BULLETIN OF MARINE SCIENCE. 64(3): 465-483. 1999
RECOVERY OF OYSTER REEFS (CRASSOSTREA VIRGINICA) IN A GULF ESTUARY FOLLOWING DISTURBANCE BY TWO HURRICANES
Robert J. Livingston, Robert L. Howell, IV, Xufeng Niu, F. Graham Lewis, III and Glenn C. Woodsum
ABSTRACT During the summer and fall of 1985, two hurricanes struck the Apalachicola Bay system, a center for oyster (Crassostrea virginica) production in the northeast Gulf of Mexico. The first storm, Hurricane Elena, physically destroyed the major oyster-producing reefs in the Apalachicola estuary in early September (9/1/85). This disturbance was followed a month later by considerable accumulations of spat on those reefs most affected by the storm. The second hurricane, Kate, struck the bay in late November (11/21/85) and probably contributed to the natural mortality of young-of-the-year oysters. However, overall oyster biomass did not seem to be affected by Kate. Subsequent oyster growth was substantial with full recovery of the oyster stock noted within a 12-mo period. A detailed evaluation was made of the response of this important estuarine population to these disturbances. The timing and nature of the disturbances relative to the natural history of the oyster were crucial to the overall recovery pattern of the population. Hurricane Elena occurred at the end of the oyster spawn- ing activity in 1985. Effects of the storm probably increased habitat availability and reduced direct competition and predation such that the oyster population benefited from the successful recruitment. The subsequent storm, Kate, coming after the spawning period, was not as destructive to oyster populations as Elena and could have even enhanced growth of the survivors. Hurricanes are common along the Gulf coast during the spawning period of the oysters; it appears that C. virginica is well adapted for such natural disturbances. The ob- served response of the Apalachicola oyster population to successive disturbances has signif- icant meaning in terms of the long-term ecological stability of estuarine populations and the evolutionary aspects of such biological response to temporally unstable habitats. In this case, such populations can be viewed as highly resilient under even the most extreme conditions of physical instability. However, the exact biological response to temporally irregular distur- bances is highly dependent on the timing of such events relative to the natural history of population in question.
Considerable life history data have been published concerning the American or eastern oyster (Crassostrea virginica [Gmelin]). Massive oyster reefs occur along the Gulf of Mexico coast. The location and condition of these reefs depend on many interacting factors which include complex combinations of geological, physical, chemical, and biological processes. Reef oysters, although tolerant to broad ranges of important habitat variables such as temperature and salinity, are susceptible to various forms of physical disturbances whereby reef structure can be adversely affected or destroyed. The success of the American oyster along the Atlantic and Gulf coasts of North America depends on various factors that influ- ence spawning, larval development in the plankton, metamorphosis of the spat stage, successful attachment to a suitable (solid) surface, and development of the sexually mature adult. Harvesting, predation, disease, prolonged low salinities, and physical processes such as wave damage and sedimentation (burial) are all major causes of mortality in the developing oyster. Research on the extensive Apalachicola oyster reefs dates back to the works of Swift (1896) and Danglade (1917). The Apalachicola estuary accounts for about 90% of Florida's commercial fishery (Whitfield and Beaumariage, 1977). Historical surveys indicate that considerable destruction of the Apalachicola oys-
465 466 BULLETIN OF MARINE SCIENCE, VOL. 64, NO.3, 1999 ter resource occurred during the fall and winter of 1893-94 due to storm-related burial and subsequent freezes. Reports of such losses have been relatively frequent from this period to the present although scientific documentation of such impact and subsequent recovery is lacking. Detailed reef descriptions (Swift, 1896) in- dicate similar distributions of oysters existed over the 90-yr period from 1896 to 1985. Conditions in the Apalachicola Bay system are highly advantageous for oyster propagation and growth (Menzel and Nichy, 1958; Menzel et aI., 1966; Livingston, 1984) with reefs covering about 7% (4350 hectares) of bay bottom (Livingston, 1984). Mass spawning takes place at temperatures between 26.5°and 28°C, usually from late March through October (Ingle, 1951). Growth rates of oysters in this region are among the most rapid of those recorded (Ingle and Dawson, 1952, 1953) with harvestable oysters taken in 18 mo. Overall, the oysters in the Apalachicola region combine an early sexual development, an extended growing period, and a high growth rate (Hayes and Menzel, 1981); effective spawning is restricted to older oysters, although young-of-the-year are able to spawn. Tropical storms and hurricanes, relatively common along the northern Gulf coast, are often accompanied by storm surges, waves, strong currents, erosion, sedimentation, flooding, altered salinities, and changes in the physiographic struc- ture of inshore waters (Hayes, 1978). Tabb and Jones (1962) indicated mortality of fishes and invertebrates due to oxygen depletion, sedimentation, and other habitat changes associated with Hurricane Donna. Andrews (1973) found that reduced salinities in Chesapeake Bay caused by Hurricane Agnes accounted for unprecedented changes in the distribution and abundance of various estuarine species. Oyster populations suffered heavy mortalities and were severely stressed but not eradicated. In various rivers, prolonged fresh-water conditions were ac- companied by long-term oyster mortality. Thus, previous studies indicate that the physical impact of hurricanes can lead to a broad range of biological responses depending on the timing and nature of the storms. On 1-2 September 1985, Hurricane Elena, with winds of approximately 200 I Ian h- , struck the Apalachicola system. A maximum storm surge exceeding 3 m was noted near the Apalachicola system with heavy rainfall (>18 cm). The angle of the storm and an extended fetch caused major disturbance in St. George Sound (Fig. 1). The strong storm surge moved in a southwesterly direction along the sound, and, together with heavy sedimentation, caused major physical damage to the Apalachicola oyster reefs in eastern parts of the bay (Livingston, pers. observ.; Berrigan, 1988, 1990). On 21 November 1985, Hurricane Kate struck the Florida coast just west of Apalachicola Bay; at landfall, the storm carried 150 Ian h-I winds with a storm surge exceeding 3.5 m. This hurricane, because of the position of landing and characteristics of the wind distributions as it came ashore, was not associated with observed major physical effects on Apalachicola Bay as was the case with Hurricane Elena (Livingston, pers. observ.). However, within a period of less than three months, two hurricanes struck the Apalachicola Bay system, and these storms occurred during a comprehensive study of the Apalachicola oyster reefs. The Apalachicola Bay system is the major commercial oyster-producing area in Florida. Commercial oystering represents a potential disturbance to the natural population changes of oysters on the chief producing reefs. The 71-80 mm range marks the lower limits of legal oyster catches (>3 in). Oystering activities were ongoing from March through May 1985 throughout the bay, and on selected reefs from May through August 1985. Due to the effects of Hurricane Elena, com- mercial oyster harvesting was suspended in the Apalachicola Bay system by the LIVINGSTON ET AL.: HURRICANES AND GULF OYSTERS 467
012345 10 Km ~ Study Area \j
.'
Figure 1. Distribution of sampling sites showing general boundaries of each oyster reef. These dis- tributions were based on historic oyster distributions, interviews with commercial oystermen and state agency personnel, and recent field studies (Livingston, unpubl. data).
Florida Department of Natural Resources (FDNR) from September 1985 through April 1986. In May 1986, several of the historically best-producing reefs in the eastern section of the bay were opened to oystering. By September 1986, the bay was fully opened to commercial harvesting. The purpose of this paper is to present a series of field analyses of oysters in the Apalachicola Bay system in an effort to define the response of such popula- tions to two hurricanes and temporal patterns of commercial fishing in the estuary.
METHODS Based on previous research in the Apalachicola system (Livingston, 1984), a series of sampling stations was established on both major and minor oyster reefs throughout the Apalachicola estuary (Fig. 1). Oyster reefs where sampling occurred comprised about 59% of the mapped bay reefs (Table 1) and represented the primary oyster-producing areas in the Apalachicola Bay system. Field locations were maintained with LORAN. Monthly water quality data were taken at each station (surface and bottom) from March 1985 through October 1986. Depth (m) was taken along with a standard Secchi disc reading. Salinity was determined with a temperature-compensated refractometer calibrated peri- odically with standard sea water. Dissolved oxygen and water temperature were measured with a Y.S.I. dissolved-oxygen meter. Turbidity was taken using a Hach model 2100-A turbidimeter, and apparent color was measured with an American Public Health Association platinum-cobalt standard test. Cli- matological data concerning local meteorological conditions and hurricane developments were pro- vided by the Environmental Data Service, National Oceanographic and Atmospheric Administration, U.S. Department of Commerce. Oyster samples (multiple) were taken with full head tongs (16-tooth head; 4.5 m handles) at each station on a monthly basis from March 1985 through October 1986. The use of tongs was standardized with respect to opening widths and sampling effort (area covered with one tong = 0.33 m2). To quantify the sampling effort, a series of 30 standardized, random tong samples was taken at the Big Bayou and Cat Point reefs in February 1985. The cumulative size frequency distribution (in lO-mm incre- ments) was determined and plotted for each sampling site. The number of samples necessary for a specified level of quantification was determined according to a method described by Livingston et al. (1976). The method allowed determination of the number of subsamples necessary to achieve specific levels of size class accumulation when compared to the results of 30 subsamples. Seven subsamples 468 BULLETIN OF MARINE SCIENCE, VOL. 64, NO.3, 1999
Table I. List of oyster reefs sampled with estimated areas of oyster distribution at each sampling site. Reefs are grouped by position within portions of the Apalachicola Bay system. Abbreviations (shown in parentheses) correspond to those sites shown in Figure I. Oyster data are given as total numbers per reef, total biomass (g AFDW) per reef, numbers m-2, and biomass (g AFDW) m-2 for oysters averaged over the study period. Table entries for total numbers per reef and total biomass per reef should be multiplied by 106.(*) = oyster spatfall accumulation stations.
Total Total Density Biomass Reef Area (ha) number biomass (Nm-2) (Bm-2) St. Vincent Sound Scorpion* (SC) 190 63,7 46,9 33.5 24.7 Schoelles Lease (SL) 85 13.7 19.3 16.1 22.7 Paradise* (PA) 232 59.2 51.0 25.5 22.0 Big Bayou (BB) 17 5.0 6.6 29.2 38.7 Pickalene* (PK) 30 13.4 3.1 67.2 15.7 Cabbage Top* (CT) 44 17.4 14.9 39.6 33.8 Kirvin's Lease* (KL) 24 1.0 1.8 4.1 7.5 Dry Bar (DB) 72 49.5 11.7 68.7 16.2 Apalachicola Bay St. Vincent (SV) 575 464.0 12.4 80.7 2.2 Pilot's Cove (PC) 20 13.4 3.1 67.2 15.7 Sike's Cut (SK) I 1.4 0.3 43.3 27.3 Nick's Hole (NH) 14 3.9 1.6 28.0 11.1 Hotel (HO) 23 6.2 1.4 26.8 6.3 Sweet Goodson* (SG) 98 89.1 25.2 91.0 25.7 East Bay Gorrie Bridge* (GB) 67 34.8 16.3 52.0 24.3 St. George Sound Cat Point Bar* (CP) 514 1,781 342 347 66.5 Platform (PL) 180 595 87.5 331 48.6 East Hole* (EH) 204 853 97.2 418 47.7 Porter's Bar* (PB) 137 28.9 2.9 21.1 2.2 Shell Point (SP) 18 2.7 0.1 14.8 0.7
accounted for 80.8% (Big Bayou) and 87.5% (Cat Point) of the sampling variability for the total sample. Accordingly, this number of subsamples (located beyond the asymptote for size class accu- mulation) was considered to constitute a representative sample taken in each of the test regions. Numbers of oysters tong-1 were recorded and converted to numbers m-2• All oysters were measured to the nearest mm in the field according to the greatest distance from beak to lip using linear calipers. A total of 140 oysters taken from four stations (n = 35 at each site) was used to determine the relationship of shell length and weight of oyster meat. Four separate length! weight equations were developed to account for known differential growth characteristics in different regions of the bay. In(AFDW) = 2.505·ln(LEN) - 10.980 (Cat Point, r2 = 0.83)
In(AFDW) = 2.303 ·In(LEN) - 10.306 (East Hole, r2 = 0.84)
In(AFDW) = 2.202·ln(LEN) - 9.125 (Paradise, r2 = 0.90)
In(AFDW) = 2.465·In(LEN) - 10.190 (Scorpion, r2 = 0.86) where AFDW is the ash-free dry weight of oyster meat and LEN is oyster shell length in mm. F-tests (P< 0.05) indicated that equations from both bars in the eastern bay (Cat Point and East Hole) were significantly different from equations developed for bars in the western bay (Paradise and Scorpion). Although the differences were not significant within the respective regions, east and west, the site- specific equations were used for the transformations of the length data into ash-free dry weights. This allowed the most comprehensive and accurate use of the data for such transformations. A fifth equation was developed for bars not in the immediate vicinity of the above four reefs and was generated from the baywide pooled data. LIVINGSTON ET AL.: HURRICANES AND GULF OYSTERS 469
In(AFDW) = 2.754·ln(LEN) - 11.742 (all reefs, r2 = 0.86) All tong data (in terms of numerical abundance and ash-free dry wt) were calculated on a unit m-2 basis. These data were then transformed to estimates of total numbers and biomass on each bar (Table 1) based on the estimated size of the bars. Areas were established from computer estimates of oyster- producing areas (Livingston, unpubl. data) based on historic records, interviews with oystermen and state environmental agencies, and our past and ongoing field studies (Livingston, 1984). To standardize our overall collection effort, tong data (oyster density and shell length) were quan- titatively compared with those derived from a series of multiple (0.25 m-2) quadrats taken on the same sampling reefs (Cat Point Bar, East Hole, Paradise) over the same period of study by other researchers (Berrigan, 1990). Tong data were based on seven random samples mo-I station-I while quadrat data were derived from five random samples mo-I reef-I. Comparisons were made only for those months when both types of collections were taken concurrently. Unfortunately, tong and quadrat samples were taken neither on the same date nor from exactly the same location on each reef. These differences undoubtedly introduced some error into the comparisons. Since the data sets deviated from normality, Wilcoxon sign rank tests for paired differences were used to compare monthly densities and shell size between the tong and quadrat collections. Spatfall accumulation was analyzed from a subset of 10 stations (Table 1). Spat baskets, constructed of plastic-coated wire (25 X 25 X 25 cm; 2.5 cm mesh), were filled with about 20 sun-bleached oyster shells and placed at each site. Bricks were placed at the bottom of each basket so that the oysters remained off the bottom to lessen problems with sedimentation. Samples were retrieved, and new sets of oyster shells were set out at two- to three-week intervals. One spat basket was used at each station. Seven shells were randomly chosen from each basket for analysis. Spat counts were made from the inner surface of each valve; this standardization was based on test results that indicated less variance of such adherence on inner surfaces than on outer surfaces. Oyster data were grouped in two ways prior to analysis: (1) bay-wide totals and (2) eastern versus western reefs. In the latter grouping strategy, selected reefs from the eastern bay (Sweet Goodson, Cat Point, East Hole, Platform, Porter's Bar) were compared to selected reefs from the western bay (Big Bayou, Paradise, Pickalene, Scorpion, Schoelles Lease). These reefs were chosen because of their relative commercial importance to overall oyster production in the bay. Intervention models (Box and Tiao, 1975; Pankratz, 1991) were used to analyze the effects of the two hurricanes on the monthly total oyster numbers (in thousands) and the monthly average shell length (in mm) of oysters at the selected reefs in the bay. Three major interventions occurred in the Apalachicola Bay during the study period: Hurricane Elena (combined with the cessation of commercial oystering after September 1985); Hurricane Kate; and the resumption of commercial oystering in May 1986. The models were used to test the possibility that the interventions were significantly associated with level changes in the monthly total oyster numbers (N(t)} and the monthly average shell lengths (S(t)}. Three indicator variables corresponding to the interventions are defined as O, t < September 1985 Xj(t) = { I, t 2: September 1985 O, t < December 1985 X2(t) = { 1, t 2: December 1985
O, t < May 1986 X3(t) = { I, t 2: May 1986
Using B as the backward shift operator such that BX(t) = X(t - I), the relationship between the monthly total oyster number (N(t)} and the three interventions can be described by the following general intervention model:
N(t) = [30 + vi(B)XI(t) + v2(B)X2(t) + v3(B)X3(t) + ~(t), (1)
where vi(B), viB), and viB) are polynomials with the typical form;
v(B) = 000 - w,B - ... - whBh
where {wo,w" ... ,wh} are parameters to be estimated. In model (I), f30 is a constant and ~(t) is a noise term which is often modeled as a stationary autoregressive moving average (ARMA; p, q) process with
W) - ,W - 1) ... -
35 35 , 30 ~ 30 ~ 0 ! !f:f : !~!! • Q. 25 L. 25 ! ! e CD '1 ' 20 a 20 !! : ~ ! ~ III :~ 15 fIll 1fHIffPffP •...15 : '! i1 III o iii 8- o '1, 10 E 10 en CD 5 I- 5 0 0 0
Elena : : Kate 140 , 12 Elena : : Kate Jii'120 10 § 100 : :!! f! ~ 8 C) 0 80 0.!. .§. 8 ffthnf~ HUftt ~ 60 'I d 4 40 f HI 5 ci , 0 , 0 20 f It : f~ I 2 , ftf ! , 0 0 MAMJJASONDJFMAMJJASO MAMJJASONDJFMAMJJASO 1985 1986 1985 1986
Figure 2. Temperature CC), dissolved oxygen (mg L-I), salinity (%0), and color (Pt-Co units) in bottom waters of the Apalachicola estuary. Data were averaged (± SO) over all stations by month from March 1985 through October 1986. directions. First, the biological response, in this case either monthly total oyster number series (N(t)} or monthly average shell length (S(t)}, may react to an intervention with a time lag. For example, the term vl(B)XI(t) = WeXI(t) - WIXI(t- I) - ... - WJCI(t- h) in model (I) indicates that the impact of the first intervention is distributed across several time periods. Second, instead of assuming that the errors ~(t) are independently distributed, ARMA(p, q) models are used for ~(t) which incorporate possible serial correlations in the response series. All intervention models were fitted using the Linear Transfer Function Identification Method proposed by Pankratz (1991). Only those coefficients where the computed t-ratio exceeded the critical t-value (t = 2.10; P < 0.05) were incorporated in the final models. Diagnostic checks included both residual autocorrelation analysis and cross correlation anal- ysis of the model residuals with residuals of each input series. Significant correlations in either of these checks may indicate an incorrect final model. In addition to the overall oyster data, intervention models were fitted to eastern and western sections of the bay using numbers m-2 and average shell length (in mm) of oysters from stations in these areas. The four series were denoted by EN(t) and WN(t) for eastern and western densities and by ES(t) and WS(t) for eastern and western shell lengths. Intervention models were fitted to the four series sepa- rately.
RESULTSANDDISCUSSION HABITATCONDITIONS:HURRICANEINFLUENCE.-The mean depth for all stations was 1.2 m, ranging from 0.5 m to 2.1 m. The relatively shallow depths of the oyster reefs constituted a factor in the effects of the hurricanes. Secchi depths were relatively uniform throughout the estuary (range of means: 0.5-1.0 m). Dis- solved oxygen values were lowest at some stations in September 1985 Gust after Hurricane Elena) and from June through October 1986 following a major drought in 1986 (Fig. 2). Dissolved oxygen concentrations (Fig. 2) remained above 4.0 mg L-I throughout most of the study and were not considered an important stress factor on the Apalachicola Bay reefs. High color values in the bay during Sep- tember 1985 reflected the impact of Hurricane Elena. In addition, there were some reductions of salinity after both hurricanes; however, such salinity changes were LIVINGSTON ET AL.: HURRICANES AND GULF OYSTERS 471
short-lived. Overall water quality effects due to the storms were considered mod- erate compared to the natural seasonal variation in the Apalachicola system. The ensuing drought during 1986 was associated with high summer temperatures and salinities in the estuary and somewhat lower color and dissolved oxygen. Although various water quality factors were somewhat affected by the hurri- canes, the chief effects on the reefs were physical. The sustained winds of Hur- ricane Elena, moving from northeast to southwest in the Apalachicola region, caused considerable structural damage to the eastern reefs (Porter's Bar, Platform Bar, Cat Point Bar, Sweet Goodson's, East Hole) due to abrasion, sedimentation, and extreme turbulence from wave action and water movement (Livingston, pers. observ.; Berrigan, 1990). By contrast, Hurricane Kate had winds from the south that did not have the direct force of extreme water flow (and the associated phys- ical impacts on oyster reef structure) observed during Hurricane Elena (Living- ston, pers. observ.). DENSITY,BIOMASSANDGROwTH.-Results of the comparison of the quadrat and tong data are shown in Figure 3. Overall, the two data sets were comparable. The primary differences in density and mean size were most evident in the Cat Point and East Hole data during the heavy recruitment in October and November 1985. Statistical analysis of the grouped (all stations, all dates) data indicated that the monthly densities estimated from the tong data were not significantly different (P > 0.05) from those estimated with the quadrat method. When the months of October and November (the major recruitment period in 1985) were excluded from the analysis, a significant difference (P < 0.05) was noted. Analysis of the average size data indicated just the opposite effect. Means from the tong collec- tions were significantly different (P < 0.05) from the quadrat samples when data were grouped (all stations, all dates); however, no significant differences (P > 0.05) were noted when the October and November data were excluded. These results are consistent with the fact that small oysters (i.e., <25 mm) were not counted in the quadrat analysis while individuals as small as 10 mm were included in the tong samples. This inclusion increased the density and decreased the shell size estimates based on tong samples during the recruitment period. Overall, col- lections taken with both methods were reasonably similar; sampling results of this study are thus directly applicable to quantitative estimates of the numbers and mean size distributions of oysters present in the Apalachicola estuary over the sampling period. The overall distribution of oysters in the Apalachicola system is summarized in Table 1. Cat Point, East Hole, and Platform bars were by far the most produc- tive of the various oyster-producing areas of the bay in terms of total estimated reef numbers and biomass (averaged over all sampling dates from March 1985 through October 1986). These three areas were also characterized by the highest oyster densities and biomass m-2• High oyster productivity in these areas was due both to the extensive areas of the reefs as well as the high mean density and biomass. Western sections of the bay produced relatively fewer oysters than the eastern sections. This was true both in terms of numbers m-2, biomass m-2, and, with the exception of Paradise reef, overall area of oyster distribution. Temporal trends of total numbers, numbers m-2, biomass m-2 and mean shell length of the oysters in the Apalachicola system are given in Figure 4. In the bay as a whole, there was a major decrease in total numbers, numbers m-2 and biomass m-2 from August to September 1985 (coincident with Hurricane Elena); mean shell size was little affected by the storm's passage. Numbers and biomass of oysters reached low points in the study period during September 1985. Berrigan (1990) also found substantial reductions of oyster numbers during this period 472 BULLETIN OF MARINE SCIENCE, VOL. 64, NO.3, 1999
Cat Point 1400 100
1200 Otong 80 -o-tong co __ quadrat E 1000 _quadrat E -.:: .a S- 60 800 GI .s N ~ l:- 600 7i 'ii c: 40 c: GI 400 I 0 :! 20 200
0 0
East Hole 2500 100
••• 2000 80 E E "i:: .a 1500 S- 60 GI S N 'ii ~ 1000 40 II) c: c: til GI GI o 500 ~ 20
o 0
Paradise 140 140
120 120 co~ E 100 E 100 S- 1S 80 GI 80 .s N 7i l:- 60 60 c: 'ii til i 40 GI 40 ~ o 20 20
o 0 MAMJJASONDJFMAMJJAS MAMJJASONDJFMAMJJAS
1985 1986 1985 1986
Figure 3, Mean oyster density (number m-2) and shell size (mm) compared from tonged (this study) and quadrat samples (Berrigan, 1990) on three reefs in Apalachicola Bay. Comparisons were based on seven tongs and five quadrat samples taken at the most productive oyster reefs in the bay during selected months from March 1985 through September 1986. which he attributed to the effects of Hurricane Elena. A primary feature of the numerical trends was the sizable recruitment just after Hurricane Elena (Fig. 4); numbers of oysters in the bay peaked during October-November 1985. During the period from September to October, mean size was reduced to lows for the period of record due to the combined loss of adult oysters during the hurricane and subsequent recruitment of small oysters. Considerable losses of numbers (but not biomass) occurred among the young-of-the-year throughout the fall of 1985. These decreases in young-of-the-year numbers likely reflected natural mortality, as commercial oystering was prohibited from September 1985 to May 1986. Dur- ing the fall to early winter period, biomass m-2 increased rapidly (Fig. 4). Num- bers of oysters were relatively stable from December 1985 through April 1986 LIVINGSTON ET AL.: HURRICANES AND GULF OYSTERS 473
12000 _Numbers 80
- -0- Average size '"•...0 10000 70 ~ CD ~ iii 8000 60 (Q U)•... CD CI) 50 U) .c 6000 N" E ::J CD c::: 4000 40 3" (i'i (5 2000 30 2- I- 0 20 : Elena: : Kate : Oystering : resumed 300 70 : _Density : N' 250 : -o-Biomass 60 E : : to ";;:: 50 0" .c 200 : 3 .s ll) : 40 en ~ 150 en "iii 30 iO c::: 100 Q) 20 --3 Cl ~ 50 10
0 0 MAMJJASONDJFMAMJJASO 1985 1986
Figure 4. Total numbers of oysters, numbers m-2, mean shell size (mm) and ash-free dry wt biomass m-2 for all stations (averaged) from March 1985 through October 1986. The timing of Hurricanes Elena and Kate are shown along with the date when oystering was resumed (commercial harvesting ceased immediately following Hurricane Elena). with growth continuing from October 1985 to May 1986. Overall numbers and biomass of oysters in the bay declined in May 1986 coincident with the resump- tion of commercial harvesting. The intervention model in (1) was fitted to the monthly total oyster numbers in the bay. The final identified model for this series was (2) with no serial correlation indicated in the noise process ~(t). The estimated pa- rameters in the final identified model are presented in Table 2A. When Hurricane Elena was followed by massive recruitment of young oysters on the damaged reefs, which resulted in a substantial increase in oyster numbers after about one month. The fitted model showed that the monthly total oyster numbers in the bay increased significantly in October (with a I-mo lag after the intervention). When hurricane Kate struck the bay on 21 November 1985, oyster densities were already in decline before the hurricane, and it is likely that the lower numbers in Decem- ber 1985 reflected both natural mortality and hurricane effects. Finally, the re- sumption of oystering in the bay beginning in May 1986 was associated with a significant reduction in the monthly total oyster numbers. The fitted model showed that the levels of monthly total oyster numbers during the four different periods (before Hurricane Elena, between Elena and Kate, between Kate and May 1986, and after May 1986) were significantly different. The coefficient of determination (r2) of the fitted model indicated that the three intervention variables explained 474 BULLETIN OF MARINE SCIENCE, VOL. 64, NO.3, 1999
Table 2. Results of the application of the intervention models to bay-wide oyster data in the Apa- lachicola system taken monthly from March 1985 through September 1986.
Estimated Standard Variable coefficients error T-ratio
A. Estimated parameters in the intervention model for the monthly total oyster numbers (in ten thou- sands). Intercept 839 314 2.68 XI (t - I) 9,473 627 15.1 X2 (t) -4,415 643 -6.87 X, (t) -1,298 465 -2.79 R2 = 0.95 B. Estimated parameters in the intervention model for the monthly average shell length of oysters (in mm). Intercept 67.2 1.76 38.2 XI (t - I) -33.4 3.05 -11.0,
X2 (t - I) 11.0 3.29 3.33 X, (t) -5.55 2.78 -2.00
R2 = 0.93 about 95% of the variation in the monthly total oyster number series during the study period. The intervention model for the monthly average shell length of oysters in the bay was identified as
Set) = Eastern Reefs Western Reefs 1600 400 ~1400 350 N ~ 1200 300 ... , :S 1000 250 , 800 0 200 , ~ 0 , 'iii 600 150 c: Gl 400 100 C 200 f 50 0 I! Iiw 0 :....•!J! Elena : : Kate : Oystering Bena : ; Kate ; Oystering 100 140 , resumed , resumed o 120 e- 80 s. 100 60 Gl 80 enN 40 60 HdHlwuhI fa Iff·tfl 1.i'l.ilflf! 40 Gl 20 " , fll!! ::i: 20 " 0 : t: : '0 0 0 0 MAMJJASONDJFMAMJJASO MAMJJASONDJFMAMJJASO 1985 1986 1985 1986 Figure 5. Average number m-2 and mean shell size (mm) of oysters taken at stations representing the eastern (Cat Point, Sweet Goodson, Platform, East Hole, Porter's Bar) and western (Scorpion, Big Bayou, Pickalene, Paradise, Schoelles Lease) sections of the Apalachicola Bay system. Data were taken monthly from March 1985 through October 1986. Monthly oyster density (numbers m-2) patterns differed between western {WN(t)} and eastern {EN(t)} sections of the bay. The intervention model for the monthly oyster density series {EN(t)} had the same form given in (2) which is the model for the monthly total number of oysters in the whole bay system. The intervention model for western bars {WN(t)} was WN(t) = 133X3(t - 3) + ~(t), (4) in which the noise series [~(t)] followed an AR(1)model with the form ~(t) = Table 3. Estimated parameters in the intervention models in the eastern and western sections of the bay for oyster data taken monthly from March 1985 through September 1986. Estimated Standard Variable coefficients error T-ratio A. Estimated parameters in the intervention models for the monthly density in eastern and western sections of the bay. Eastern Reefs Intercept 69.4 16.9 4.12 XI (1 - l) 668 33.7 19.8 X2 (1) -406 34.5 -11.8 XJ (1) -128 25.0 -5.13 R2 = 0.97 Western Reefs XJ (1 - 3) 64,9 20.2 3,22 <1>1 0.97 0.12 8.08 R2 = 0.94 B. Estimated parameters in the intervention models for the monthly average shell length of oysters in the eastern and western sections of the bay. Eastern Reefs Intercept 55.0 2.15 25.6 XI (1 - I) -37.1 3.72 -9.97 X2 (1 - I) 19.8 3.46 5.73 R2 = 0.87 Western Reefs Intercept 88.7 4.24 20.9 XI (1 - l) -20.8 5.78 -3.59 XJ (1) -25.4 5.78 -4,40 R2 = 0.80 than to some lagged influence of the resumption of oystering at eastern bars. Unlike other intervention models identified in this study, the noise series {E(t)} in the model for {WN(t)} showed strong serial correlations. Intervention models were identified for the monthly average shell size for east- ern {ES(t)} and western {WS(t)} reefs. The model for {ES(t)} was identical in form to that specified in (3) for the monthly average shell size of oysters in the whole bay, except that the third intervention was not statistically significant. The identified intervention model for {WS(t)} had the form WS(t) = ao + ajX.(t - 1) + a3X3(t) + E(t). (6) The estimated parameters in the two models for {ES(t)} and {WS(t)} are listed in Table 3B. The relationships of the two hurricanes with the series {ES(t)} were similar to those on the monthly average shell size of oysters in the whole bay. The second hurricane, Kate, was not significantly related to the monthly shell size of oysters in the western bay. This was probably influenced by the limited damage to adult oyster populations here along with a relatively poor recruitment in western areas during 1985. Berrigan (1990) discussed the generally poor recruitment in the western bay as a consequence of the patchy, unconsolidated nature of the reefs. Contrary to these findings, the resumption of oystering was correlated sig- nificantly with shell size in western reefs but not in eastern bars. As with {WN(t)}, this was likely due to good recruitment following peak:spatfall in June 1986 and the loss of the 31-40 mm size class (Figs. 6,7). LIVINGSTON ET AL.: HURRICANES AND GULF OYSTERS 477 Eastern Reefs Western Reefs ~ 50 ~ 40 "iii .r; 30 ~rn as a. 20 CJ) .0 10 z ! 0 I MJJASONDJFMAMJJASO MJJASONDJFMAMJJASO 1985 1986 1985 1986 Figure 6. Oyster spatfall (mean number of spat shell-I wk-') in eastern (Cat Point, Sweet Goodson, Gorrie Bridge, Platform, East Hole) and western (Scorpion, Cabbage Top, Pickalene, Paradise, Kirvins Lease) reefs within the Apalachicola estuary collected every 2-3 wks from March 1985 through October 1986. The data indicated that, following a stable period with relatively low densities of oysters during the summer of 1985, Hurricane Elena destroyed the primary oyster-producing areas in eastern portions of the Apalachicola system. Major oys- ter recruitment was noted in eastern sections that were most affected by the hur- ricane; oyster numbers may have been thinned out in November 1985 by Hurri- cane Kate thus exacerbating existing, natural levels of oyster mortality. The com- bination of specific attributes of the hurricanes and the timing of these storms relative to the natural history of the oysters defined to a considerable degree the nature and extent of the impact and response of this population. Although the .=109 oysters ~Ie,:,al. I~a~ · Il?ys~ri~g . 141-150 resumed 131-140 I· I· · \. 121-130 ,...., 1 I 1 E 111-120 E 101-110 I. I. · I. '-' 91-100 l/) I' I' · I' Q) 81-90 • • l/) · I' I' • I • l/) 71-80 · · • . . . · · CIS • • • • • • · I. ·I. • • U 61-70 • • • • • • I. . • • • • Q) 51-60 • • • • • · I· · I· . .1. • N · · • ••• • Vi 41-50 • • • · I· · I· • 31-40 •· · . .~...... • • · I ·I· • ••••••• 21-30 · • · ••••••• 11-20 • I. • •• 1 •••••• 1-10 • ••• • • N A N J A S 0 N 0 J F N A N J J A S 0 1985 1986 Figure 7. Oyster numbers by size class by month from March 1985 through October 1986. The area of the circles is proportional to the square root of the total numbers of oysters by size class in the Apalachicola estuary. 478 BULLETIN OF MARINE SCIENCE. VOL. 64. NO.3. 1999 storms (especially Hurricane Elena) had a major economic impact in virtually destroying the Apalachicola oyster industry (Berrigan, 1988, 1990), the resilience of the oyster and the fortuitous timing of the storm (before spawning was com- pleted) allowed rapid recovery. Hurricane Kate, in possibly thinning out the newly settled oysters, may have provided improved growing conditions for the survivors by reducing competition. Subsequent increases in biomass were substantial during the winter-spring of 1985-86 prior to the resumption of oystering in May. Modest recruitment during the summer-early fall of 1986 enhanced full recovery of system numbers and biomass in less than 1 yr from the occurrence of Hurricane Elena. SPATFALLANALYSIs.-Theseasonal pattern of spatfall (Fig. 6) differed between eastern and western sections of the bay over the period of study. During 1985, oyster spat were first detected in eastern sections of the bay in June with incre- mental increases in July and August. By early October, there was a major spatfall event that was indicative of increased spawning around the time of the early September hurricane. In 1986, the spatfall in the eastern parts of the bay was highest during June; subsequent levels were relatively low, with slight increases in August and September. The lowest spatfalls were noted in May and late Sep- tember-October 1986. Western sections of the bay were characterized by rela- tively low oyster spatfall during 1985. In 1986, there was a major spatfall in early June with a subsequent smaller peak during September. Thus, there were consid- erable differences in oyster spatfall between eastern and western areas of the Apalachicola estuary. Ingle (1951) attributed this disparity to greater fluctuations and lower averages of temperature in western parts of the bay. Berrigan (1990) noted limited reproductive success in the western areas relative to the eastern sections of the bay. He suggested this difference was a function of the high density, consolidated nature of the eastern reefs compared to the low density, patchy nature of the western reefs. Fertilization and subsequent settling of larvae on suitable substrata (particularly other oyster shells) are presumably enhanced over dense, highly aggregated reefs. Olguin-Espinoza (1987), in a study of repro- ductive processes of Apalachicola Bay oysters (March 1985-March 1986), found that peak levels of gametogenesis occurred during spring months with spawning at temperatures above 25°C. Spawning ended in October 1985 and was timed with reductions of water temperature. Hurricane Elena did not have an effect on the gonad condition of the surviving oysters. There was no indication that Hur- ricane Elena had an effect on the spawning activities of the Apalachicola oysters. The relatively high standard deviations of spatfall indicated substantial station- to-station variation. In terms of spatfall (number of spat shell~1wk-I), the primary regions of the bay contributing to the October 1985 spatfall event included Gorrie Bridge (60.6), Sweet Goodson's (45.2), East Hole (16.3), and Cat Point (14.6). These eastern reefs were also the most seriously damaged areas during Hurricane Elena although the connection of the storm with spatfall occurrence remains un- documented. The highest observed densities of spat and young oysters over the entire study were found in these areas during October 1985. Most of the oyster reefs in Apalachicola Bay and St. Vincent Sound had moderately low to low numbers of oyster spat at this time. During the June 1986 peak of spatfall, the primary recruitment areas included Pickalene (38.3), Cabbage Top (35.8), and Scorpion (16.2) in the western bay with lesser concentrations at eastern reefs such as Porter's Bar (14.6), Cat Point (12.7), and East Hole (9.6). These data indicate that at least part of the high productivity of the eastern bars is due to continued high levels of spatfall. It is possible that the combination of available habitat and the lack of competition and predation from existing oysters and oyster predators contributed to the success of the spatfall in fall 1985. Thus, the primary factors LIVINGSTON ET AL.: HURRICANES AND GULF OYSTERS 479 that contribute to the population structure of the oysters in the Apalachicola es- tuary include habitat features (temperature, salinity), the extent of suitable bottom type, successful spatfall on a year-to-year basis, and the response of the population to natural disturbances such as storms and biological factors such as competition and predation. TEMPORALCHANGESINPOPULATIONCOMPOSITION.-Monthlysize frequency data of oysters in the Apalachicola Bay system (Fig. 7) reflect the effects of various disturbances over the period of study. Between March 1985 and July 1985, re- cruitment of newly spawned oysters was low. Spatfall was low during this period. By June, there were reductions in most size classes; such low levels persisted during the early summer months, particularly among the larger oysters (>71-80 mm). By August 1985, increased spatfall was accompanied by recruitment of the smaller size classes (10-30 mm) which was associated with increased local rain- fall and periodic reductions in salinity. Hurricane Elena, occurring at the begin- ning of September, had a devastating effect on the oyster population of the Ap- alachicola estuary with a decrease of oysters by almost an order of magnitude to the lowest levels recorded in this study. By October, there was a major recruitment of young oysters; this recruitment was consistent with the spatfall record (Fig. 6) and continued into November 1985. Over this period, there was no appreciable increase in oysters above the 71-80 mm size class despite the fact that commercial oystering had been suspended. The effects of Hurricane Kate could have contrib- uted to ongoing reductions of the youngest size classes; there was, between No- vember and December 1985, a loss that approached 50% of the new crop of oysters. By the end of December 1985, there was evidence of increased growth of the remaining oysters. It is possible that this growth was aided by reductions of oyster numbers due to Hurricane Kate. Increases of the remaining young-of- the-year oysters were noted in the size classes between 21 and 100 mm with substantial increases in the 21-30 mm increment. Thus, the impact of the two storms depended to a large degree on the timing of the individual disturbances relative to the stage of the life cycle of oysters in the Apalachicola Bay system. Hurricane Elena occurred prior to the end of the spawning season and, although the hurricane was extremely destructive to existing adult oysters, it did not pre- clude major recruitment success during the following fall period. This event could have created a set of environmental conditions that actually contributed to the success of the succeeding cohort of young oysters. Hurricane Kate, with less adverse impacts on the existing oysters in the bay, did not substantially affect biomass increases of the surviving oysters and could have actually enhanced growth of these oysters by reducing competition. From January 1986 through April 1986, there was a generally high growth rate of the younger cohorts with no discernible changes in overall numbers of oysters. The numbers of legally obtainable oysters did not change substantially. The return of commercial oystering in the bay during the late spring of 1986 coincided with reductions in the bay oyster numbers. From June through August, there was re- cruitment of young oysters which brought total numbers up to post-Kate levels. Commercial-sized oysters more than doubled to levels comparable to or exceeding pre-hurricane numbers as the growth of the post-Elena population continued. The commencement of full-scale commercial oystering in the fall of 1986 was accom- panied by reductions of selected size classes. By October 1986, oyster numbers stabilized; there were increased numbers of commercial-sized oysters due to growth at most levels of the overall population. In this way, the oyster population in the Apalachicola estuary reflected growth of the fall 1985 young-of-the-year cohort together with summer 1986 spatfall recruitment. The resumption of com- 480 BULLETIN OF MARINE SCIENCE. VOL. 64. NO.3. 1999 mercial oystering during the spring and fall of 1986 may have affected the pop- ulation age-class distribution although such changes were also undoubtedly af- fected by the high June spatfall in that year. It appears that the Apalachicola Bay oyster population had fully recovered from the effects of the fall 1985 storms. Such resilience was due in large part to the successful recruitment that followed Hurricane Elena in eastern sections of the bay that were most affected by the hurricane. EXTREMEEVENTSANDBIOLOGICALRESILIENCE.-The observed changes in the Apalachicola oyster population should be placed within the context of long-term changes of major habitat controlling features such as Apalachicola River flow. Meeter et al. (1979) found that oyster landings from 1959 to 1977 were correlated negatively with river flow. The highest oyster landings coincided with drought conditions. Wilber (1992), using oyster landings from 1960 to 1984, found that river flows were correlated negatively with oyster catch per unit effort within the same year and positively with catches 2 and 3 yrs later. Highest oyster harvests occurred in 1980-1981, coinciding with a major drought. Predation on newly settled spat during periods of high salinity was given as a possible explanation of the 2-yr time lags between low flow events and subsequent poor production. Livingston et al. (1997), however, found that increases of the Apalachicola Bay non-oyster bivalve mollusk populations during droughts were related to changes in the trophic organization of the estuary. They suggested that relatively high, non-oyster bivalve production during low flow years was probably due to in- creased primary productivity as a function of altered physical conditions (i.e., increased light penetration) in the receiving estuary. Increased productivity con- tributed to increased growth rates and ultimately increased bivalve production. Such changes in river flow and productivity were regular and occurred within prescribed progressions of river flow fluctuations. This trophic explanation was suggested as an alternative to the predation hypothesis put forth to explain the observed relationship between flow and oyster productivity (Wilber, 1992). Hur- ricane effects, on the other hand, represent asymmetrical events, with population response dependent on both the timing of the incident and the state of the pop- ulation just prior to the storm. The concepts of biological stability and resilience have been defined in various ways (see Harrison, 1979, and Santos and Bloom, 1980, for a brief review of the semantic problems encountered). Stability is generally defined as the ability of a given system, once perturbed, to return to its previous state. Resilience refers to the degree, manner, and pace of restoration of the initial system function and structure following a disturbance (Westman, 1978). Cairns and Dickson (1977) referred to various parameters of a recovery index: proximity of recolonization sources, mobility of propagules, physical and chemical suitability of habitat for recolonization, toxicity of the disturbed habitat, and effectiveness of human man- agement initiatives to facilitate rehabilitation. By these criteria, the high degree of resilience of the Apalachicola oysters to massive disturbance can be examined. Following a devastating physical event, the remaining oysters in the bay, along with a relatively prolific mode of reproduction, provided the means of the noted recovery. At the time, there was ample habitat available for settlement. Within one or two weeks, habitat conditions were highly favorable for spat accumulation. Salinity conditions showed a rapid recovery to pre-storm conditions. The loss of existing oysters and various natural predators apparently enhanced spat coloni- zation, and could have been an important factor in the oyster recovery process. Subsequent shell-cultching activities of the Florida Department of Natural Re- sources also aided in the habitat rehabilitation. Thus, the habitat conditions and LIVINGSTON ET AL.: HURRICANES AND GULF OYSTERS 481 natural history of the oysters were favorable to the high level of resilience of the Apalachicola population in response to the destructive effects of the hurricanes. The response to repeated disturbances may take various forms (Westman, 1978), but, in most instances, such response is more extreme with each repetition. The timing of successive interventions is crucial in the effects on subject popu- lations. Hurricane Kate occurred after the spawning season had ended so that recruitment was no longer a factor. The subsequent declining numbers due to natural mortality of the new cohort could have been further affected by Hurricane Kate, although oyster biomass continued to increase indicating that the survivors could have benefited from the selective mortality engendered by the storm. Once again, the nature of the disturbance relative to local habitat conditions and the life history stage of the organism contributed to the population response. Bohn- sack (1983) has pointed out that past experimental studies of disturbances have suffered from scaling problems, and relatively few field studies have sufficient data taken prior to the disturbance for an adequate evaluation. In a review of the influence of the record cold spells on fishes in the Florida Keys, Bohnsack (1983) found a high rate of recruitment of juvenile fishes, presumably due to reduced competition and/or predation, which added to the generally high resilience of reef fishes to regional disturbances. Such response parallels that of the Apalachicola oyster population. Although the competition/predation explanation is favored by parsimony, other explanations of the observed resilience of the oyster population remain possible. These include the increased success of succeeding spatfall as a result of possible increases of primary productivity, altered current patterns, and increased levels of habitat availability due to as yet unknown mechanisms. Thus, the processes of recovery depend on the timing of the disturbance relative to the life history stage of the subject population; this amounts to a stochastic response within a relatively structured life history progression. CONCLUSIONS The occurrence of two hurricanes in the Apalachicola estuary during a field study of oysters provided a natural experiment that allowed the close surveillance of the response of a population to a series of natural and anthropogenous distur- bances. The nature of the impact of the storms depended on various factors. The effective aspects of the disturbance included the dimensions and timing of the storms, local existing habitat conditions, and the life history stage of the subject population at the times of the disturbances. Storms, including hurricanes, occur frequently along the northern gulf coast. Hurricanes occur with the highest fre- quency during summer-fall months, overlapping the usual spawning season for oysters. The key to the adaptive response to the destruction of major portions of the oyster population by the first storm was a highly successful spatfal!. Had Hurricane Elena struck during the winter months, it is doubtful that there would have been a rapid recovery of this population. Conditions were such, in terms of adequate habitat, that the spat were able to survive in considerable numbers after the hurricane. The second hurricane, Kate, occurred after the spawning season, was not associated with major reductions of the new cohort and could have aided in the rapid increase in biomass of the survivors through some possible combi- nation of factors such as reduced competition for food, space, and other factors associated with crowding. Reproduction and subsequent successful recruitment and growth in eastern parts of the bay were likely due to the generally higher reproductive capacity of the oysters here relative to the less productive western oyster reefs. There were thus differential effects on the overall population that 482 BULLETIN OF MARINE SCIENCE, VOL. 64, NO.3, 1999 depended on specific biological differences among different oyster reefs. Obvi- ously, oysters are relatively well adapted to disturbances such as storms, even when the immediate effects include substantial damage to the existing population. Under such circumstances, the resilience of the oysters was enhanced by specific aspects of its life history that included rapid and considerable spawning capabil- ities, a relatively high rate of growth due to the usually optimal habitat conditions in the Apalachicola estuary, and the return of habitat availability and natural productivity of this system within days to weeks of the disturbance. The return of the Apalachicola oyster population was aided by other by-products of the storm that included the absence of natural predators (including human beings). Com- mercial oystering has a significant impact on the density and population structure of oyster reefs. The overall outcome of oyster population changes thus indicated an adaptive response and high resilience of this species that allows survival under even extreme conditions of natural stress. Stochastic natural disturbance could even be viewed as an important stimulus to the long-term productivity of species such as oysters that are already well adapted to the rigors of a river-dominated estuary. ACKNOWLEDGMENTS Funding for this project came in part from the Center for Aquatic Research and Resource Manage- ment (Florida State University), the Franklin County (Florida) Board of County Commissioners, the Florida Department of Environmental Regulation, the U,S, Man and the Biosphere Program, and the Florida State University COFRS program. The data analysis was aided by a grant from the Northwest Florida Water Management District. Analytical work was carried out by L. E. Wolfe and J, Jimeian. This manuscript benefited greatly from the comments and suggestions of M, Berrigan (Florida De- partment of Environmental Protection) and two anonymous reviewers. LITERATURE CITED Andrews, J, D. 1973. Effects of Tropical Storm Agnes on epifaunal invertebrates in Virginia estuaries. Ches. Sci. 14: 223-234. Berrigan, M. E. 1988. Management of oyster resources in Apalachicola Bay following Hurricane Elena, J, Shellfish Res. 7: 281-288, ---. 1990. Oyster resources in Apalachicola Bay. Unpub, Rpt. 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Shellfish management in Apalachicola Bay: Past, present, and future. Pages 130-140 in R. J. Livingston and E. A. Joyce, Jr., eds. Proceedings of the conference on the Apalachicola drainage system. Fla. Dept. Nat. Res., Mar. Res. Pub!. 26. Tallahassee, Florida. 177 p. Wilber, D. H. 1992. Associations between freshwater inflows and oyster productivity in Apalachicola Bay, Florida. Estuar. Coast. Shelf Sci. 35: 179-190. DATESUBMITTED:November 26, 1996. DATEACCEPTED:June 25, 1997. ADDRESSES:(R.J.L., R.L.H.,G.C.W.) Center for Aquatic Research and Resource Management, Flor- ida State University, Tallahassee, Florida 32306-2043, Email: [email protected]; (X.N.) Depart- ment of Statistics, Florida State University, Tallahassee, Florida 32306-3033; (F.G.L.) Northwest Flor- ida Water Management District, Route 1, Box 3100, Havana, Florida 32333-9700.