harbor: 0.029, both p . 0.05). Bay Shelf (21.3-m Seine) Fish assemblages of the shallow bay shelf habitat tended to be segregated by estuary. At the 75% level, the 1999 Tampa Bay assemblage was more similar to Charlotte Harbor assemblages than to assemblages in other years within Tampa Bay, and the 2000 assemblage in Tampa Bay was very different from assemblages in all other years there (Fig. 4). The 2001 Charlotte Harbor assemblage separated from all other years at 76% similarity. In Tampa Bay, the 1999 assemblage differed from the major 76% similarity group (including assemblages from 1996–1998 and 2002–2004) mainly by higher

1999 abundances of principal discriminating taxa (Table 1). Taxa that discriminated Tampa Bay’s 2000 assemblage from assemblages in the major group of years were more evenly divided between those that were either more or less abundant in this year compared to other years. The 2001 Tampa Bay assemblage was different from assemblages in the major group of years principally because of low abundances of discriminating taxa in this year. The 2001 Charlotte Harbor assemblage differed from assemblages in the other years because the discriminating taxa were fairly evenly divided between those that were more abundant and those that were less abundant. The discriminating species that decreased in abundance during 2001 were similar for both Tampa Bay and Charlotte Harbor (both shared A. mitchilli, L. rhomboides, silver perch (Bairdiella chrysoura), Eucinostomus mojarras, E. gula, Gulf pipefish (Syngnathus scovelli), and spotted seatrout (Cynoscion nebulosus)). There was relative stability in both estuaries’ fish assemblages from 1996 to 2005, as was indicated by no serial change over the study period (IMS: Tampa Bay: 0.154, Charlotte Harbor: 20.138, both p . 0.05). Bay Shoreline (21.3-m Seine) The small-bodied fish assemblage of bay shorelines largely differed between estuaries (Fig. 4). The relatively high interannual variability in Tampa Bay can be attributed to low sampling intensity (five samples month21 in Tampa Bay over most of the

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TABLE 1. Principal taxa responsible for discriminating outlying years’ fish assemblages in Tampa Bay (TB) and Charlotte Harbor (CH). Outlying years are compared to remaining years on the basis of the MDS and cluster analysis results (see text), and taxa that were either more (+) or less (2) abundant in the outlying year noted. Taxa are ranked according to the number of instances in which they discriminate assemblages. River shoreline (21.3-m seines) Species

Lagodon rhomboides (Pinfish) Anchoa mitchilli (Bay anchovy) Eucinostomus gula (Silver jenny) Bairdiella chrysoura (Silver perch) Eucinostomus spp. (Eucinostomus mojarras) Lucania parva (Rainwater killifish) Menidia spp. (Silversides) Eucinostomus harengulus (Tidewater mojarra) Microgobius gulosus (Clown goby) Syngnathus scovelli (Gulf pipefish) Ariopsis felis (Hardhead catfish) Leiostomus xanthurus (Spot) Trinectes maculatus (Hogchoker) Harengula jaguana (Scaled sardine) Orthopristis chrysoptera (Pigfish) Synodus foetens (Inshore lizardfish) Centropomus undecimalis (Common snook) Cynoscion arenarius (Sand seatrout) Dasyatis sabina (Atlantic stingray) Menticirrhus americanus (Southern kingfish) Sphoeroides nephelus (Southern puffer) Cynoscion nebulosus (Spotted seatrout) Gobiosoma robustum (Code goby) Mugil cephalus (Striped mullet) Strongylura notata (Redfin needlefish) Syngnathus louisianae (Chain pipefish) Archosargus probatocephalus (Sheepshead) Floridichthys carpio (Goldspotted killifish) Fundulus similis (Longnose killifish) Mugil gyrans (Whirligig mullet) Anchoa hepsetus (Striped anchovy) Bagre marinus (Gafftopsail catfish) Chilomycterus schoepfii (Striped burrfish) Elops saurus (Ladyfish) Fundulus grandis (Gulf killifish) Gobiosoma bosc (Naked goby) Membras martinica (Rough silverside) Opisthonema oglinum (Atlantic thread herring) Prionotus scitulus (Leopard searobin) Prionotus tribulus (Bighead searobin) Rhinoptera bonasus (Cownose ray) Sciaenops ocellatus (Red drum) a b

River channel (6.1-m otter trawls)

Bay shoreline (21.3-m seines)

Bay shelf (21.3-m seines)

Bay shoreline (183-m haul seines)

2004 (TB)

1996 (CH)

2000 (TB)

2000 (CH)

1999 (TB)

2000 (TB)

2001 (TB)

2001 (CH)

2004 (CH)

1996 (TB)

1996 (CH)

2ab 2ab 2b — +ab

+ab +a +ab +a 2ab

+a +ab — +ab 2ab

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+ab 2ab 2b 2a 2ab

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2a 2ab 2ab 2a 2ab

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2b +b — — 2b — — — —

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— — 2a +a 2ab — — — —

+ab +b — — — +a +a +b —

+b +b — +a — 2a +a — —

2ab +b — — — 2a +a — —

+ab +b — — — — 2a +b —

— 2b — +a — — — +b —

— — 2ab 2a — 2a — — 2ab

— — 2ab — — +a 2a — 2ab

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+ab +b 2ab

2ab +ab +ab

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2b

2a

















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2ab — — — —

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Discriminating taxon on the basis of contribution to overall average dissimilarity. Discriminating taxon on the basis of consistency of contribution to overall average dissimilarity.

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study period compared to 12 samples month21 in Charlotte Harbor). Sampling intensity in Charlotte Harbor was considerably greater, and 2004’s assemblage clearly separated from assemblages in the remaining years (77% similarity level). The difference in the 2004 hurricane-year assemblage was largely due to decreased abundances of the main discriminating taxa (Table 1). Fish assemblage structure in both estuaries was relatively stable over the 9-yr study period (IMS: Tampa Bay: 20.05, Charlotte Harbor: 0.153, both p . 0.05). Bay Shoreline (183-m Haul Seine) Large-bodied fishes in the bay shoreline habitat were well separated by estuary at the 75% similarity level (Fig. 4). The 1996 fish assemblage was distinguished from assemblages in other years in Charlotte Harbor at the 79% similarity level; at this level of similarity, several small groups existed within the Tampa Bay assemblages, of which the hurricane-year assemblage formed a group by itself but was not greatly different from the assemblages in other years. The MDS representation for the large-bodied bay shoreline fish assemblage was of sufficient quality (Stress 5 0.1) to allow greater attention to be paid to the two-dimensional ordination, as opposed to the results of the cluster analysis, than was the case for the other assemblages (Fig. 4; Clarke and Warwick 2001). In this light, it was apparent that Tampa Bay and Charlotte Harbor shared 1996 as an unusual year. In Tampa Bay, the 1996 assemblage differed from assemblages in the other years primarily because of low abundances of most discriminating taxa (Table 1). In Charlotte Harbor, the 1996 assemblage differed from assemblages in other years because of a fairly even division of discriminating taxa between those that were more abundant in 1996 and those that were less abundant in 1996. There was no serial change in assemblage structure from 1996 to 2005 in Tampa Bay (IMS 5 0.235, p . 0.05), but a significant change did occur in Charlotte Harbor (IMS 5 0.538, p 5 0.001; Fig. 4). Discussion Although Tampa Bay and Charlotte Harbor are proximate and similar in size, clear differences were evident between the fish assemblages in these estuaries. Differences in overall assemblage structure may be due to a combination of geographic location and habitats sampled within each estuary (Monaco et al. 1992; Elliott and Dewailly 1995). These estuaries share many species, but species in each estuary are at different points in their geographic ranges, which may contribute to overall assemblage differences. Although the general habi-

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tats are similar in the two estuaries, they are by no means equivalent; e.g., the riverine habitat of Tampa Bay included the Manatee River, the lower portion of which is close to the bay mouth and includes high salinity areas (Figs. 1 and 2); in our analyses, Charlotte Harbor has no similar river. The main discriminating species are generally more abundant in Tampa Bay than in Charlotte Harbor (Greenwood unpublished data). This may reflect greater ecosystem productivity driven by higher nutrient concentrations in Tampa Bay (McPherson and Miller 1994). Aside from temperature, physicochemical characteristics of the water bodies did not show the same interannual trends in each estuary. This fact alone may explain interestuarine differences in the identity of the apparent ‘unusual’ years in terms of assemblage structure, because assemblages often respond to environmental conditions (e.g., Garcia et al. 2001; Hagan and Able 2003). The majority of fishes sampled in the present study were juveniles of marine or estuarine origin, which have been shown to lack interspecific correlations in relative abundance between areas considerably closer together than Tampa Bay and Charlotte Harbor (Scharf 2000; Kraus and Secor 2005). Genner et al. (2004, p. 659) suggested that a combination of ‘‘differing sampling environments, species compositions and local ecological interactions’’ generate spatially contrasting biotic responses to environmental variation. Overlap in Tampa Bay and Charlotte Harbor assemblages was occasionally evident and generally occurred during periods of extreme conditions, in particular very dry periods (e.g., 1996, 1999–2000). An unprecedented number of hurricanes affected southwest Florida in 2004 (Sallenger et al. 2006), with environmental effects ranging from substantial physical damage in Charlotte Harbor to greatly elevated rainfall and freshwater inputs to estuaries. Note that the latter months of the present study’s final year included the most severe harmful algal bloom (red tide) event since 1971 (see Florida Fish and Wildlife Conservation Commission website, http://research. myfwc.com/features/default.asp?id51018). Hurricane, and possibly red tide, effects appear to have influenced two of the fish assemblages in this study (river assemblages in Tampa Bay and shoreline assemblages in Charlotte Harbor). The distinct assemblage of small-bodied fishes present in the shoreline estuarine portions of Tampa Bay’s rivers during the hurricane year may have resulted from downstream movement induced by enhanced river flows, because organisms may respond to the altered salinity regimes that occur with changing freshwater inflow (Flannery et al. 2002; Kimmerer 2002) or be physically displaced (Burkholder et al. 2004). Taxa normally most abundant in the downstream, higher

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salinity areas of these rivers were relatively scarce (e.g., A. mitchilli and L. rhomboides), whereas those that are normally found in upstream, oligohaline reaches were more abundant during the hurricane year (e.g., naked goby (Gobiosoma bosc) and hogchoker (Trinectes maculatus)). A similar effect on river assemblages was not apparent in Charlotte Harbor; this may be attributable to fish assemblages in Charlotte Harbor being more adapted to greater river flows than those in Tampa Bay (note scale differences in Fig. 2). This higher river flow may already define the Charlotte Harbor fish assemblages for any given year relative to Tampa Bay. The hurricane effect that was evident in Charlotte Harbor, i.e., in the small-bodied fish assemblages along the bay shoreline, may have resulted from a combination of shoreline damage and reduction of gear efficiency. Mangroves fringe much of the shoreline of Charlotte Harbor and widespread mangrove mortality was evident after the hurricane (Mallin and Corbett 2006; Sallenger et al. 2006). Seagrasses occur in close proximity to mangroves (Poulakis et al. 2003), and damage to seagrasses immediately along the shoreline was evident in exposed areas (Stevens personal observations), probably the result of intense wave action during the storm. The presence of sticks and debris along shorelines during the hurricane year could have reduced gear efficiency, resulting in an overall decrease in catch rates. Some species show an increase in relative abundance after the hurricane, suggesting that the effect of reduced gear efficiency may have been minimal. The species that were more abundant after the hurricane include those often associated with nonvegetated bottom (e.g., inshore lizardfish, Synodus foetens; Rydene and Matheson 2003; spot, Leiostomus xanthurus; Stoner 1983), or live in the water column (e.g., silversides, Menidia spp., and redfin needlefish, Strongylura notata; Stevens personal observations). Those that were less abundant include species associated with seagrasses (e.g., L. rhomboides and S. scovelli; Rydene and Matheson 2003) and shorelines (e.g., goldspotted killifish, Floridichthys carpio; Poulakis et al. 2003). Some species may have moved into the damaged shorelines, presumably to take advantage of detritus-based foods associated with the defoliation of mangroves, while others may have lost their cover resulting in higher predation rates or avoidance of damaged areas. Given the paucity of information about how mangrove damage may influence fish assemblages (see review by Manson et al. 2005), we will attempt to examine differences in the fish assemblages found along hurricane-damaged and undamaged mangrove shorelines of Charlotte Harbor in future studies. Although effects of the 2004 hurricane season on fish assemblages were apparent, disruption due to

the influence of hurricanes apparently is not great when compared to perturbations attributable to other factors. Over the 9 yr of the study, conspicuously different fish assemblages tended to occur during or after the La Nin ˜ a-induced drought period, i.e., 1999 to 2001. In some cases, Charlotte Harbor and Tampa Bay fish assemblages exhibited similar responses (e.g., both estuaries share similar species as discriminating 2001 bay shelf assemblages from other years). Other unusual years that were common to both estuaries did not share similar abundance responses of principal discriminating species, e.g., 2000 for river channel assemblages. There was also some evidence that assemblages in 1996 (another drought year) were quite different from those in other years. The 1996 river shoreline assemblage in Charlotte Harbor was more akin to assemblages from Tampa Bay because of increased abundances relative to other Charlotte Harbor years; the increased salinity caused by lower levels of river inflow may have resulted in an assemblage closer to those of the Tampa Bay tributaries. The unusual assemblage structure of 1996’s Charlotte Harbor bay shoreline large-bodied fishes may have been attributable to the increased number of discriminating species that are known to prefer higher salinities and may extend their range further into the estuary during such conditions (e.g., scaled sardine, Harengula jaguana; Atlantic thread herring, Opisthonema oglinum; striped burrfish, Chilomycterus schoepfii; Springer and Woodburn 1960; Stevens personal observations). An entangling net restriction was enacted in July 1995, which may have contributed to an increase in discriminating species that are susceptible to gill nets (e.g., common snook, Centropomus undecimalis; striped mullet, Mugil cephalus; sheepshead, Archosargus probatocephalus) in years following 1996; this may have driven the apparent serial change in assemblage structure from 1996 to 2005. Given the number of tests for serial change that were conducted (i.e., ten), it is possible that this single positive result was spurious, although the observed probability (p 5 0.001) was still well below the Bonferroni-corrected critical value (0.05/ 10 5 0.005). Long-term changes in fish assemblages attributed to enhanced fishery regulations were noted by Fisher and Frank (2002). The present study demonstrated effects related to the multiple hurricanes of 2004, but the changes to fish assemblage structure were generally within the range of variability exhibited over the previous 8 yr. This suggests that the fish assemblages in these estuaries are quite resilient to environmental perturbation. Hurricane-induced fish kills occurred in some areas of the study estuaries, particularly in hypoxic regions of Charlotte Harbor (Stevens personal observations), but it appears that fish

Hurricane Effects on Estuarine Fishes

motility may have mostly mitigated changes at the overall assemblage level. The considerable temporal and spatial extent of this study compelled us to simplify our analyses to average annual fish assemblages. A more detailed study of immediate assemblage change (involving additional post-hurricane sampling in Charlotte Harbor) demonstrated that short-term perturbations were great in several of our study habitats, but that assemblage structure was largely restored within 4 wk of the hurricane (Stevens et al. 2006). Fishery-independent monitoring continues at these locations and will allow us to examine whether the unusual assemblages observed in 2004–2005 (i.e., small-bodied fishes in Tampa Bay rivers and Charlotte Harbor bay shorelines) remain different from the assemblages found during the 1996–2004 baseline years, or if post 2004–2005 assemblages revert to a more familiar structure. It remains to be seen whether the majority of assemblages that were not very different in 2004– 2005 begin to differ as long-term changes take effect. Given the anticipated increase in Atlantic hurricane activity in coming years (Goldenberg et al. 2001), well illustrated by the record-breaking 2005 season, any effects of 2004’s hurricanes may be masked in the future. The present study focused on assemblage-level changes caused by interannual differences in species abundance and composition, but other important, unanalyzed aspects (e.g., mean size, sex ratio, and prevalence of disease) may also have changed throughout the study period or following the multiple hurricanes of 2004. ACKNOWLEDGMENTS We thank the field crews of the Florida Fish and Wildlife Conservation Commission’s Fisheries-Independent Monitoring Program for collecting and processing the data. Support for this study was provided in part by funds from Florida Recreational Saltwater Fishing License sales and U.S. Department of the Interior, Fish and Wildlife Service, Federal Aid for Sportfish Restoration Project Number F-43. Thanks to Judy Leiby and Jim Quinn of the Fish and Wildlife Research Institute for constructive comments on an earlier draft of the manuscript. Many thanks to two anonymous reviewers for insightful reviews that greatly improved the manuscript.

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SOURCE OF UNPUBLISHED MATERIALS MCMICHAEL, R. H. unpublished data. Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, 100 8th Avenue SE, St. Petersburg, Florida 33701 TOMASKO, D. A. personal communication. PBS & J, 5300 West Cypress Street, Suite 300 Tampa, Florida 33607. Received, January 4, 2006 Accepted, March 10, 2006