EFFECTS OF SALINITY AND OTHER STRESSORS ON EASTERN OYSTER
(CRASSOSTREA VIRGINICA) HEALTH AND A DETERMINATION OF
RESTORATION POTENTIAL IN NAPLES BAY, FLORIDA.
A Thesis
Presented to
The Faculty of the College of Arts and Sciences
Florida Gulf Coast University
In Partial Fulfillment
Of the Requirement for the Degree of
Master of Science
By
Katie Sue Laakkonen
2014
2
APPROVAL SHEET
This thesis is submitted in partial fulfillment of
the requirements for the degree of
Masters of Science
______Katie S. Laakkonen
Approved: May 2014
______Aswani K. Volety, Ph.D. Committee Chair/Advisor
______Michael Savarese, Ph.D.
______Michael Bauer, Ph.D.
The final copy of this thesis has been examined by the signatories, and we find that both the content and the form meet acceptable presentation standards of scholarly work in the above mentioned discipline. 3
ACKNOWLEDGMENTS
This research would not have been possible without the support of many people. First, I would like to thank my committee members, Dr. Aswani Volety, Dr. Michael Bauer, and
Dr. Michael Savarese for their guidance, advice, and expertise that they provided throughout this process. Dr. Aswani Volety’s expertise and foundation of oyster research in Southwest Florida lead to my thesis work in Naples Bay and made all of this possible.
A special thank you goes to Dr. Michael Bauer for the numerous hours helping me in the field collecting data, cleaning oysters, and enduring many cuts from oyster shells. This research project could not have been completed without all of his efforts and guidance.
Thank you to Dr. Michael Savarese for his thorough review of my thesis work and invaluable advise. I would also like to thank Monique Barnhart and Lacey Smith for assistance in the field collecting data. Thanks to Lesli Haynes and Lacey Smith for their lab assistance at FGCU, training me on processing procedures and Perkinsus marinus microscopic ID, and always being available to answer my questions. A big thank you and appreciation to Dr. Brian Bovard for the willingness and perseverance in helping me analyze my data. And finally, I am grateful for the support of my family and friends, especially my loving husband Keith, for their encouragement and moral support through this challenging journey.
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ABSTRACT
Naples Bay, a highly urbanized estuary, has lost an estimated 80% of its oyster reefs
since the 1950s due to dredging and development activities. Artificial canals, primarily
the Golden Gate Canal, have increased freshwater flows into Naples Bay causing extreme
swings in salinity. This study characterizes the health of the eastern oyster, Crassostrea
virginica, at four sites along a salinity gradient by investigating and correlating various oyster responses to salinity, dissolved oxygen, and temperature. Prevalence and intensity of Perkinsus marinus infection varied significantly among sites, with the northernmost upstream Site 1 showing the lowest infection. Condition index varied significantly among sampling months and sites, and decreased during the spawning period, April through October. Sites 1 and 2, with more optimal salinities for the first 8 months of the study, had the highest mean condition index. Significant differences were found among sampling months for spat recruitment and sites and peaked in August. Spat recruitment was greatest at the southernmost Site 4 which is located furthest from the freshwater influence and therefore has less extremes in salinity. Living densities (# live oysters m 2) also varied significantly among sampling months and sites, with living densities increasing when moving downstream. Higher living densities were found in the wet season than the dry season reflecting recruitment occurring onto the reefs. The wet season is when extreme swings in salinities result upstream which corresponds with oyster reproduction. Site 1 experienced a 31 ppt drop in salinity within a few days in July when significant rainfall began. This is a tremendous stressor on oysters and could result in mortality of juvenile oysters and the flushing of spat downstream due to high freshwater flows. This study highlights that freshwater flows and resulting salinities are a 5
driving force for oyster reef health and distribution in Naples Bay. It also provides a baseline assessment of the oyster population that will allow for future comparisons when
water quality improves due to diversions of freshwater from the Golden Gate Canal.
These diversions are planned for the near future by the South Florida Water Management
District. This study also assists resource managers in determining potential oyster
restoration sites in the bay. Management recommendations include focusing oyster
restoration sites at the downstream locations due to less salinity extremes, high oyster
living densities, and higher spat recruitment.
6
TABLE OF CONTENTS
ACKNOWLEDGMENTS………………………………………………………..….3
ABSTRACT……………………………………………………………...... 4 5
TABLE OF CONTENTS…………………………………………………………….6
LIST OF FIGURES…………………………………………………………………..7 9
INTRODUCTION…………………………………………………………………....10 23
RESEARCH OBJECTIVES…………………………………………………………24
METHODS…………………………………………………………………………...25 31
RESULTS…………………………………………………………………………….32 37
DISCUSSION……………………………………………………………………….. 38 52
REFERENCES……………………………………………………………………….53 62
FIGURES…………………………………………………………………………….63 78
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LIST OF FIGURES
Figure 1. This map shows the study area and the four sampling locations in the Naples Bay/Gordon River Estuary and the long term City and County water quality locations.
Figure 2. This map shows a comparison of historical Naples Bay (1953) and current day Naples Bay (2010). The channelized neighborhood seen today on the left side of the photo is Port Royal and used to be mangrove wetlands as observed in the 1953 photo. Note the oyster bars throughout the bay in the 1953 aerial.
Figure 3. This map shows the Golden Gate Canal Weirs #1 and #2, and the 4 USGS datasonde locations.
Figure 4. This map shows both the historical (10 sq mile) watershed and the expanded watershed (120 sq mile) that resulted from the dredging of the Golden Gate Canal (South Florida Water Management District).
Figure 5. This map shows a habitat comparison between 1953 and 2003 and the approximate historic versus present day oyster and seagrass coverage (Schmid et al. 2005).
Figure 6: Monthly salinities (ppt) at each site showed a delayed start to the rainy season, which typically begins in June. Site 1 had the most extreme salinity swing and dropped 31 ppt within a few days.
Figure 7: Mean salinities (ppt) from long term water quality sites adjacent to oyster research sites were recorded from 2005 2011. Salinities varied significantly among sites (p < 0.0001). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
Figure 8: Mean salinities (ppt) from long term water quality sites varied significantly among sites and between seasons (p < 0.5). Dry season salinities were significantly higher than the wet season. Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
Figure 9: Monthly temperatures (oC) at each site showed a typical increasing trend into the summer months. Temperature values were similar among sites (within 2 oC) for a given month.
8
Figure 10: Mean temperatures (oC) from long term water quality sites were approximately 25 oC for all sites. Error bars represent one standard deviation.
Figure 11. Monthly dissolved oxygen values at each site were similar for a given month and stayed within 2 mg/l of each other (with the exception of July). Due to equipment failure, data were not recorded for September or October 2011.
Figure 12. Mean dissolved oxygen values from long term water quality sites were all within the range of 5 6 mg/l. Error bars represent one standard deviation.
Figure 13. Monthly mean condition index of oysters from all sampling sites varied significantly among sampling months (p < 0.0001) and sites (p < 0.0001). Error bars represent one standard deviation.
Figure 14. Mean condition index of oysters for each site varied significantly among sites (p < 0.0001). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
Figure 15. Monthly mean infection intensity of P. marinus from all sampling sites varied significantly among sampling months (p < 0.0001) and sampling sites (p < 0.001). Error bars represent one standard deviation.
Figure 16. Mean infection intensity of P. marinus for each site varied significantly among sampling sites (p < 0.001). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
Figure 17. Monthly mean prevalence (%) of infected oysters did not vary significantly among months, but did vary significantly among sampling sites (p = 0.005). Error bars are too small to show on graph.
Figure 18. Mean prevalence (%) of infected oysters varied significantly among sampling sites (p = 0.005). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
9
Figure 19. Mean recruitment per shell per month varied significantly among sampling sites (p < 0.003). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
Figure 20. Monthly mean recruitment per shell per month varied significantly among sampling months (p < 0.0001), peaking in August. Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
Figure 21. Mean living densities using triplicate shell trays were too variable to run statistics. Error bars represent one standard deviation. . Figure 22. Mean living densities by wet and dry season varied significantly among seasons and sites (p < 0.05). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
Figure 23. Mean living densities varied significantly among sites (p < 0.05). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
Figure 24. Mean oyster length (mm) by wet and dry season varied significantly between sampling seasons (p < 0.0001) and among sites (p = 0.0067). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
Figure 25. Mean oyster length (mm) varied significantly among sampling sites (p = 0.0067). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
Figure 26: Mean oyster lengths (mm) in triplicate shell trays were too variable to run statistics. Error bars represent one standard deviation.
10
INTRODUCTION
Watersheds around the United States have been greatly altered to accommodate growing populations and people’s need for increased water resources and areas for development. Florida is among the most populous states with 19.5 million people as of
2013 and is one of the fastest growing with the addition of 1.2 million people just in the past 6 years (U.S. Census Bureau 2013). Southwest Florida experienced tremendous growth and development over the last 50 years and has one of the highest rates of population growth in the United States (U.S. Census Bureau 2013). This has resulted in numerous urbanized watersheds and altered hydrology. Timing and magnitude of freshwater flows to estuaries have been altered due to diversion, withdrawal, channelization, and damming of rivers (Whitfield and Wooldridge 1994, Hopkinson and
Vallino 1995, Jassby et al. 1995). The extensive canal systems in Southwest Florida were dredged to drain wetlands and provide fill for development. This channelization of the landscape precludes freshwater from slowly flowing across the uplands as sheet flow and instead results in rapid delivery of freshwater to estuaries that can greatly stress the biota. For example, altered freshwater flows have had detrimental effects on habitats in the Caloosahatchee River, FL (Chamberlain and Doering 1998, Barnes et al. 2007),
Galveston Bay, TX (Powell et al. 2003), Breton Sound, LA (La Peyre et al. 2009),
Rookery Bay, FL (Rubec et al. 2006), Naples Bay, FL (Simpson et al. 1979), and the St.
Lucie Estuary, FL (Wilson et al. 2005). Balancing the needs of both human and estuarine environments will continue to be a challenge for resource managers when managing and manipulating freshwater flows (Sklar and Browder 1998).
11
Naples Bay estuary is located within the City of Naples, Collier County, FL with the Gordon River bordering it to the north and Rookery Bay National Estuarine Research
Reserve just to the south. It is a long, linear estuary running approximately 3 miles north to south and ranges between 100 1500 ft in width, with Gordon Pass being the one major inlet to the Gulf of Mexico. Historically, Naples Bay received the majority of its freshwater from rainfall that would slowly sheet flow over the landscape and from small natural tributaries—Gordon River, Rock Creek, and Haldeman Creek (Fig. 1). The watershed’s historic drainage area was approximately 10 square miles and was comprised of mostly mesic and hydric flatwoods in addition to cypress swamps (SFWMD SWIM
Plan 2007). Mangroves dominated the shoreline of this shallow estuary and the bay once thrived with oyster reefs, seagrass beds, and numerous fish species (Simpson et al. 1979).
Extensive development, watershed alterations, and dredging activities over the past 70 years transformed Naples Bay into a highly urbanized estuary where detrimental impacts have occurred to the bay and its habitats (Fig. 2). The natural tributaries have been altered by urban infrastructure, and numerous canals were dug which significantly changed historic flowways to the estuary, disrupting the timing, quantity, and magnitude of freshwater flows. The watershed now is comprised of residential developments, industrial areas, and agricultural lands, which have increased the pollutant loads to the bay (SFWMD SWIM Plan 2007). The construction of canal systems in residential areas has increased the perimeter of the bay by 53% and the water surface area by 23%
(Schmid et al. 2005). Surface water that once sheet flowed and was naturally filtered through wetlands is now rapidly conveyed into Naples Bay via stormwater pipes and 12
canals, resulting in degraded water quality (increased nutrients, sediments, metals). The creation of the Golden Gate Canal (Fig. 3) in the 1960s, expanded the City of Naples watershed from approximately 10 square miles to over 120 square miles, a more than ten fold increase (SFWMD SWIM PLAN 2007, Fig. 4). It drains the Northern Golden Gate
Estates, a large residential development, as well as agricultural and ranchlands in eastern
Collier County, and directly connects to the Gordon River and Naples Bay.
The Golden Gate Canal is the main contributor of freshwater to Naples Bay.
With an average of 250 cubic feet per second (cfs) flowing into the estuary from this weir controlled canal and a seasonal range of 0 to almost 1,400 cfs, large influxes of freshwater in the wet season alter the natural salinity regime of the bay. This results in harmful impacts to the aquatic biota, including declines in seagrasses and oysters (Tebeau
1957, Baum 1973, Simpson et al. 1979). In addition, the freshwater flows from the
Golden Gate Canal cause severe stratification of the water column in the wet season
(June Oct), which can deplete dissolved oxygen levels in the benthos, inhibit vertical mixing, and decrease water clarity. Browder and Moore (1981) documented that these flows are great enough to flush planktonic organisms out of Naples Bay. This results in negative ramifications to fish and oyster populations that depend upon estuaries as nursery grounds and settling areas. Areas in the bay that may have historically been optimal habitats for oyster reefs may not be any longer due to shifts in the salinity gradient and direct impacts to hard substrates. In the dry season (Nov May), relatively uniform salinities exist from Gordon Pass up through the Gordon River. When the wet season (June Oct) starts, and freshwater coming over the weirs of the Golden Gate Canal 13
begins to flow through the Gordon River and into Naples Bay, the bay experiences
extreme swings in salinity which serve as a stressor for oysters .
Canals, seawalls, and bulkheads replaced extensive areas of mangroves that once lined Naples Bay. Over 70% of the mangrove shoreline has been converted to residential development (Schmid et al. 2005, Fig. 2). It is estimated that the Bay has lost 80% of its oyster reefs and 90% of its seagrass beds (Schmid et al. 2005, Fig.5). Major alterations to the bay began in 1930, when a 40 ft. wide channel was dredged the entire length of the bay, cutting through numerous oyster bars (Antonini et al. 2002). Major development and dredging continued throughout the 1950s and 1960s. The cumulative impacts of extreme salinity swings, increased pollutant loads, and physical impacts from dredging activities all contributed to the decline in oyster abundance in Naples Bay. In addition to the estimated 80% loss of oyster reefs in Naples Bay, oyster loss has been observed within other Southwest Florida estuaries (Volety et al. 2009, 2010), in St. Lucie, Florida
(Wilson et al. 2005), in Mobile Bay, Alabama (Gregalis et al. 2008), and in Chesapeake
Bay (Judy 1999).
Efforts are underway by the Big Cypress Basin of the South Florida Water
Management District (SFWMD), to divert some of the freshwater from the Golden Gate
Canal to restoration areas in need of rehydration. This will result in decreased flows into
Naples Bay (SFWMD SWIM PLAN 2007). In addition, City of Naples projects, such as
the creation of filter marshes (wetlands) and the replacement of concrete swales with
grassy swales, have been implemented to slow and treat stormwater runoff before 14
entering the natural waterways in order to mimic a more natural system. Historically, rainfall slowly sheet flowed across the landscape through wetlands and swamps before entering bays and rivers. Routing water through manmade wetlands or vegetated areas allows nutrient laden runoff to be treated through plant uptake of nutrients and the settling out of sediments. This results in cleaner stormwater entering our natural waterbodies.
Naples Bay is classified as a Class II, “shellfish propagation or harvesting”
waterbody by the Florida Department of Environmental Protection (DEP). The
urbanization of Naples Bay and subsequent degradation in water quality and oyster
habitat prohibits oyster harvesting despite this classification. Surrounding tributaries and
canals are classified as Class III, “recreation and propagation and maintenance of a
healthy well balanced population of fish and wildlife.” Each Class has its own set of
state standards for water quality (Florida Administrative Code 62 302), with Class II being more restrictive for a few parameters such as fecal coliform. Naples Bay, as
evaluated by the DEP through Section 303(d) of the Clean Water Act, is impaired (polluted)
for fecal coliform, iron, low dissolved oxygen, and copper (Florida Administrative Code 62
303). Recently, numeric nutrient criteria were established by DEP for the bay, adding nutrient exceedences to the pollution issue.
Oyster reefs are important biological and structural components of estuaries
(Rheinhardt and Mann 1990, Coen et al. 1999, Gutierrez et al. 2003). Oysters stabilize shorelines against erosion and are considered a keystone species due to their creation of 15
complex reef habitats that house and provide food for hundreds of invertebrate species
(Wells 1961). Oyster reefs are utilized by fish, crustaceans, other bivalves, birds, and mammals (Coen et al. 1999, Sanders et al. 2004, Tolley et al. 2005, Abeels et al. 2012).
The species being examined in this study is the eastern oyster, Crassostrea virginica , and
is highly valued for both its ecological and economic roles in the northern Gulf of
Mexico (Dame 1996, Plunket and La Peyre 2005, Coen and Grizzle 2007). It is also an
important commercial fishery from the Gulf of Mexico up through the Gulf of St.
Lawrence, Canada (Stanley and Sellers 1986). Eastern oysters form intertidal and
subtidal reefs all along the U.S. Atlantic east coast (Bahr and Lanier 1981, Burrell 1986).
Oysters in the Gulf of Mexico are a separate population from Atlantic oysters (Eastern
Oyster Biological Review Team 2007). Oysters are excellent filter feeders and cleansers of estuarine waters and provide many ecological goods and services by improving water quality. They do this by facilitating mineralization of nutrients and by removing sediment, organic detritus, microbial pathogens, and contaminants from the water column
(Bahr and Lanier 1981, Dame et al. 1985, Newell 1988). The filtering capability can vary from 4 – 40 L of water per hour per oyster (Galtsoff 1964). The decrease in suspended sediment can increase light penetration through the water column, which in turn promotes the growth of submerged aquatic vegetation (Dame 1979, Dame et al.
1980, 1985, 1989, Newell and Koch 2004, Booth and Heck 2009).
Oysters are often considered sentinel organisms. They are used as ecological indicators of bay health and as a means of measuring restoration goals as outlined in the
Comprehensive Everglades Restoration Plan (Systems Status Report 2009). In addition, 16
oysters can be good long term indicators of estuarine health due to their ability to concentrate contaminants over time, which can reveal water quality problems when analyzing their tissue (Cantillo 1998). In the Caloosahatchee River, oysters are used as ecological indicators to measure the success of Everglades Restoration (Volety et al.
2009). The National Oceanic and Atmospheric Administration (NOAA) uses both oysters and mussels to monitor concentrations of trace metals in waterbodies throughout the nation. In a 2005 study published by NOAA, copper levels in oyster tissue at one site in Naples Bay (near Site 3 in this study, Fig. 1) were reported to be some of the highest in the nation (Kimbrough et al. 2008). A statistically significant increasing trend was found for copper from 1986 to 1999 in Naples Bay and can likely be attributable to anthropogenic inputs (O’Connor and Lauenstein 2005).
Several factors control the distribution and health of oysters, with the primary three being salinity, temperature, and substrate availability (Jones 1950, Shumway 1996).
Freshwater inputs are essential to create optimal salinities for oyster reefs, and oyster abundance and health can correlate well with varying salinity conditions as demonstrated in the Suwannee River Estuary in northeast Florida (Bergquist et al. 2006). Unlike
Naples Bay, the Suwannee River lacks the freshwater it needs and therefore has a
minimum flow and level (MFL) set by the DEP to ensure enough freshwater flows
downstream in order to sustain estuarine habitats. Bergquist et al. (2006) found a greater percent cover of living oysters and densities of C. virginica where lower salinities (less
than 20 ppt) were found near the mouth of the river. In Apalachicola Bay, FL, higher
salinities resulted in greater oyster mortality while highly variable salinity favored greater 17
oyster production (Livingston et al. 2000). So the timing and magnitude of freshwater flows into estuaries will dictate where oyster habitat exists, with extreme variability in flows being detrimental to oyster reef habitat. Altered freshwater flows have profound effects on salinity, and can greatly influence community structure, biological productivity, biodiversity, pollutant inputs, and other key ecosystem processes (Montague and Ley 1993, Sklar and Browder 1998, Kimmerer 2002, Montagna et al. 2002). Tolley et al. (2005) found diversity, biomass, and organism density to vary relative to salinity in the Caloosahatchee River, FL. Large influxes of freshwater are considered to be the most common stressor in estuarine systems (Jassby et al. 1995, Sklar and Browder 1998,
Volety 2008, Volety et al. 2009, 2010). Because oysters are sensitive to changes in salinity, freshwater inflows can determine the distribution of oysters within an estuary
(Powell et al. 2003, Tolley et al. 2005). Salinity also significantly influences oyster larval growth and survival (Davis 1958, 1964, Hidu and Haskin 1978) and physiological processes (Butler 1949, Loosanoff 1953, Shumway and Koehn 1982, Shumway 1996).
Changes in salinity (and temperature) can affect the prevalence of Perkinsus marinus, a protozoan parasite commonly known as dermo disease (Mackin 1956, Soniat
1985, Andrews and Ray 1988, La Peyre et al. 2009), which contributes to the mortality of eastern oysters (Chu et al. 1993). Perkinsus marinus is the primary pathogen of oysters and has devastated oyster populations in the Atlantic (Chu et al. 1993, Burreson and
Ragone Calvo 1996) and the Gulf of Mexico (Soniat 1996). Increases in salinity and temperature result in higher infection prevalence and intensity with resulting increased mortality rates (Andrews and Ray 1988, Ford and Haskin 1988, Powell et al. 2003). 18
High infection intensities by this protozoan may substantially reduce oyster growth rates or kill oysters, thus having real impacts to shellfish harvesting and the ecology of coastal estuaries (Ford 1996). Albright et al. (2007) found high intensities of P. marinus in
deployed oyster spat during a drought where salinities were 4 6ppt higher than normal.
During a second deployment of oyster spat, the first drought year was followed by a
freshet year (short term decrease in salinity), and P. marinus infections were significantly
lower, thus resulting in much lower mortalities.
In addition to salinity, temperature, disease, and the need for hard, stable
substrate for oyster spat settlement, predation (MacKenzie 1970) and food availability
(Mackin 1959, Wilbur 1992), also play a large role in oyster distribution. Similar to
increased disease prevalence, higher salinities can result in higher predation rates,
attracting crabs, starfish, oyster drills and boring sponges (Butler 1954, Hopkins 1962,
Galtsoff 1964, Menzel et al. 1966, Andrews and Ray 1988, Soniat and Brody 1988,
Soniat and Gauthier 1989, Shumway 1996, Livingston et al. 2000). Temperature has an
effect on the rate of ontogenic developments (Shumway 1996) as well as limiting
infection intensity (Mackin 1951, Ray 1954, Mackin 1956, Andrews and Hewatt 1957,
Quick and Mackin 1971, Andrews and Ray 1988, Chu and La Peyre 1993). Of all of
these factors, salinity is considered to be the dominant one directly affecting the health
and productivity of oyster populations.
Live oyster density is influenced by larval production, spat recruitment, survival,
water quality, predation, and food availability. These factors are influenced either 19
directly or indirectly by salinity and flows. The physical flushing of larvae to downstream locations is possible in times of high flows. Volety et al. (2010) found higher living densities further downstream when freshwater flows were high coming into the Caloosahatchee Estuary, which could be a function of larvae being pushed downstream as well as creating unfavorable salinities for survival and growth of oysters at upstream locations. Conversely, that study found higher living densities upstream during low flow times, likely a result of more favorable salinities upstream and more larvae being retained.
The condition index of an oyster is a ratio of dry tissue weight to shell weight and serves as a proxy for the physiological condition of an oyster (Lucas and Beninger 1985).
Natural processes such as reproduction, filter feeding, and other maintenance requirements use metabolic energy. Any remaining energy not used in these natural processes allows for increased biomass of the oyster (Volety et al. 2009). Growth, however, can be reduced if less energy is available for reproduction, feeding, etc. due to environmental stressors including disease and sub optimal water quality. The excessive freshwater inputs seen in Naples Bay and the Gordon River can cause rapid changes to water quality, which stresses oysters. This in turn can make them more susceptible to disease. Therefore, a comparison of condition index among reefs should signify oyster health and the effects of driving forces such as salinity and disease.
Although oysters can tolerate a wide range of habitats, their preferred habitat and ranges of water quality parameters are well established through numerous studies 20
(Shumway and Koehn 1982, Hargis and Haven 1999, Shumway 1996). Oysters can tolerate salinity fluctuations ranging from 5 40 ppt, with their optimal range being from
14 to 28 ppt (Galtsoff 1964, Quast et al. 1988, Shumway 1996). Shumway (1996) found a minimum salinity of 10 ppt is necessary for oyster growth. The optimal pH range for oyster larvae is 6.75 8.75 (Calabrese and Davis 1966), and a minimum dissolved oxygen requirement of 20% saturation is required (Eastern Oyster Biological Review Team
2007). Optimal temperatures for growth range from 20 to 30 oC (Stanley and Sellers
1986). Oysters have been found to survive extreme temperatures, with Galtsoff (1964) and Shumway (1996) documenting survival in freezing temperatures as well as in excess of 45 oC in intertidal areas. However, lengthy exposure to extreme temperatures will stress and ultimately cause mortality in oysters. Shumway and Koehn (1982) found the oxygen consumption rate in oysters was significantly lower at 10 oC versus 20 oC and at
20 oC versus 30 oC. Loosanoff (1958) found the pumping rates for feeding were negatively affected at temperatures above approximately 35 oC. The Eastern Oyster
Biological Review Team (2007) found oyster mortality occurs in the summer when water
temperatures exceed 30 oC in the Gulf of Mexico.
Very few oyster studies have been conducted in Naples Bay, and more quantitative and comprehensive monitoring efforts are necessary to determine oyster health, recruitment, mortality, growth rate, and living densities (Savarese et al. 2007).
This study strives to provide these needed data and provide resource managers with guidance on site selection for habitat restoration. The Naples Bay Study (Simpson et al.
1979) was the first comprehensive documentation of the various issues facing Naples 21
Bay, including bay stratification in the wet season resulting from excessive influxes of freshwater and various habitat impacts. This 1979 study serves as the basis for determining changes to the area since the early 1900s. A study carried out by Schmid et al. (2005) involved benthic habitat mapping in Naples Bay and the Gordon River, and the results compared current oyster reef distribution with historical distribution through photointerpretation of 1953 aerial images. It is estimated that the Bay has lost approximately 80% of its oyster reefs since the 1950s (Schmid et al. 2005, Fig. 5).
Several small scale restoration efforts using mesh bags filled with fossil shell to create substrate, and a resident volunteer oyster gardening program, have been initiated in Naples Bay with some success. Florida Gulf Coast University (FGCU) deployed 200 shell bags at two sites in Naples Bay—one in the northern part, closer to the freshwater influence and one in the southern, more saline part of the bay. They found spat recruitment and growth on the shell bags were greater at the southern, more saline site
(Savarese et al. 2007). This project did not link oyster recruitment or survival with water quality factors, which is a gap this study aims to address. Integration of water quality with oyster response data is essential in order to get a complete picture for restoration to be successful. Substrate mapping was also conducted in Naples Bay by FGCU in 2006.
The results showed that the substrate in the southern half of the bay was much more conducive to oyster growth than the northern half of the bay (Savarese et al. 2006,
Dellapenna et al. 2013). However, the health of existing reefs utilizing these substrates was still unknown and furthering that research was a recommendation of that study.
22
Providing vertical relief and hard substrate for spat to settle on is a documented method for restoring impacted coastal areas and facilitating the growth of oyster reefs.
Oyster restoration efforts using shell bags as substrate have proven successful in other areas including Estero Bay, Florida (Volety, personal communication), Mobile Bay,
Alabama (Gregalis et al. 2008), and the South Carolina coast (Brumbauch and Coen
2009). Before any large scale restoration efforts are initiated in Naples Bay utilizing these techniques, a scientific basis is needed for how restoration sites are chosen. This study provides that information by assessing oyster health and spat recruitment potential, and relating those to water quality parameters. This will provide a better understanding of where oysters are impacted the most from freshwater releases and other factors, as well as where to focus future restoration efforts based on available substrate and water quality.
Restoration efforts can only be successful if suitable water quality exists to support the habitat. Reducing primary pollutants is key, and freshwater is the number one pollutant in Naples Bay, causing estuarine imbalances that harm its biota. The City, however, does not have control over the amount of freshwater coming out of the Golden
Gate Canal. The SFWMD is responsible for the management of the canal’s weir system and for the volume and timing of water that enters Naples Bay. It is the goal of the City to keep this issue a high priority for the SFWMD. This study will establish a baseline assessment of oyster health in Naples Bay that can be used for comparison once planned freshwater diversions occur and flows are reduced. This study will also help determine potential locations for oyster restoration under the current salinity regime and can perhaps 23
guide restoration efforts in other geographical areas that face similar freshwater influxes.
Success can be achieved in restoring some of the lost oyster habitat in the bay by re establishing optimal salinity ranges and reducing salinity extremes for oysters and all of their commensal species.
24
RESEARCH OBJECTIVES
The primary goal of this study is to investigate and characterize the health and abundance of the eastern oyster, Crassostrea virginica, at four sites in Naples Bay and relate those data to abiotic estuarine conditions. Exploring the complex relationships among various oyster responses, watershed alterations, and resulting changes to water quality can result in an increased understanding of how ecosystems respond to and are impacted by urban development. Ultimately, these results can be used by environmental managers to determine the potential of oyster restoration by identifying locations in the bay that might be appropriate to support such activities. This will aid future management objectives of trying to restore oyster reefs lost to development. To achieve this goal, the following objectives are investigated:
1. Investigate and correlate water quality parameters (temperature, dissolved oxygen, and salinity) to measured oyster health responses in order to identify potential oyster restoration sites in Naples Bay.
2. Characterize and compare oyster health and ecological responses in Naples
Bay using the condition index of adult oysters, disease prevalence and intensity of the parasite Perkinsus marinus, living densities (percent live/m 2), and spat recruitment both
seasonally and spatially at four locations along a salinity gradient in Naples Bay and the
tidally influenced Gordon River (Fig. 1).
25
METHODS
Study Site
The Naples Bay/Gordon River estuary has three tributaries: Rock Creek, Gordon
River Extension, and Haldeman Creek (Fig.1). Flows from these tributaries are minimal
compared to the Golden Gate Canal that delivers 250 cubic feet per second (cfs) on
average of freshwater daily to the river and bay. During peak summer flows, the Gordon
River turns fresh and the bay experiences extreme salinity swings and stratification. Four
sampling sites were established along the salinity gradient, with the upstream Gordon
River Site 1 being closest to the freshwater source (Fig. 1). Site 2 is located on the west
side of the bay adjacent to the City Dock; Site 3 is located in the mouth of Haldeman
Creek; and Site 4 is located on the east side of the bay along the mangrove fringe south of
Haldeman Creek (Fig. 1). Oyster collection occurred once per month at each site for one
year spanning one dry and one wet season from November 2010 October 2011.
Condition index
Fifteen adult oysters were harvested from each site monthly (n=60) to determine
the condition index, which is the ratio of dry oyster tissue weight to shell weight (Lucas
and Beninger 1985). Condition index is a proxy for the physiological condition of the
oyster and allows for a comparison of oyster health among sites affected by a variety of
stressors. Harvested oysters were placed on ice and refrigerated overnight and then
transported the next day to Florida Gulf Coast University’s marine science laboratory.
Shell length (mm) was recorded for each oyster, and all barnacles, worm tubes, and other
encrusting organisms were scraped off of each shell in order to obtain an accurate shell 26
weight. All oysters were shucked and rectal tissue samples were taken for Perkinsus marinus tests (see below). Tissue was then scraped into pre weighed aluminum tins and
weighed. The tissue and shell were then both placed in a drying oven at 60 oC for 24 – 72 hours. Dry tissue and shell weight were then recorded. Condition index was calculated using the following: dry tissue weight/shell weight x 100 (Volety 2008).
Disease prevalence
Rectal tissue samples were taken from fifteen adult oysters harvested from each site monthly (n=60), and were cultured in glass tubes and assayed using Ray’s fluid thioglycollate medium technique (Ray 1954). Tubes were filled with 10ml of media and
100 µg penicillin/streptomycin to suppress bacterial growth and 2 ml nystain to suppress fungal growth. After 5 6 days, tissue was placed on a slide with 1 2 drops of Lugol’s iodine stain, which allows for visual identification of P. marinus that appear as blue to black spheres under a microscope. Infection intensity of P. marinus was recorded using a modified Mackin scale (Mackin 1962), where 0 = no infection, 1 = very light, 2 = light,
3 = light/moderate, 4 = moderate/heavy, and 5 = heavy. In some instances, tubes had non recoverable tissue samples, so results could not be obtained in those cases.
Oyster recruitment
To determine oyster recruitment potential, 3 replicate shell stringers were deployed at each of the 4 sites at the start of spawning season (April) and were replaced with new stringers every month through October 2011. Each shell stringer was comprised of 12 adult oyster shells with holes drilled in the middle and strung together 27
using galvanized wire (Haven and Fritz 1985). The stringers were suspended a few inches from the bottom using PVC “T’s” that were driven into the substrate. After the stringers had been deployed for a month, they were collected, the outer 2 oyster shells were discarded, and the remaining 10 shells were examined on both sides for recruits.
The number of spat was recorded as number of spat per oyster shell per month.
Triplicate 0.6m x 0.6m plastic trays filled with fossil shell were also deployed at each site at the start of the project in November 2010 to quantify total net recruitment throughout the year. Net recruitment is the number of additions expected in the oyster population during this timeframe, or how many spat remained alive after settling onto the
trays, after experiencing mortality throughout the year. Trays were to remain at each site
for the duration of the year; however, in July 2011, trays were observed missing at Site 1,
and trays were present but devoid of shell at Site 2. The trays and shell were immediately
replaced at these 2 sites; therefore recruitment recorded at these 2 sites reflects 4 ½
months of tray deployment versus 13 months for Sites 3 and 4. It should also be noted
that at Site 4, upon collection of the recruitment trays in December 2011, 2 of the 3 trays
were only half full. All shells in each tray were observed for living oysters, and the total
number of living oysters per tray per site was calculated. One hundred randomly selected
living oysters from each tray were measured and lengths were recorded in mm. They
were averaged together to get a mean length per tray per site.
28
Living densities
Living density is an indirect measure of reef productivity. The number of live oysters per m2 was determined by randomly placing a ¼m 2 quadrat near mean low water four times at each site. The total number of live oysters was recorded for each quadrat, as well as oyster lengths for 50 oysters. The number of living oysters per quadrat was multiplied by 4 and then averaged together to get the total number of living oysters per square meter. This effort was conducted once in the dry season and once in the wet season.
Water quality
Using a handheld YSI 600 multiprobe sonde, dissolved oxygen, temperature, and salinity were recorded monthly at each site from a depth of 0.3m when oyster collection occurred. Dissolved oxygen was recorded in mg/l, and those results were used in conjunction with temperature values to determine % saturation of dissolved oxygen for the purpose of comparison to the 20% threshold value. In addition, water quality data are collected on a monthly basis by the City of Naples’ Natural Resources Division at 16 sites throughout Naples Bay (eight sites are sampled one month and the other eight the next month). Data collection began in January 2005 by the Department of Environmental
Protection (DEP) and was taken over by the City in January, 2006. In January 2011, some monthly water quality sampling locations were moved and the total number of sites was reduced to 8. These 8 sites had both bottom and surface measurements recorded to document salinity, temperature, and dissolved oxygen stratification that occurs when high summer flows are coming from the Golden Gate Canal. Collier County staff also has a 29
water quality sampling program and collect estuarine surface samples on a monthly basis for these same parameters at a few sites in Naples Bay and the Gordon River (Fig. 1).
In order to have a more robust, long term water quality dataset for this oyster project, data from the City’s and County’s monthly sampling sites that are similar in their geographic location to the oyster collection sites were also used (Fig. 1). Parameters from these long term datasets were averaged together by site to determine the water quality for that oyster site. To ensure grouped sites were truly similar in water quality at a given time, simultaneous readings with the YSI sonde were taken at all grouped sites and compared. This was repeated twice in the field during monthly water quality sampling to verify that water quality conditions were indeed similar for grouped sites for temperature, dissolved oxygen, and salinity. Nutrient data collected by Collier County’s water quality sampling program are also integrated in this study.
Additional data for Naples Bay, provided by the South Florida Water
Management District (SFWMD), consist of flow rates over the Golden Gate Canal weirs, continuous salinity and temperature data recorded by four datasondes (managed in cooperation by the U.S. Geological Survey), and rainfall data. The datasondes maintained by the U.S. Geological Survey record continuous salinity data at three locations in Naples Bay (USGS 02291315, USGS 02291325, and USGS 02291330) and one in the Gordon River (USGS 02291310). The northernmost datasonde is located approximately half a mile upstream from Site 1, the second datasonde is located adjacent to Site 2, and the southernmost datasonde is located just inside of Gordon Pass (Fig. 3). 30
Statistical analysis
The relationship among sites and oyster responses (condition index, P. marinus intensity, spat recruitment, oyster length, and living densities) was analyzed using both parametric and non parametric two way ANOVA’s using SAS’s JMP software (Sall et al.
2007). Living density data met normality and equal variance assumptions, therefore parametric analysis was conducted. When significant differences (p < 0.05) between means were detected, a multiple comparison of means using Tukey HSD post hoc test was used to determine which sites showed differences, and a Student’s t post hoc test was used for determining differences among seasons. Oyster length data collected while conducting living densities violated the normality assumption. Data were transformed by taking the square root of all data, which made the data normally distributed with equal variances. When significant differences (p < 0.05) between means were detected, a multiple comparison of means using Tukey HSD post hoc test was used to determine which sites showed differences, and a Student’s t post hoc test was used for determining differences among seasons.
Stringer recruitment, P. marinus infection intensity and prevalence, and condition index data failed the assumptions of parametric tests and were analyzed using a non parametric Kruskal Wallis two way ranking analysis in JMP. When significant differences (p < 0.05) were detected between ranks, a Steel Dwass All Pairs post hoc test was conducted to determine differences among sites and seasons. P. marinus prevalence data were transformed using arcsine in order to eliminate percentages.
31
Results from the shell trays (number of live oysters and lengths) that were
deployed for one year produced small, highly variable data sets. Due to several
challenges requiring replacement trays and shell to be deployed at various times and sites
throughout the study timeframe, statistical analyses were not conducted on these data.
However, the results are still included for reference.
Water quality data did not meet the normality or equal variance assumptions.
Salinity data for 2005 2011 were averaged by month to reduce variance.
Transformations were attempted and none were effective in meeting the normality assumption. Therefore, the non parametric Kruskal Wallis two way ANOVA was used for analysis. When significant differences (p < 0.05) between ranks were detected, a
Steel Dwass All Pairs post hoc test was conducted to determine differences among sites and seasons. This test did not account for interactive effects among sites and seasons.
Temperature and dissolved oxygen did not vary much among sites and were not analyzed statistically.
32
RESULTS
Water quality--temperature, salinity, and dissolved oxygen
Considering only the water quality data that were collected at the time of oyster collection, salinity remained relatively constant at all 4 sites during the dry season
(November 2010 – June 2011, Fig. 6). With a late start to the wet season (July rather than June), salinities dropped noticeably starting in July 2011 at all sites. Site 1 had the most varied salinity exhibiting 36.0 ppt in June 2011, dropping to 5.0 ppt in July 2011—a decrease of 31.0 ppt. Site 2 and 4 both had a decrease of 17.0 ppt, and Site 3, located in
Haldeman Creek, had a decrease of 14.0 ppt. Prior to July 2011, most site salinities were within 4.0 ppt of each other. From July 2011 to October 2011, site salinities differed by as much as 19.0 ppt. For salinity data collected from 2005 through 2011, Site 1 had the most varied salinity, ranging from 0.01 ppt to 36.0 ppt. Site 1 had significantly lower mean salinities (19.7 ± 12.7 ppt) from Sites 2, 3, and 4 (26.0 ± 10.2, 28.5 ± 8.5, and 27.6
± 9.1 respectively; p < 0.0001, Fig. 7). As expected, significant differences were also found between seasons with the dry season having higher salinities than the wet season
(Fig. 8).
Temperature did not vary widely among the sites with values remaining within
2oC of each other (Fig. 9). One exception to this was in January 2011, showing a
difference of 2.6 oC between Site 1 and 4. Temperatures steadily increased as expected from December 2010, with a low temperature of 14 oC, through July 2011, peaking at
33 oC. All four sites averaged approximately 25 oC from 2005 through 2011 (Fig. 10).
33
Dissolved oxygen for all 4 sites stayed within 2 mg/l of each other for any given month, with the exception of July 2011 where a difference of 5 mg/l was observed (Fig.
11). Site 2 had a high reading of 10 mg/l that month with Site 1 exhibiting 5 mg/l.
Dissolved oxygen readings averaged from 2005 2011 were all within the range of 5 6 mg/l (Fig. 12).
Rainfall
Rainfall data from the South Florida Water Management District for the
Southwest coast of Florida for the study period show below average rainfall for 2010 with an approximate 13 inch deficit below the annual average of 56 inches. April 2011 through June 2011 had below average rainfall, resulting in relatively stable salinities between November 2010 – June 2011, with wet season rains starting in July. Despite the late start to the wet season which usually begins in June, the total rainfall average for
Southwest Florida in 2011 was approximately 53 inches. The high rainfall events in
October 2011 were due to a tropical depression that resulted in totals greatly above average for that month. This made up for the deficit earlier in the year and was also the last month of data collection for this study.
Golden Gate Canal flows
The majority of daily flow data recorded at the Golden Gate Canal weir #1
(SFWMD DBHYDRO online database) from November 2010 March 2011 revealed that there was no freshwater flow during this time period. Due to repairs and maintenance needed on weir #1, no flow data exists from April 2011 through July 2011. However, 34
flow data exists upstream at weir #2, and records from March 2011 through June 2011 show no freshwater flow coming from the Golden Gate Canal; flows started to enter
Naples Bay in early July 2011. Freshwater flows for this study period peaked in late
October 2011 with 717 cubic feet per second (cfs) entering Naples Bay, and dropped to below 200 cfs starting in December 2011. Flows from the Golden Gate Canal can range from 0 1000 cfs in the dry season and can exceed 1400 cfs in the wet season.
Condition index
Condition index varied significantly among sampling months (p < 0.0001, Fig.13) and sites (p < 0.0001, Fig.14). The range across all sites is 1.4 to 4.2 with a mean condition index across all sites ranging from 2.1 ± 0.4 to 2.8 ± 1.0. Mean condition index by month remained above 2.5 in the dry season (Nov May) with a mean of 2.9 ± 0.7, and fell below 2.5 with a mean of 2.0 ± 0.4 for the remainder of the wet season (June Oct).
Sites 1 and 2 had the highest condition index with a similar mean condition index of 2.8 ±
0.9 and were significantly different from Sites 3 and 4 (2.1 ± 0.4 and 2.5 ± 0.3 respectively). Site 3 had the lowest condition index and was significantly different from all other sites.
Perkinsus marinus intensity and prevalence
Infection intensity varied significantly among sampling months (p < 0.0001,
Fig.15) and sampling sites (p < 0.001, Fig.16). Site 1, as expected, had the lowest mean score (0.91 ± 0.3), which was significantly different from Sites 2, 3, and 4. Site 3 had the highest intensity of infection (1.88 ± 0.5) followed by Sites 2 and 4 (1.38 ± 0.5, 1.36 ± 35
0.5 respectively). Intensity was lowest in April (0.89) and highest in September (1.94).
The range of intensity from all sites is 0.47 to 2.93.
Prevalence of infection did not vary significantly among months (Fig. 17), but did vary significantly among sampling sites (p = 0.005, Fig. 18). Prevalence (% of infected oysters) values from all sites ranged from 46% to 100% during the sampling period, with means across all sites ranging from 69 ± 13.1 to 94 ± 8.5. As with infection intensity, prevalence was lowest in April (70%), however, it was highest in January
(98%). Results by site for prevalence were similar to that of intensity, where Site 1 had significantly lower % infections (69 ± 13.1) than the rest of the sites, and Site 3 had higher prevalence of infection (94 ± 8.5) followed by Sites 2 and 4 (88 ± 14.1 and
88 ± 9.5 respectively).
Spat recruitment
Recruitment in the stringer experiments varied significantly among sampling sites
(p < 0.003, Fig. 19) and months (p < 0.0001, Fig. 20), peaking in August. Site 4, the southernmost site and furthest from the freshwater influence, had significantly higher recruitment than the other 3 sites (4.68 ± 3.1 mean spat/shell). Mean recruitments at Sites
1, 2, and 3 were all similar (1.46 ± 1.3, 1.81 ± 2.0, and 1.43 ± 1.2 respectively), which is much less than observed recruitment in the Caloosahatchee River during Oct 1999 July
2010 with a mean range of 0 to 25 oysters/shell (Volety et al. 2010).
36
Net oyster recruitment in the shell trays varied among sites (Fig. 21), but significance was not determined. Recruitment at Site 4, with a mean number of 2169 ±
341.6 live oysters per m 2, was higher than Site 1, 2, and 3, which had 1176 ± 35.0, 1080
± 28.4, 853 ± 7.2 respectively. Site 3 had the second highest living density, yet had the lowest net recruitment.
Living density
The number of live oysters per m2 varied significantly among seasons (p =
0.0004, Fig. 22) and sites (p < 0.0001; Fig. 23), with no interactive effects among sites and seasons (p > 0.05). The wet season (June Oct) had significantly higher living densities (1,574 ± 655.0 oysters m 2) than in the dry season (Nov May, 932 ± 453.8
oysters m 2). Site 4 had significantly higher living oysters m 2 (1,880 ± 567.9) than the
other 3 sites. Sites 1, 2, and 3 had statistically similar living densities with Site 1
showing the lowest living density (742 ± 410.4) followed by Site 2 (895 ± 438.7, Fig.
23). Site 3 had the second highest living density (1,497 ± 768.0 oysters m 2) despite
having low monthly recruitment.
Oyster lengths
Oyster lengths (mm) varied significantly among sampling seasons (p < 0.0001,
Fig. 24) and sites (p = 0.0067, Fig. 25). Interaction among seasons and sites was
significant (p < 0.0001) indicating that season does have an effect on oyster length.
Mean oyster lengths ranged from 45.3 ± 6.2 to 47.3 ± 0.8 mm, and Site 1 was
significantly higher (47.3 ± 0.8 mm) than Sites 2, 3, and 4 (45.6 ± 10.0, 45.3 ± 6.2, 45.5 ± 37
2.5 mm respectively). Dry season mean oyster length was higher (50.2 ± 3.9 mm) than wet season (41.7 ± 4.1 mm), which would be indicative of recruitment and measuring spat as well as adult oysters.
Oyster lengths measured from the shell filled trays were also recorded, although statistical analysis was not performed due to a small, highly variable dataset.
Site 2 had the largest oysters (32 ± 2.8 mm) with Site 1 having the smallest oysters (19 ±
1.8 mm). Sites 3 and 4 were similar at 24 ± 1.1 and 25 ± 1.2 mm respectively (Fig. 26).
These data are contrary to the results discussed above, however, they reflect one year of growth and recruitment and may be more representative of true oyster length even with the data being highly variable.
38
DISCUSSION
Oysters within Naples Bay exhibit a variety of physiologic and ecologic responses to changes in salinity. This demonstrates that the freshwater management of the Golden
Gate Canal has significant ramifications on oyster health. Salinity regimes, including the extremes, are determined by freshwater flows into the estuary and influence all physiological aspects of oysters. This relationship between oyster health, recruitment, and abiotic conditions in the estuary is what controls where oysters thrive and determines where future restoration sites should exist to best ensure success.
Oyster Responses
Significant differences in condition index were observed both among sampling sites (Fig. 14) as well as among sampling months (Fig. 13). Condition index, a ratio of dry tissue weight to shell weight serves as a proxy for the physiological condition of an oyster (Lucas and Beninger 1985). It varies with the reproductive cycle as oysters spawn
(Apr Oct) and release gametes (Volety et al. 2003). Mean condition index by month remained above 2.5 in the dry season (Nov May) and fell below 2.5 for the remainder of the wet season (June Oct). This suggests that decreased tissue mass was due to the release of gametes during this timeframe of oyster spawning, a phenomenon documented in other local studies in Estero Bay and the Caloosahatchee River (Volety 2008, Rasnake
2011). These studies also determined gonadal index values, which are determined by histological analysis examining gonadal state, gender, reproductive potential, and gametogenic state of oysters. These studies show specific gonadal index ranges that are indicative of actively spawning oysters and those indices covary with condition index. 39
These results corroborate the interpretation of lower condition indices as an indication of reproduction activity and confirmed a similar spawning period for Estero Bay, the
Caloosahatchee River, and Naples Bay. The range for oyster condition index in Naples
Bay from all sites is 1.4 to 4.2 with means across all stations ranging from 2.1 ± 0.4 to 2.8
± 1.0. This range is similar to others found in Estero Bay (Rasnake 2011) and Faka
Union (Volety and Savarese 2001). Sites 1 and 2 had the highest condition index and were significantly different from Sites 3 and 4. This finding is contrary to what other studies found in the Caloosahatchee River and Estero Bay that showed an increase in condition index with increasing distance downstream (Volety et al. 2003, Volety 2008, and Rasnake 2011). Lower condition indices at the downstream sites in this study could be due to higher, sub optimal salinities (33 38ppt) persisting during the first 8 months of the study period and more favorable salinities found at the upstream sites (30 37ppt).
Annual means for salinity at Sites 1 and 2 were 25.7 ± 11.3 and 27.7 ± 10.1 respectively and were lower than Sites 3 and 4 that were 30.7 ± 6.1 and 30.6 ± 7.6 respectively. The low rainfall and lack of freshwater inputs kept the northernmost sites in a more optimal salinity range for the first 8 months of the project period.
Site 3 had the lowest condition index (Fig. 14) and was significantly different from all other sites. A low condition index can be indicative of multiple stressors (e.g., disease, poor water quality) acting upon oysters resulting in less energy for growth
(Volety 2008). One observation that was made over multiple months was the presence of a thick mat of filamentous algae blanketing the reef. Previous studies have found that macroalgae blooms can negatively impact oysters by smothering them (impeding 40
feeding), depleting oxygen when they decompose, and harming early life stages with biotoxin production (Leverone et al. 2006, 2007). Excessive algal growth is oftentimes caused by excessive nutrients in the water column, and Haldeman Creek receives drainage from adjacent neighborhoods dominated by canal systems and industrial areas in
Collier County. Nutrient data from Haldeman Creek from May 2010 through October
2011 show 9 out of 16 samples, or 56% of samples, had total nitrogen levels above 0.7 mg/l. Of those, 4 of the total nitrogen samples were greater than 1.0 mg/l. Total phosphorus was not as high for the same time period, showing that 3 of the 16 samples, or 19% of samples, were greater than 0.08 mg/l (Collier County and City of Naples data).
Nutrient thresholds that could cause this type of algal bloom are unknown; however, these nutrient values are above allowable numeric nutrient criteria set by the Florida
Department of Environmental Protection.
Another possible stressor is high accumulations of copper in oyster tissue.
NOAA, through their Mussel Watch Program, has documented elevated copper values at
a nearby monitoring site from 1986 to 2005 (O’Connor and Lauenstein 2005).
Contaminants negatively impact oysters by increasing disease susceptibility and mortality
(Chu and Hale 1994). Oysters concentrate copper more so than other metals, and levels
are oftentimes 10 times higher in oysters than in mussels. For data collected by NOAA between 1986 – 1999, the mean copper concentration in oyster tissue in Haldeman Creek
was 583 µg/g (dry) which is above the 85 th percentile of 360 µg/g (O’Connor and
Lauenstein 2005). In the 2008 NOAA Status and Trends Mussel Watch Program
Publication, copper concentrations ranging between 647 – 1660 ppm were labeled as 41
“high.” Naples Bay oysters tested in 2005 showed levels at 1400 ppm. It is important to note that copper levels in oysters are not known at the other 3 sites in this study, so direct comparisons are not possible. While oysters can accumulate high levels of copper and still maintain physiological function, toxic effects cannot be ruled out at these high levels of accumulation (Kimbrough et al. 2008).
Perkinsus marinus prevalence (% of infected oysters) and distribution are
influenced by temperature, salinity, and concentrations of various pollutants. Higher
temperatures and salinity values promote growth of the organism P. marinus (Burreson
and Ragone Calvo 1996, Soniat 1996, Chu and Volety 1997, Volety 2008), which at high
enough levels can be fatal. P. marinus infection intensity varied significantly among
sampling months (Fig. 15) and sites (Fig. 16). In contrast, prevalence did not vary
significantly among months (Fig. 17), but did vary significantly among sampling sites
(Fig. 18). As expected, the most upstream Site 1 that experiences the lowest salinities
had the lowest prevalence and intensity of infection. In general, increasing infection
intensity was found when moving downstream with the exception of Site 4 which was
similar to Site 2. Site 3 had the highest intensity and prevalence of infection by P.
marinus (and the lowest condition index), which could be the result of additional stressors caused by algal growth or heavy metal accumulation.
Infection prevalence and intensity were lowest in April (Figs. 15, 17) despite constant higher salinities and warmer temperatures. Infection intensity was highest in the summer and early fall months and lowest in the winter months, which is similar to 42
findings from the Caloosahatchee River (Volety 2008). Although mean infection prevalence was high in Naples Bay, overall mean infection intensity was low (0.9 ± 0.3 to
1.9 ± 0.5) and was found to be similar to those observed in Estero Bay (0.5 to 1.7). In contrast, infection intensities were slightly higher in Naples Bay than those observed in the Caloosahatchee River (0.5 to 1.1) and could be explained by those sites reaching lower salinities in the wet season and therefore resulting in lower infection intensities.
When considering data from 2009 2012 for the Caloosahatchee River, overall mean intensity was 1.3 ± 0.5 which is comparable to the overall mean intensity for Naples Bay at 1.4 ± 0.4.
Recruitment of oyster spat onto shell stringers started in April 2011 and continued through October 2011, peaking in August 2011 (Fig. 20). This suggests that adult oysters in Naples Bay were spawning from April – October, although spawning reduced significantly after September. Recruitment studies conducted in Estero Bay (Rasnake
2011) and the Caloosahatchee River (Volety et al. 2003) found similar reproductive periods. All four sites experienced recruitment in April, with Site 4, the southernmost site and furthest from the freshwater influence, having significantly higher recruitment
(Fig. 19). One contributing factor may be that spat get flushed downstream due to the velocity of flows coming from the north (Golden Gate Canal). In addition, Site 4 has the greatest living density per m2 providing a greater supply of oyster larvae than the other sites. Mean recruitment at Sites 1, 2, and 3 were all similar, with the greatest variability among sites occurring in July and August when freshwater flows began.
43
Net oyster recruitment quantified using shell filled trays deployed over the entire study period varied among sites (Fig. 21), but the significance of the results could not be determined due to the high variability in the data from shell loss and replacement.
Despite the challenges in the field with the recruitment trays, results were similar to those found with the shell stringers. Site 4, with a mean number of 2169 ± 341.6 live oysters per m 2, had the highest recruitment of all the sites. Similar to the shell stringers, little difference was found in tray recruitment among the remaining 3 sites, with Site 3 having slightly lower recruitment than Sites 1 and 2. As mentioned previously, this could be the result of filamentous algae which blanketed the reefs for several months hindering recruitment onto the reef and trays. In addition, with Site 3 being located just inside the mouth of Haldeman Creek, freshwater flows coming down the creek could be flushing spat downstream to Site 4. The upstream sites could also be experiencing spat mortality due to extreme swings in salinity.
Living densities (# of living oysters per m 2) varied significantly among sites
(Fig. 23) and between the wet and dry seasons (Fig. 22). Living densities increased when moving upstream to downstream. These findings are similar to those found by Volety
(2008) and Rasnake (2011). Living densities were higher at all sites in the wet season
(June Oct) rather than the dry season, which reflects the increase in juvenile oysters due to spawning and subsequent recruitment of spat onto the reefs. This is contrary to what
Volety et al. (2010) reported for the Caloosahatchee River which found the dry season living densities to be significantly higher (1207 oysters m 2) than the wet season (916
oysters m 2) at 6 sites along a salinity gradient. This could be explained by extremely 44
high flows the Caloosahatchee experiences in the summer months, causing mortality to juvenile oysters and spat. Site 4 had significantly higher living oysters m 2 (1,880 ±
567.9) than the other 3 sites. Sites 1, 2, and 3 had statistically similar living densities with Site 1 showing the lowest living density (742 ± 410.4) followed by Site 2 (895 ±
438.7, Fig. 23). Site 3 had the second highest living density (1,497 ± 768.0 oysters m 2) despite having low monthly recruitment. A mean living density of 1227 ± 3.0 oysters m 2 was reported for the Caloosahatchee River (2009 2012, Volety et al. 2014), as compared to a mean of 1253 ± 529.7 oysters m 2 for Naples Bay.
Oyster length (mm) varied significantly among sampling seasons (Fig. 24) and sites (Fig. 25). Interaction among seasons and sites was significant, indicating that season does have an effect on oyster length. Mean oyster lengths ranged from 45.3 ± 6.2 to 47.3 ± 0.8 mm, and Site 1 was significantly higher than Sites 2, 3, and 4. Dry season mean oyster length was higher than the wet season, which would be indicative of recruitment activities in the wet season, and measuring spat as well as adult oysters.
Oyster lengths measured from the shell filled trays were also recorded, although statistical analysis could not be performed due to a small, highly variable dataset (Fig.
26). Since trays were deployed for the entire study period, they reflect one year of growth, recruitment, and mortality, and may be more representative of oyster length even though the data are highly variable. In contrast to the results above, Site 2 had the largest oysters with Site 1 having the smallest oysters. Sites 3 and 4 had similar mean lengths
(Fig. 26). The smaller oysters from the trays at Site 1 could be the result of a reduced 45
growth rate of spat that settled during the summer months when high freshwater flows caused sub optimal conditions (low salinity) for oyster growth.
Water Quality and Physical Factors
Salinity and temperature values at all four sites exhibited typical seasonal and spatial trends for Southwest Florida estuaries (Figs. 6, 9) including Estero Bay and the
Caloosahatchee River (Volety et al. 2003, Rasnake 2011). Typically, salinity is lower in
Naples Bay during the wet summer months and higher in the cooler, drier months.
Cooler temperatures in drier, winter months increase in the spring and peak during the wet, summer months. Temperature did not vary widely among the sites with values remaining within 2 oC of each other (Fig. 9). Values remained within the optimal 20 oC –
30 oC range 9 out of 12 months with colder, sub optimal values in December and January
(14 oC – 17 oC), and higher values in July (32 oC 33 oC). Dissolved oxygen values were
within the preferred ranges for oysters at all 4 sites (> 20 % saturation) during all 12
months. Similar to temperature, dissolved oxygen values for all sites did not vary widely
and stayed within 2 mg/l of each other with the exception of July when the freshwater
flows started (Fig. 11). In contrast, salinity did vary significantly among the sites with
the most pronounced extremes existing in the upper portions of the bay. Given that
salinity was the most variable factor in this study, one would expect salinity to be the
driving force in the differences observed among sites and seasons for the measured oyster
responses.
46
June is considered the start of the wet season; during this study, however, the wet season started a month later than usual in July 2011. This resulted in high salinities at all sites prior to significant rainfall in July 2011 and into the summer months. Both the salinity data collected during the project period, along with the US Geological Survey datasonde data, reflect the start of the rainfall and freshwater flows from the Golden Gate
Canal in July 2011 with surface salinity values falling from 36 ppt to 5 ppt at Site 1—a decrease of 31 ppt. The USGS datasondes show on a finer scale the oscillations that occur in salinity during the wet season. Even though Site 2 had a similar drop in salinity
(17 ppt) as Site 4 in July, the datasonde data show salinity decreasing from approximately
35 ppt to a low of 9 ppt (a decrease of 26 ppt) at Site 2 in July 2011. Site 2 exhibited extremes in salinity ranging from 5 to 28 ppt through November 2011. The datasonde upstream of Site 1 in the Gordon River was even more variable, and had salinities ranging approximately from 0 to 28 ppt from July 2011 through November 2011. These data highlight the need for continuous salinity readings to capture these extreme events and the entire range of salinity values. Unfortunately, there are no data available for the southern portion of the bay near Sites 3 and 4 as that datasonde, just south of Haldeman
Creek, was not installed until March 2012. For comparison, the southernmost datasonde, just inside Gordon Pass, exhibited a drop of 11 ppt (36 ppt to 25 ppt) in July, with
salinities mostly remaining within this range through mid October 2011.
In addition to suitable water quality, oyster larvae require appropriate
sedimentologic conditions. Oyster larvae settle onto coarse substrates (e.g. sand or shell
gravels) and have higher survival on those substrates with minimal traction transport of 47
sediment (Kennedy 1996). Mature oyster reefs can exist on muddy substrates that are able to support the cumulative weight of adult oysters (Jenkins et al. 1997). Hard, stable substrate used in past oyster restoration projects in numerous estuaries have included loose shell, shell bags, rocks, and reef balls. Areas that have suitable substrate as well as optimal water quality are where oysters will thrive and have the best chance for forming dense reefs. The presence of hard, stable substrate is a key consideration in determining suitable locations for oyster restoration activities. In an effort to determine the distribution of existing substrate availability for reef development in Naples Bay, a surface and subsurface substrate mapping effort was conducted using shallow seismic
CHIRP (Compressed High Intensity Radar Pulse) and side scan sonar in May 2005
(Savarese et al. 2006, Dellapena et al. 2013). Since suitable substrate greatly affects the distribution of oyster reefs, this study investigated where such materials were located in
Naples Bay and its tidal creeks, and whether more prolific substrate availability was present in the shallow subsurface. Shallow seismic CHIRP was used to detect any buried oyster reefs in the shallow subsurface. The study found that the periphery of the bay and areas surrounding mangrove islands exhibited shallow buried reefs, confirming the historical existence of oyster reefs as seen in old aerial photographs. It is important to note, however, that widespread subsurface mapping of all historical reef distribution was not possible, as reefs were physically removed starting in the 1940s during dredging projects and development activities. Using side scan sonar, maps were produced by
Savarese et al. (2006) and Dellapena et al. (2013) characterizing the existing benthos and
substrate types. They found that the southeast shorelines of Naples Bay and Haldeman
Creek (adjacent to Sites 3 and 4 in this study) have more natural substrate due to the 48
presence of fringing mangroves rather than seawalls in the west. It is also important to
note that when the bay margins are left undeveloped, oyster reefs occur as fringe habitat
due to the gradual slopes into intertidal depths. This allows greater accommodation space
for oysters than when seawalls and dredged basins line the bay perimeter, as they do
today. They also found that fringing reefs exist to the south along with low density
oyster shell which indicates areas of former productive reef growth. When just
considering substrate requirements, these areas in the southern portion of the bay are
conducive for future reef restoration due to the available areas of sand and shelly
substrate. However, Savarese et al. (2006) emphasize that water quality is also a key
factor to consider when choosing restoration sites. This current study fills that gap and
considers both substrate and water quality when choosing suitable restoration sites.
Salinity ranges found in this study are conducive to oyster reef growth at this southern
area adjacent to Sites 3 and 4.
Management Implications
Identifying the differences in water quality, oyster health, recruitment potential,
and shallow substrate availability in upstream versus downstream locations is essential
when considering restoration strategies. A primary objective of this study is to link
measured oyster responses with water quality parameters in order to identify potential
oyster restoration sites in Naples Bay given the current water quality conditions. Long
term water quality data showed significantly lower salinities at the most upstream Site 1
(Fig. 7) with extreme swings in salinity coinciding with peak oyster reproduction. These
low salinities (5 8 ppt) fall well below the optimal range of 14 28 ppt (Fig. 6), suggesting 49
that Site 1 would not be suitable for oyster restoration. Potential oyster restoration efforts appear to be best targeted in the southern portion of the bay which is furthest from the freshwater influence and therefore experiences less extreme swings in salinity that can stress oysters and cause mortality. In addition, Site 4 had the highest living density of oysters and the highest recruitment of spat on both shell stringers and shell filled trays.
Ample shallow hard substrate has also been documented in the southern portion of the bay. Although the northern part of the bay has moderately high mean living densities
(742 ± 410.4 and 895 ± 438.7), restoration efforts would be better focused in the southern part of the bay where salinities are less “flashy.” Historical extent of oyster reefs, as
observed in 1950s aerials, was greater in the southern portion of the bay as well.
One factor that must be considered as a part of any restoration project in the
southern part of Naples Bay is the high energy environment that exists due to boat wakes.
Large wakes constantly pound the shoreline and erosion of formerly existing reefs has
occurred. Therefore, creating reefs using shell filled bags would be preferable to loose
cultch which would rapidly scatter from the wave energy. Wall et al. (2005) found that
survival of juvenile oysters was significantly reduced on reefs impacted by recreational boating activity and that dead margins resulted following boat wake impacts. They found
that high relative water motion, and high sediment loads and percent silt/clay caused
Crassostrea virginica to do poorly on impacted reefs. Reef restoration design can
mitigate these factors and reduce the potential for erosion. For example, stacking cultch bags in front of and among existing reefs would help limit further erosion. Also
designing reefs to provide considerable vertical relief by stacking bags higher on the side 50
fronting the boat channel and tiering the bags shoreward would likely protect the backside of the reef, allowing oysters to become established despite the constant energy produced from boat wakes.
As the South Florida Water Management District and Collier County plans move forward, diverting a significant portion of fresh water from the Golden Gate Canal would reduce the tremendous flows into Naples Bay through the Gordon River (Atkins 2011).
Potential ramifications of this would be a reduction in the salinity gradient as well as in salinity extremes. Optimal and more stable salinities would expand the region of suitable restoration habitat northward into the bay and Gordon River allowing for increased recruitment and natural expansion of oyster reefs. Unfortunately, there is less fringing habitat in the northern part of the bay, so restoration here would likely involve the bay’s interior as well as its shoreline. Decreased flow volumes would also result in greater retention of oyster larvae upstream to populate existing or restored reefs. Restoration success here would not have to contend with the problem of boat wakes seen in the southern part of the bay. All navigable waters in the northern part of Naples Bay and all of the Gordon River are zoned “idle speed, no wake.”
Managing flows and implementing freshwater diversions from the Golden Gate
Canal will require consideration of timing, duration and the magnitude of flows. Not only is the magnitude of freshwater flowing into Naples Bay excessive in the wet season, the timing of peak flows coincides with oyster reproduction. These intense freshets result in extreme decreases in salinity over the course of several days that result in detrimental 51
impacts. When altering these flows, it is recommended that a range of flows be considered since having some minimal flow into the estuary is beneficial. Also, the intensity of the freshets should be minimized by having flows released incrementally during the wet season. This would result in gradual decreases in salinity which is less stressful on the ecosystem and allows for biota to acclimate to seasonal changes.
Previous mapping efforts have identified the remaining oyster reef locations in
Naples Bay and the Gordon River, but the health of those reefs was unknown. This study was able to establish a baseline of oyster health and spat recruitment in Naples Bay.
These findings demonstrate how oyster health responses can be linked with various stressors such as extreme salinity swings and excess nutrients (creating filamentous algae blooms). It also provides a greater understanding of the cumulative impacts from development activities, altered hydrology, physical impacts from dredging, and degraded water quality on oyster health. Past studies have demonstrated that salinity is a driving force for oyster reef health, and Naples Bay is no different. This study also provides a basis for choosing optimal restoration areas based on the current health of existing reefs, the recruitment potential in Naples Bay and the Gordon River, and the availability of suitable substrate. Recognizing that oysters are exposed to multiple stressors at any given time, further investigation is needed to account for numerous other factors such as predation, metals, pesticides, PCBs, red tide events, bivalve competition and so forth. All
of these stressors can contribute to increased expenditure of energy reserves, negatively
impacting growth, fecundity, and larval survival, and can result in an impaired defense
system causing increased disease susceptibility (Chu and Hale 1994, Anderson et al. 52
1996, Volety and Savarese 2001). In addition, diversity and abundance of commensal species that inhabit and directly rely on oyster reefs should be investigated when looking at managing water flows within an estuary. For example, Tolley et al. (2006) found that community structure and diversity of commensal species varied significantly along a salinity gradient in the Caloosahatchee River Estuary. Because the eastern oyster is so prolific in the Gulf of Mexico and Atlantic waters and has extensive water quality and ecosystem benefits, many regions that have experienced significant oyster loss and altered watersheds similar to Naples Bay can employ parallel techniques in determining the restoration potential and health of their oyster reef ecosystems.
53
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Tolley, G.S., A.K. Volety, M. Savarese, L.D. Walls, C. Linardich, and E.M. Everham III. 2006. Impacts of salinity and freshwater inflow on oyster reef communities in Southwest Florida. Aquatic Living Resources 19:371–387.
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Volety, A.K. 2008. Effects of salinity, heavy metals and pesticides on health and physiology of oysters in the Caloosahatchee Estuary, Florida . Ecotoxicology 17:579– 590.
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Figure 1. This map shows the study area and the four sampling locations in the Naples Bay/Gordon River Estuary and the long term City and County water quality locations.
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Figure 2. This map shows a comparison of historical Naples Bay (1953) and current day Naples Bay (2010). The channelized neighborhood seen today on the left side of the photo is Port Royal and used to be mangrove wetlands as observed in the 1953 photo. Note the oyster bars throughout the bay in the 1953 aerial.
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Figure 3. This map shows the Golden Gate Canal Weirs #1 and #2, and the 4 USGS datasonde locations. 66
Figure 4. This map shows both the historical (10 sq mile) watershed and the expanded watershed (120 sq mile) that resulted from the dredging of the Golden Gate Canal (South Florida Water Management District). 67
Figure 5. This map shows a habitat comparison between 1953 and 2003 and the approximate historic versus present day oyster and seagrass coverage (Schmid et al. 2005).
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45 Site 1 40 Site 2 Site 3 35 Site 4 30 25 20 15 Salinity Salinity (ppt) 10 5 0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct '10 '10 '11 '11 '11 '11 '11 '11 '11 '11 '11 '11
Sampling Month
Figure 6. Monthly salinities (ppt) at each site showed a delayed start to the rainy season, which typically begins in June. Site 1 had the most extreme salinity swing and dropped 31 ppt within a few days.
40 B B B 35 A 30
25
20
15
Salinity Salinity (ppt)2005-2011 10
5
0 Site 1 Site 2 Site 3 Site 4
Figure 7. Mean salinities (ppt) from long term water quality sites adjacent to oyster research sites were recorded from 2005 2011. Salinities varied significantly among sites (p < 0.0001). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation. 69
40 B A Dry Season B B Wet Season 35 B* B* 30 B*
25 A*
20
15
Salinity Salinity (ppt)2005-2011 10
5
0 Site 1 Site 2 Site 3 Site 4
Figure 8. Mean salinities (ppt) from long term water quality sites varied significantly among sites and between seasons (p < 0.5). Dry season salinities were significantly higher than the wet season. Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
Site 1 40 Site 2 35 Site 3 Site 4
C) 30 o 25 20 15 10 Temperature ( 5 0 Nov Dec Jan Feb Mar Apr May Jun Jul '11 Aug Sep Oct '10 '10 '11 '11 '11 '11 '11 '11 '11 '11 '11
Sampling Month
Figure 9. Monthly temperatures ( oC) at each site showed a typical increasing trend into the summer months. Temperature values were similar among sites (within 2 oC) for a given month. 70
35
30
25
20 C)2005-2011 o 15
Temp( 10
5
0 Site 1 Site 2 Site 3 Site 4
Figure 10. Mean temperatures ( oC) from long term water quality sites were approximately 25 oC for all sites. Error bars represent one standard deviation.
12 Site 1 10 Site 2 Site 3 8 Site 4 6 DO(mg/l) 4
2
0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct '10 '10 '11 '11 '11 '11 '11 '11 '11 '11 '11 '11
Sampling Month
Figure 11. Monthly dissolved oxygen values at each site were similar for a given month and stayed within 2 mg/l of each other (with the exception of July). Due to equipment failure, data were not recorded for September or October 2011. 71
8 7 6 5 4 3 DO(mg/l) 2005-2011 2 1 0 Site 1 Site 2 Site 3 Site 4
Figure 12. Mean dissolved oxygen values from long term water quality sites were all within the range of 5 6 mg/l. Error bars represent one standard deviation.
4.5 4.0 3.5 3.0 2.5 2.0 1.5
ConditionIndex 1.0 0.5 0.0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct '10 '10 '11 '11 '11 '11 '11 '11 '11 '11 '11 '11
Sampling Month
Figure 13. Monthly mean condition index of oysters from all sampling sites varied significantly among sampling months (p < 0.0001) and sites (p < 0.0001). Error bars represent one standard deviation.
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4.5 A 4.0 A
3.5 C 3.0 B 2.5
2.0
1.5
ConditionIndex 1.0
0.5
0.0 Site 1 Site 2 Site 3 Site 4
Figure 14. Mean condition index of oysters for each site varied significantly among sites (p < 0.0001). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
3.0
2.5
2.0
1.5
1.0 InfectionIntensity 0.5
0.0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sept Oct '10 '10 '11 '11 '11 '11 '11 '11 '11 '11 '11 '11
Sampling Month
Figure 15. Monthly mean infection intensity of P. marinus from all sampling sites varied significantly among sampling months (p < 0.0001) and sampling sites (p < 0.001). Error bars represent one standard deviation. 73
C 2.5
2.0 B B
1.5 A
1.0 Infection Intensity 0.5
0.0 Site 1 Site 2 Site 3 Site 4
Figure 16. Mean infection intensity of P. marinus for each site varied significantly among sampling sites (p < 0.001). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
100 90 80 70 60 50 40 30
Infected oysters (%) 20 10 0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sept Oct '10 '10 '11 '11 '11 '11 '11 '11 '11 '11 '11 '11
Sampling Month
Figure 17. Monthly mean prevalence (%) of infected oysters did not vary significantly among months, but did vary significantly among sampling sites (p = 0.005). Error bars are too small to show on graph.
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B B B 100 90 A 80 70 60 50 40 30
Infected oysters (%) 20 10 0 Site 1 Site 2 Site 3 Site 4
Figure 18. Mean prevalence (%) of infected oysters varied significantly among sampling sites (p = 0.005). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
9
8 B
7
6
5 A 4 A 3 A
Spat/shell/month 2
1
0 Site 1 Site 2 Site 3 Site 4
Figure 19. Mean recruitment per shell per month varied significantly among sampling sites (p < 0.003). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
75
8 B 7 B B 6 B 5
4 B 3
2 A Spat/shell/month 1 A 0 Apr '11 May '11 Jun '11 Jul '11 Aug '11 Sep '11 Oct '11
Sampling month
Figure 20. Monthly mean recruitment per shell per month varied significantly among sampling months (p < 0.0001), peaking in August. Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
3000
) 2500 -2
2000
1500
1000
500 NetRecruitment (m 0 Site 1 Site 2 Site 3 Site 4
Figure 21: Mean net recruitment using triplicate shell trays were too variable to run statistics. Error bars represent one standard deviation. .
76
3000 Wet Season A A Dry Season 2500 ) -2 A* 2000 AB 1500 B AB* B* 1000 B* Living Density (m 500
0 Site 1 Site 2 Site 3 Site 4
Figure 22: Mean living densities by wet and dry season varied significantly among seasons and sites (p < 0.05). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation. .
3000 A 2500 AB ) -2 2000
1500 B B 1000 Living Density (m 500
0 Site 1 Site 2 Site 3 Site 4
Figure 23: Mean living densities varied significantly among sites (p < 0.05). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation. 77
70 Wet Season 60 A* Dry Season A A* A* 50 A B* B 40 B
30
Oyster Oyster Length(mm) 20
10
0 Site 1 Site 2 Site 3 Site 4
Figure 24: Mean oyster length (mm) by wet and dry season varied significantly between sampling seasons (p < 0.0001) and among sites (p = 0.0067). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
60 B A B B 50
40
30
20
10 Oyster Oyster length(mm) 0 Site 1 Site 2 Site 3 Site 4
Figure 25: Mean oyster length (mm) varied significantly among sampling sites (p = 0.0067). Statistically significant differences are denoted by letters above data results where matching letters indicate results that are statistically similar. Error bars represent one standard deviation.
78
40 35 30 25 20 15 10 Oyster Oyster Length(mm) 5 0 Site 1 Site 2 Site 3 Site 4
Figure 26: Mean oyster lengths (mm) in triplicate shell trays were too variable to run statistics. Error bars represent one standard deviation.