Introduction
Among Bivalvia, oysters have unique growth patterns and life history strategies. Bivalves are characterized by laterally compressed soft bodies enclosed in paired valves, which are attached to one another by a dorsal hinge. Typically, the bivalve morphology includes two adductor muscles, one anterior and one posterior to the hinge, and an extendable foot that facilitates burial. Valve morphology is generally conservative across the class and the vast majority of bivalve species are infaunal. Few groups in Bivalvia stray from this general plan; however, oysters have lost both the anterior adductor muscle and the foot. Modern oysters in the Family Ostreidae, particularly the cupped oysters of the genus Crassostrea, show remarkable variation in individual shape and allometry, and are gregarious, forming complex, three-dimensional reefs. Reef formation is facilitated by the oyster life history, where pelagic larvae preferentially settle, metamorphose, and cement themselves onto the shells of extant adults (Bonar et al., Reference Bonar, Coon, Walch, Weiner and Fitt1990; Turner et al., Reference Turner, Zimmer-Faust, Palmer, Luckenbach and Pentchef1994; Tamburri et al., Reference Tamburri, Finelli, Wethey and Zimmer-Faust1996, Reference Tamburri, Luckenbach, Breitburg and Bonniwell2008). Reefs are maintained by rapid growth and variable shell morphology, which maximizes shell production relative to biomass and provides abundant substrate for larval settlement (Powell and Stanton Jr, Reference Powell and Stanton1985; Mann et al., Reference Mann, Harding and Southworth2009a, Reference Mann, Southworth, Wesson, Thomas, Tarnowski and Homer2022; Powell et al., Reference Powell, Mann, Ashton-Alcox, Kim and Bushek2016). Though unusual, the oysters' life history strategy led to their success over geological time scales.
Oysters provide critical hard benthic structure in temperate estuaries worldwide. The oyster form emerged in the Triassic (252–251 mya) as the fossil Liostrea sp, which were epifauna on ammonites in marine habitats (Hautmann et al., Reference Hautmann, Ware and Bucher2017). The subsequent Gryphaea sp. shifted to shallow subtidal habitats and exhibited thick, deeply cupped asymmetrical valves (McRoberts, Reference McRoberts1992; El-Sabbagh and El Hedeny, Reference El-Sabbagh and El Hedeny2016; Hautmann et al., Reference Hautmann, Ware and Bucher2017). The modern Ostreidae oysters occupy shallow coastal and estuarine habitats (Gunter, Reference Gunter1954; Li et al., Reference Li, Kou, Zhang, Hu, Huang, Cui, Liu, Ma and Wang2021). The Ostreid form, particularly those in the genus Crassostrea, facilitated the invasion into intertidal, estuarine habitats. The success of this form is predicated on individual plasticity in growth and shell shape across the post settlement life stages, such as rapid juvenile growth along irregular substrates, development of asymmetrical valves, and longevity to a large terminal size which ensures accumulation and maintenance of the underlying reef structure.
Understanding allometric relationships is a fundamental part of fisheries science. Length–weight relationships are used to relate easily measured dimensions, such as length, to biomass for a variety of taxa (Hilborn and Walters, Reference Hilborn and Walters1992; Froese, Reference Froese2006; Sousa et al., Reference Sousa, Vasconcelos and Riera2020). Traditionally, length–weight relationships are described using the model formulation Wi = aLib, where Wi is the weight and Li is the length for the i th individual. The parameter b is a coefficient that controls the strength of the exponential relationship, which facilitates inference on growth patterns (e.g. isometric vs allometric growth). For bivalves and a variety of other molluscs, the parameter b is approximately 3, indicating isometric growth (Powell and Stanton Jr, Reference Powell and Stanton1985; Tokeshi et al., Reference Tokeshi, Ota and Kawai2000; Gaspar et al., Reference Gaspar, Santos and Vasconcelos2001; Hemachandra, Reference Hemachandra2008). In contrast, many oyster species, due to indeterminate growth and highly variable conditions across estuaries (e.g. salinity, temperature, reef density), b may be below 3, indicating allometric growth (Powell et al., Reference Powell, Mann, Ashton-Alcox, Kim and Bushek2016). While there is a general acknowledgement that oysters have highly variable growth, few studies have quantified variability in oyster allometry (Galtsoff, Reference Galtsoff1964; Kennedy et al., Reference Kennedy, Newell and Eble1996; Mann et al., Reference Mann, Southworth, Harding and Wesson2009b; Nagi et al., Reference Nagi, Shenai-Tirodkar and Jagtap2011; Powell et al., Reference Powell, Mann, Ashton-Alcox, Kim and Bushek2016).
Herein, we explore variation in allometry for eastern oysters (C. virginica Gmelin, 1791) collected from reefs in the western tributaries and main stem in the Virginia portion of the Chesapeake Bay. The specific project objectives are to: (1) describe the proportional carbonate contributions from each valve; and (2) examine oyster allometry, for both shell and tissue weight, in the Chesapeake Bay using a nonlinear mixed-effects model framework.
Materials and methods
Sample collection
To describe oyster morphometric relationships, oysters were collected during annual fall (September through December) stock assessment surveys (dredge and patent tong) in the western tributaries and the main stem of the Chesapeake Bay as well as Tangier and Pocomoke Sounds. Dredge survey methods are described in detail in Southworth and Mann (Reference Southworth and Mann2020) and Mann et al. (Reference Mann, Southworth, Harding and Wesson2009b). Patent tong survey methods are described in Southworth et al. (Reference Southworth, Harding, Wesson and Mann2010) and Harding et al. (Reference Harding, Mann, Southworth and Wesson2010). The stock assessment programme collects oysters across a size range from 19 reef locations annually to monitor body condition and shell morphometrics. Collections from 2021 and 2022 were included in the analyses. Additionally, large oysters, >100 mm in shell length (umbo to ventral margin), were opportunistically collected across all survey locations in 2019, 2020, and 2021. We collected a total of 1122 oysters from 48 reefs in eight tributaries and the main stem of the Virginia portion of the Chesapeake Bay (Figure 1; Table 1). Oyster collections reflect the size availability in extant populations, except for Lower Sturgeon Sanctuary, where collections focused on larger individuals.
Figure 1. Map of the Virginia Portion of the Chesapeake Bay showing the locations of 48 reefs where samples were collected. Sites with ≥20 individuals collected (triangles) were used in the length–weight model. Grey boxes indicate spatial domain for Virginia Estuarine Coastal Observing System (VECOS; http://vecos.vims.edu/) data flow programme, which was used to compare environmental conditions.
Table 1. Summary of oyster collections in the Virginia portion of the Chesapeake Bay
Shell lengths are reported in mm, dry shell and dry tissue weights are reported in g, and n denotes the sample size from each reef. Standard deviations are only reported in cases where there are ≥3 individuals collected. Shaded rows indicate reefs with ≥20 individuals which were included in the length–weight model.
All oysters were brought back to the lab for processing. We removed biofouling from the exterior of the shell and measured shell length (umbo to ventral margin) to the nearest 0.1 mm. Soft tissue was removed from the valves and both tissue and shells were dried to a constant weight at 80°C (72 h) to obtain dry shell and dry tissue weights. All measurements were to the nearest 0.01 g.
Proportional shell weight
To estimate the proportional weight of the left valve, we dried and weighed the left and right valves of specimens with fully intact valves. The proportional weight was defined as the dry weight of the left valve divided by the combined dry weight of both valves. We calculated the mean proportional weight of the left valve across specimens. We investigated the relationship between the proportional weight of the left valve and oyster length using a simple linear regression.
Length–weight relationships
Traditionally, length–weight relationships are described using the following nonlinear model formulation:
where Wi = weight of the i th individual, Li = length of the i th individual, a and b are constants, and εi is the error associated with the i th individual. The parameter b is a coefficient controlling the strength of the exponential relationship. Often this formulation, specifically the normally distributed error structure, is inappropriate, due to increasing variability in weight as individuals increase in size (heteroscedasticity). The nonlinear model formulation can be modified to incorporate a multiplicative error structure (2) and transformed to a log-log linear model (3) to make the errors additive and stabilize variance.
Given that oyster reefs are aggregations of individuals living under similar conditions, there is inherent clustering within the data which violates independence (Pinheiro and Bates, Reference Pinheiro and Bates2000; Zuur et al., Reference Zuur, Ieno, Walker, Saveliev and Smith2009). Thus, we extended the previous model formulation to a nonlinear mixed-effects model (NLMM) and incorporated reef as a random-slope effect to account for spatial variability (4).
In this final model formulation, Wij = weight of the j th individual from the i th reef and Lij = length of the j th individual from the i th reef. We used this model formulation to explore the relationship between oyster biomass, as both dry tissue weight (g) and dry shell weight (g), and length. All statistical analyses were completed in R Version 4.3.1 (R Core Team, 2023) using the nlme package (Pinheiro et al., Reference Pinheiro and Bates2023). Figures were created using the ggplot package (Wickham, Reference Wickham2016).
Local conditions
Long-term water quality monitoring was not available for each reef location. We accessed water quality data from the Virginia Estuarine Coastal Observing System (VECOS, http://vecos.vims.edu/) data flow programme for upriver and downriver regions of tributaries which had concurrent monitoring across rivers. We identified three tributaries (James, York, and Rappahannock) which had biweekly or monthly data flow cruises in 2007 and 2008 (Figure 1). While the VECOS data does not coincide with our oyster collections, it characterizes the general seasonal patterns and the upriver to downriver gradient in environmental conditions. The data flow system pumps water through a YSI 6600 multiparameter sonde and measures salinity, turbidity, water temperature, pH, and dissolved oxygen every 3–4 s. In wider tributaries, such as the James, York, and Rappahannock, the vessel follows fixed depth contours (shallow <2 m; mid-depth ~5 m; channel >10 m) running parallel to the shoreline to characterize water conditions throughout a tributary segment.
Oyster population density data was available from annual fisheries independent patent tong surveys run by the Virginia Institute of Marine Science and Virginia Marine Resources Commission. During fall surveys, a patent tong is used to sample 1 m−2 of bottom reef habitat on oyster reefs in the main stem and western tributaries of the Chesapeake Bay, as well as Tangier and Pocomoke sounds (Mann and Wesson, Reference Mann and Wesson1994, Reference Mann and Wesson1997; Mann et al., Reference Mann, Southworth, Harding and Wesson2009b; Harding et al., Reference Harding, Mann, Southworth and Wesson2010; Southworth et al., Reference Southworth, Harding, Wesson and Mann2010). Oysters were measured from umbo to ventral margin (length) to the nearest millimetre and qualitatively assessed as either young of the year or adult oysters (Southworth et al., Reference Southworth, Harding, Wesson and Mann2010). We accessed oyster population data from 2019 to 2021 during the time period when oysters were collected and quantified mean adult oyster density for each reef.
Results
Collection summary
A total of 1122 individual oysters were collected from 48 reefs in eight tributaries and the main stem of the Chesapeake Bay (Figure 1, Table 1). An average of 23.4 individuals (±23.3 SD, range 1–58) were collected from each reef. Shell lengths, measured from umbo to ventral margin, ranged from 24.9 to 172 mm. Dry shell weights and dry tissue weights ranged from 1.02 to 405.95 and 0.03 to 8.20 g, respectively.
Proportional shell weight
A subset of individuals with intact valves (n = 807) were used to estimate the proportional weight of the left valve. These individuals comprised the entire range of shell lengths from the collections (24.9–172 mm). On average, the proportional weight of the left valve was 0.5614 or approximately 56% (±0.2% SE) of the total weight of the shell. The best-fit equation describing the relationship between proportional weight of the left valve (Lpro) and valve length (L) was Lpro = 0.55 + 0.00015×L (Figure 2). Despite a significant relationship, the model only explained 0.6% of the variation in proportional weight of the left valve (F = 6.24, df = 1, 805, P < 0.05, adjusted R 2 = 0.006) and provides evidence for a minute increase in the proportion of the total weight contributed by the left valve as individuals grow.
Figure 2. Proportional weight of the left valve for oysters in the Virginia portion of the Chesapeake Bay. The mean proportional weight of the left shell is 0.5614 (±0.002 SE, dashed grey line). The linear relationship is described as LPro = 0.55 + 0.00015×L, where Lpro is the proportional weight of the left valve and L is the valve length in mm (pink line). Pink shading indicates the 95% confidence interval.
Length–weight relationships
To examine length–weight relationships for oysters, we focused our analysis on reefs where ≥20 individuals were collected (Table 1). We included 20 reefs across eight tributaries and 1004 individual oysters in an NLMM. In the NLMM with dry shell weight as the response, on average b was estimated as 2.43 (95% CI = 2.35, 2.51). The random effect provides insight on the change in weight associated with an oyster growing on a particular reef. The random effect b coefficients were variable among reef locations (Figure 3). Notably, three reefs in the James (Upper Deep, Middle Horse, Point of Shoal) had lower reef specific b coefficients than other sites and, therefore, oysters collected from these reefs had less shell biomass on average for a given length (Figure 4). Reef as a random effect explained 11.42% of the total random variance in dry shell weight.
Figure 3. Estimated random-effect coefficients from the dry shell length–weight relationship for reefs (n = 20) in the eight tributaries of the Chesapeake Bay. Dashed line indicates the mean response. For tributaries with multiple reefs, the reefs are organized from upriver (top) to downriver (bottom).
Figure 4. Predicted dry shell length–weight relationships for reefs (n = 20) in the eight tributaries of the Chesapeake Bay. Grey lines indicate the mean response across all reefs. Coloured lines indicate the predicted length–weight relationship for each reef. Points show data observations. Colours correspond to the tributary of origin.
In the NLMM with dry tissue weight as the response, on average b was estimated as 2.03 (95% CI = 1.97, 2.10). Similar to dry shell weight, the random effect b coefficients were variable among reef levels (Figure 5). The same three reefs in the James (Upper Deep, Middle Horse, Point of Shoal) had lower reef specific b coefficients than other sites which indicates oysters collected from these reefs had lower tissue biomass on average for a given length (Figure 6). Reef as a random effect explained 5.3% of the total random variance in dry tissue weight.
Figure 5. Estimated random-effect coefficients from the dry tissue length–weight relationship for reefs (n = 20) in the eight tributaries of the Chesapeake Bay. Dashed line indicates the mean response. For tributaries with multiple reefs, the reefs are organized from upriver (top) to downriver (bottom).
Figure 6. Predicted dry tissue length–weight relationships for reefs (n = 20) in the eight tributaries of the Chesapeake Bay. Grey lines indicate the mean response across all reefs. Coloured lines indicate the predicted length–weight relationship for each reef. Points show data observations. Colours correspond to the tributary of origin.
Local conditions
We accessed VECOS data flow monitoring data for upriver and downriver segments of the James, York, and Rappahannock tributaries. The VECOS programme measured water quality at 227,845 points across the six tributary segments. We excluded 1432 observations (<1%) due to being outliers. On average, the upper James had lower salinity in both 2007 and 2008 compared to the other tributary segments (Figure 7). In spring months (March, April, May), the upper James had substantially higher turbidity in both 2007 and 2008 compared to the other tributary segments (Figure 7). All segments had comparable variability in temperature, dissolved oxygen saturation, and pH during the 2007 and 2008 survey period (Supplementary Figure S1).
Figure 7. Turbidity (top) and salinity (bottom) measurements from upper and lower regions of the James, Rappahannock, and York tributaries. Data show the monthly means (±SE) from the Virginia Estuarine Coastal Observing System (VECOS; http://vecos.vims.edu/) data flow programme.
The annual patent tong surveys included 19 of the 20 reefs included in the length–weight model. Only Bell Rock in the York tributary did not have oyster population data available. Across the 19 reefs, adult oyster density ranged from 7.0 to 492.9 oysters m−2 on average (Figure 8A). Reefs in the upper James (Upper Deep, Middle Horse, and Point of Shoal) had markedly higher mean oyster densities compared to lower James reefs and reefs in other tributaries. Higher mean oyster densities were associated with lower reef specific b coefficients (Figure 8B).
Figure 8. (A) Mean (±SE) oyster density m-2 for 19 reefs within eight Chesapeake Bay tributaries. For tributaries with multiple reefs, the reefs are organized from upriver (left) to downriver (right). (B) Relationship between mean oyster density (m-2) and estimated b coefficients for dry shell weight.
Discussion
This work explores variation in eastern oyster (C. virginica) allometry across reefs in the main stem and tributaries of the Virginia portion of the Chesapeake Bay. We documented the proportional relationship between oyster valves across a size range. On average, the left valve was responsible for ~56% of the weight of the shell. Further, oyster length–weight relationships showed substantial inter-reef variation, where upriver reefs in some tributaries appear to produce less shell and tissue biomass on average for a given size. We posit this variability may be due to differences in local conditions. In particular, the upriver James reefs are characterized by high turbidity in spring months and lower salinity throughout the year compared to other sites in 2007 and 2008; though temperature, dissolved oxygen, and pH were similar across all sites. Oyster density is considerably higher at the upriver James reefs relative to other sites. Though concurrent environmental monitoring is not available across all tributaries and reef locations, these observations suggest local conditions may play an important role in determining oyster growth patterns.
Local conditions
Estuaries are highly dynamic environments, where environmental conditions may vary dramatically across temporal scales (e.g. tidal, seasonal, annual). Eastern oysters tolerate a wide range of conditions and occupy estuaries along eastern North America from the Gulf of Mexico to the Gulf of St. Lawrence; however, due to oysters' sessile life history, they are unable to escape physiologically stressful conditions when they occur. Oysters can endure stressful periods by closing their valves and relying on anaerobic metabolism, whereupon they are unable to filter feed or flush accumulated toxic metabolites (Michaelidis et al., Reference Michaelidis, Haas and Grieshaber2005; Meng et al., Reference Meng, Wang, Li and Zhang2018). Therefore, local conditions are intimately linked with oyster growth and carbonate production.
Salinity influences oyster distribution, reproduction, and survival (Loosanoff, Reference Loosanoff1953; Shumway, Reference Shumway, Kennedy, Newell and Eble1996; Bayne, Reference Bayne2017; Scharping et al., Reference Scharping, Plough, Meritt and North2019). Eastern oysters occupy habitats where average salinities exceed 5 (Galtsoff, Reference Galtsoff1964; Castagna and Chanley, Reference Castagna and Chanley1973). In low salinity environments, juvenile and adult oysters experience slower growth, but reduced predation and disease pressure (Kraeuter et al., Reference Kraeuter, Ford and Cummings2007; Munroe et al., Reference Munroe, Borsetti, Ashton-Alcox and Bushek2017; Manuel et al., Reference Manuel, Hare and Munroe2023). In contrast, oysters in high salinity experience faster growth, but increased predation and disease pressure. Oysters living on the upper James reefs experience lower salinity throughout the year, which are either below or on the lower end of the physiological optimum (~12–24 ppt) for oysters (Shumway, Reference Shumway, Kennedy, Newell and Eble1996). Our oyster collections occurred during the post-spawning rebuilding phase in fall months. During this time, oysters in the upper James are physiologically compromised due to a combination of higher temperatures and lower salinity, which may be causing the observed lower tissue weights for a given size.
Turbidity influences individual oyster survival and growth patterns, as well as reef persistence. Oysters prefer filtering in relatively clear water and, in the presence of suspended sediments, will close their valves (Loosanoff, Reference Loosanoff1962; Poirier et al., Reference Poirier, Clements, Coffin, Craig, Davidson, Miron, Davidson, Hill and Comeau2021). Valve closure reduces opportunities for oysters to respire and filter feed; however, sedimentation or persistent high suspended sediment loads for extended periods of time may directly cause oyster mortality (Rothschild et al., Reference Rothschild, Ault, Goulletquer and Héral1994; Comeau, Reference Comeau2014; Poirier et al., Reference Poirier, Clements, Coffin, Craig, Davidson, Miron, Davidson, Hill and Comeau2021). When oyster reefs are crowded and in muddy bottom habitats, oysters tend towards an elongate, narrow shell shape (Galtsoff, Reference Galtsoff1964; Quayle, Reference Quayle1988). The upper James reefs are high density, patchy reefs with higher reef relief (generally >15 L shell m−2 above the sediment-water interface). Higher reef relief helps mitigate the impacts of sedimentation and contributes to overall reef persistence (Colden et al., Reference Colden, Latour and Lipcius2017). Oysters living in the upper James experience both crowding and higher turbidity, which was associated with an elongated growth form relative to other sites. The elongate growth pattern contributes to the observed lower average shell biomass for a given size. Anecdotally, juvenile oyster moved from the upper James to other tributaries as part of ‘seed’ movements lose the elongate form and adopt the morphological characteristics of the recipient location, which suggests that pressures in the local environment are driving the observed growth patterns.
Oysters have highly variable growth patterns; however, few studies have quantified variability in oyster allometric relationships across an estuarine gradient. Prior work focuses on the relationship between length and tissue biomass. For eastern oysters (C. virginica), the average b coefficient for length–dry tissue weight relationships is generally close to 2 (Dame, Reference Dame1972; Powell et al., Reference Powell, Klinck, Hofmann, Wilson-Ormond and Ellis1995, Reference Powell, Mann, Ashton-Alcox, Kim and Bushek2016; Grizzle et al., Reference Grizzle, Greene and Coen2008; Mann et al., Reference Mann, Southworth, Harding and Wesson2009b). We estimated the average b coefficient as 2.03 in the Virginia portion of the Chesapeake Bay. Previous work estimated b as 2.3 in the Piankatank (Harding et al., Reference Harding, Mann, Southworth and Wesson2010), 2.7 in the Great Wicomico (Southworth et al., Reference Southworth, Harding, Wesson and Mann2010), and, on average, 2.04 (range 1.6–2.8) in the Virginia portion of the Chesapeake Bay (Powell et al., Reference Powell, Mann, Ashton-Alcox, Kim and Bushek2016); however, these estimates encompass a narrower size range or are tributary wide averages, which do not explicitly account for differences in oyster growth among reefs. In the James River, b was estimated as 2.15 at Swash reef (Mann et al., Reference Mann, Southworth, Harding and Wesson2009b). Swash is near the upriver sites in the James where we observed the lowest b coefficients; however, Swash differs by having substantially lower oyster density and, thus, oysters exhibit more ovoid shape (Mann et al., Reference Mann, Southworth, Harding and Wesson2009b; Southworth and Mann, Reference Southworth and Mann2020). Since the 2010s, oyster densities throughout western tributaries of the Chesapeake Bay have increased (VOSARA: https://cmap22.vims.edu/VOSARA/). Estimates for b reported in the literature include values from South Carolina of 2.17 (Grizzle et al., Reference Grizzle, Greene and Coen2008) and 2.21 (Dame, Reference Dame1972), and values from Delaware Bay ranging from 1.7 to 2.4 (Powell et al., Reference Powell, Mann, Ashton-Alcox, Kim and Bushek2016). Prior work estimated shell production in the Chesapeake Bay using, in part, descriptors for the relationship between length and dry shell biomass (Mann et al., Reference Mann, Southworth, Wesson, Thomas, Tarnowski and Homer2022). We estimated the average b coefficient as 2.43 for length–dry shell weight relationships. Oysters living in the upper James produced less shell on average for a given size (lower b coefficient) relative to other reefs in the Virginia portion of the Chesapeake Bay, which is in agreement with differences in oyster growth patterns (tending towards globose vs elongate) among areas and observations from Mann et al. (Reference Mann, Southworth, Wesson, Thomas, Tarnowski and Homer2022). Despite highly variable growth patterns in oysters, the relationship between biomass and size is relatively constant across a wide spatial range and appears to be influenced by environmental conditions local to individual reefs.
Comparing condition indices for oysters across space is challenging. Many bivalves exhibit seasonal variation in body condition across the gametogenic cycle (Barber and Blake, Reference Barber and Blake1981; Ojea et al., Reference Ojea, Pazos, Martínez, Novoa, Sánchez and Abad2004; Moura et al., Reference Moura, Gaspar and Monteiro2008; Peharda, Reference Peharda2012; Gosling, Reference Gosling2015; Marquardt et al., Reference Marquardt, Clark, Maietta, Park and Ruttenberg2022). Sample collection may occur across wide temporal windows, which can be particularly problematic if it spans multiple seasons and therefore different stages of the gametogenic cycle (Powell et al., Reference Powell, Mann, Ashton-Alcox, Kim and Bushek2016). Many methods for condition indices are discussed in the literature (Mann, Reference Mann, Thorp and Gibbons1978; Crosby and Gale, Reference Crosby and Gale L1990; Rainier and Mann, Reference Rainier and Mann1992), where a ratio between tissue and shell is used as a proxy for environmental signals, to assess gametogenic cycles over time or compare ‘meat’ quality or nutritive state among populations. We observed disparities in length–biomass relationships among sites for both shell and tissue biomass, which comprises both components in a condition index calculation. Our results suggest that shell and tissue biomass can scale at different rates with size over small spatial scales within tributaries, which may bias condition index comparisons among sites. Sites may be physically close to one another, but still experience dramatically different local conditions that can drive changes in shell morphology. Future studies using condition indices should carefully consider seasonality among collections and variation in local conditions among sites.
Evolutionary trends
A modest proportion of Bivalvia occupy epifaunal habitats. Notable epifaunal groups found in temperate zones include the scallops (Pectinidae), mussels (Mytilidae), and oysters (Ostreidae). Scallops have a wide variety of lifestyles, from sessile, attached (e.g. Crassadoma gigantea) to active free swimming (e.g. Amusium spp.) species (Minchin, Reference Minchin2003; Alejandrino et al., Reference Alejandrino, Puslednik and Serb2011). Scallops have acute visual systems and all non-attached species have the ability to swim (Speiser and Johnsen, Reference Speiser and Johnsen2008; Serb et al., Reference Serb, Alejandrino, Otárola-Castillo and Adams2011; Palmer et al., Reference Palmer, Taylor, Brumfeld, Gur, Shemesh, Elad, Osherov, Oron, Weiner and Addadi2017). Swimming was facilitated by divergence from the typical bivalve morphology, including losing one adductor muscle, reducing the foot, and developing asymmetrical valve inflation. Scallop shell morphology changes over ontogeny (Márquez et al., Reference Márquez, Amoroso, Gowland Sainz and Van Der Molen2010); however, shell morphology is consistent within a species and is influenced by species behaviour (Serb et al., Reference Serb, Alejandrino, Otárola-Castillo and Adams2011). Mussel shells exhibit valve asymmetry, where the anterior adductor muscle is reduced, and the hinge and ligament are shifted anterior to create a wedge shape. Byssal threads, in combination with the wedged shell morphology, allow mussels to form dense, three-dimensional ‘mats’ or beds. Mussels are an important foundation species in temperate and polar littoral zones (Gosling, Reference Gosling2021). Mussel beds provide structural habitat for settlement and refugia for newly recruited juvenile mussels (Seed, Reference Seed and Bayne1976; McGrath et al., Reference McGrath, King and Gosling1988; Gosling, Reference Gosling2021). Atlantic blue mussels, Mytilus edulis and M. trossulus, were documented to produce more elongate, narrower shells in low salinity or other unfavourable conditions (Telesca et al., Reference Telesca, Michalek, Sanders, Peck, Thyrring and Harper2018); however, the intraspecific plasticity in shell morphology for scallop and mussel species is minimal when compared to oysters.
Oysters' intraspecific plasticity in shell morphology contributes to their success as reef builders in temperate systems. Oyster larvae preferentially cement themselves onto adult oysters (Bonar et al., Reference Bonar, Coon, Walch, Weiner and Fitt1990; Turner et al., Reference Turner, Zimmer-Faust, Palmer, Luckenbach and Pentchef1994; Tamburri et al., Reference Tamburri, Finelli, Wethey and Zimmer-Faust1996, Reference Tamburri, Luckenbach, Breitburg and Bonniwell2008). Juvenile oysters conform their shape to fit into available spaces on the reef, which provides protection during early post-settlement stages and ensures individuals are in close proximity to maximize fertilization success during mass spawning events. Our results suggest that oysters in the Virginia portion of the Chesapeake Bay exhibit allometric growth, where tissue and shell biomass scales closer to the square (b < 3). This more elongate growth form arguably relieves oysters from the terminal size constraints experienced by ovoid bivalve forms, as evidenced by old, large oysters in historic, prehistoric, and fossil records for C. virginica (De Broca, Reference De Broca1865; Rick et al., Reference Rick, Reeder-Myers, Hofman, Breitburg, Lockwood, Henkes, Kellogg, Lowery, Luckenbach, Mann, Ogburn, Southworth, Wah, Wesson and Hines2016; Kusnerik et al., Reference Kusnerik, Lockwood, Grant, Tyler and Schneider2018) and even larger Ostreid forms in the fossil record (Kirby, Reference Kirby2001, Harzhauser et al., Reference Harzhauser, Djuricic, Mandic, Neubauer, Zuschin and Pfeifer2016). During the Pleistocene, C. virginica is described as up to 259 mm shell length (umbo to ventral margin) and were substantially larger than the maximum length we observed in extant populations (172 mm; Table 1). Mortality in the old, large oyster size classes disproportionately contributes to the underlying reef structure (Powell and Stanton Jr, Reference Powell and Stanton1985; Mann and Powell, Reference Mann and Powell2007; Waldbusser et al., Reference Waldbusser, Powell and Mann2013; Powell et al., Reference Powell, Mann, Ashton-Alcox, Kim and Bushek2016). Oysters' gregarious settlement, rapid shell production, and individual longevity support the formation and maintenance of biogeomorphic reef structures in estuaries over decadal or longer time frames (Mann and Powell, Reference Mann and Powell2007; La Peyre et al., Reference La Peyre, Humphries, Casas and La Peyre2014; Mann et al., Reference Mann, Southworth, Wesson, Thomas, Tarnowski and Homer2022; Smith et al., Reference Smith, Lusk and Castorani2022).
Estuaries are geologically ephemeral features. Oysters occupied Atlantic estuaries, including the Chesapeake Bay, for at least 3 million years, and invaded newly formed estuarine habitat as sea level rose and fell (Smith et al., Reference Smith, Roach and Bruce2003; Hobbs, Reference Hobbs2004; Mann et al., Reference Mann, Harding and Southworth2009a; Rick et al., Reference Rick, Reeder-Myers, Hofman, Breitburg, Lockwood, Henkes, Kellogg, Lowery, Luckenbach, Mann, Ogburn, Southworth, Wah, Wesson and Hines2016; Lockwood and Mann, Reference Lockwood and Mann2019). During the Holocene, sea level rise was rapid and is thought to exceed 10 mm yr−1 in the Chesapeake Bay (Kennett, Reference Kennett1982; Bratton et al., Reference Bratton, Colman, Thieler and Seal2002; Hobbs, Reference Hobbs2004). Estuaries drain large coastal regions and may have high sedimentation rates. Sedimentation rates in the extant Chesapeake Bay are around 0.1–1.0 cm yr−1 (Cronin et al., Reference Cronin, Sanford, Langland, Willard and Saenger2003). Further, oyster reefs break down as a result of taphonomic processes, such as shell dissolution, breakage, and bioerosion (Powell et al., Reference Powell, Kraeuter and Ashton-Alcox2006; Waldbusser et al., Reference Waldbusser, Steenson and Green2011; Carroll et al., Reference Carroll, O'Shaughnessy, Diedrich and Finelli2015; Pace et al., Reference Pace, Poussard, Powell, Ashton-Alcox, Kuykendall, Solinger, Hemeon and Soniat2020). Oyster shell has high turnover rates and taphonomic losses can be up to or greater than 30% yr−1 (Pace et al., Reference Pace, Poussard, Powell, Ashton-Alcox, Kuykendall, Solinger, Hemeon and Soniat2020; Mann et al., Reference Mann, Southworth, Wesson, Thomas, Tarnowski and Homer2022). Reef persistence requires accretion rates exceeding sea level rise, sedimentation, and taphonomic losses. Over geologic timescales, oyster reefs have persisted through these challenging conditions; however, over the last century, oysters in the Chesapeake Bay were subjected to intensive overfishing and disease epizootics (Perkinsus marinus and Haplosporidium nelsonii), which decreased oyster abundance and individual longevity (Haskins and Andrews, Reference Haskins, Andrews and Fisher1988; Rothschild et al., Reference Rothschild, Ault, Goulletquer and Héral1994; Andrews, Reference Andrews1996). Despite this diversity of challenges, oysters' spatially variable allometry enabled them to maintain aggregative reef structures, which are central to their evolved life history strategy.
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0025315424001140.
Acknowledgements
We thank the Virginia Marine Resource Commission's Shellfish Management Division staff for their collaboration on the annual oyster stock assessment and help with sample collection. Thank you to Nathan Otto for assistance with sample processing. Thank you to Dr Hyman for constructive feedback on methods.
Data availability
Data will be made available on request.
Author contributions
Alexandria R Marquardt: conceptualization, methodology, investigation, formal analysis, writing – original draft. Melissa Southworth: conceptualization, methodology, investigation, writing – review and editing, project administration. Roger Mann: conceptualization, writing – review and editing, supervision.
Financial support
A. R. M. was supported by a Virginia Sea Grant Graduate Research Fellowship.
Competing interest
None.
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