Comparison of Crassostrea virginica Gmelin (Eastern
Oyster) Recruitment on Constructed Reefs and Adjacent
Natural Oyster Bars over Decadal Time Scales
Juliana M. Harding, Melissa J. Southworth, Roger Mann, and James A.Wesson
Northeastern Naturalist, Volume 19, Issue 4 (2012): 627–646
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2012 NORTHEASTERN NATURALIST 19(4):627–646
Comparison of Crassostrea virginica Gmelin (Eastern
Oyster) Recruitment on Constructed Reefs and Adjacent
Natural Oyster Bars over Decadal Time Scales
Juliana M. Harding1,2,*, Melissa J. Southworth1, Roger Mann1,
and James A.Wesson3
Abstract - Since 1993, oyster reef replenishment efforts in the Virginia portion of the
Chesapeake Bay have relied heavily on construction of oyster shell reefs with enhanced
vertical relief. We evaluated the performance of six reefs constructed in proximity to
natural subtidal oyster bars by comparing recruit densities (spat m-2, where spat are
young-of-the-year oysters with shell heights less than 50 mm) between habitats. Recruitment
was higher on the reefs than bars during the first 1–3 yr post-construction, usually
by at least an order of magnitude. Within 7 yr, recruitment was similar between reef-bar
pairs although both reefs and bars received additions of shell, live oysters, or both during
the study period. At decadal time scales, constructed oyster reefs did not show enhanced
recruitment relative to adjacent natural oyster bars. The rapid decline in reef recruitment
post-construction is likely related to three processes: (i) shell degradation by taphonomic
processes, (ii) biofouling that occludes the shell surface to recruitment, and (iii) inability
of extant oysters on the reef to produce new shell at a rate commensurate with losses to
(i) and (ii). There appears to be a requirement for continued replenishment activity to
maintain the shell base on these reefs, contrary to the dynamics of a healthy natural oyster
population. The similarity in recruitment between constructed reefs and natural bars at
decadal time scales suggests that subtidal shell plants or shell additions to natural bars
may be a more cost-effective repletion strategy because they provide equal population
enhancement per unit area.
Introduction
Crassostrea virginica Gmelin (Eastern Oyster) reefs were a dominant habitat
in the Chesapeake Bay prior to European colonization (e.g., Hargis 1999,
Newell 1988). The extensive reef fields that developed in the lower Chesapeake
Bay during the Holocene epoch included fringing reefs as well as large
intertidal three-dimensional reefs that were navigation hazards (Hargis 1999,
Smith et al. 2003). The combination of post-colonization harvest pressure and
environmental degradation drastically reduced oyster populations from their
original spatial footprint and vertical extent such that by the 1890s the Commonwealth
of Virginia commissioned Lt. J.B. Baylor to survey the remaining
oyster resources (Baylor 1896). The decline in Virginia oyster populations continued
through the 20th century (Andrews 1996, Haven et al. 1978, Rothschild
1Department of Fisheries Science, Virginia Institute of Marine Science, College of William
& Mary, Gloucester Point, VA 23062. 2Current address - Department of Marine
Science, Coastal Carolina University, PO Box 261954, Conway, SC 29528. 3Virginia
Marine Resources Commission, 2600 Washington Avenue, Newport News, VA 23607-
0756. *Corresponding author - jharding@coastal.edu.
628 Northeastern Naturalist Vol. 19, No. 4
et al. 1994) and was exacerbated by the introduction of Haplosporidium nelsoni
Haskin, Stauber, and Mackin (MSX; Andrews 1968, Andrews and Wood 1967,
Burreson et al. 2000) and environmental conditions in the 1980s that intensified
Perkinsus marinus Mackin, Owen, and Collier (Dermo; Andrews 1996, Burreson
and Ragone Calvo 1996). These diseases affect oysters in their second or
third years and may increase the observed mortality of older oysters depending
on site- and year-specific ambient environmental conditions (Andrews 1968,
Burreson and Ragone Calvo 1996, Carnegie and Burreson 2011, Harding et al.
2010a, Mann et al. 2009a, Southworth et al. 2010). Neither disease directly impacts
oysters within the first year post-settlement (recruits).
Natural subtidal oyster reef structures have a veneer of live oysters approximately
10 to 30 cm thick overlaying the reef core (DeAlteris 1988, Hargis 1999).
The filling of the interstitial spaces or matrix in a natural reef is a gradual process
that results from natural shell degradation and biodeposition. On a living reef,
this infilling is balanced with reef accretion through growth of individuals and
natural recruitment such that the living oyster layer expands outward over time
(Hargis 1999, Powell and Klinck 2007).
The destruction of biogenic reef shell habitat is concurrent with the loss
of the biological and ecological services provided by living oysters (Beck et
al. 2011; Mann and Powell 2007; Mann et al. 2009a; Powell et al. 2009a, b;
Woods et al. 2005). Oyster shell half life is typically on the order of 3–6 yr in
mid-Atlantic estuaries (Powell et al. 2006); thus, natural accretion rates for
equilibrium or growing reef systems must match or exceed rates of shell degradation
combined with sea-level rise (Mann et al. 2009a, Powell and Klinck
2007). Extant Virginia oyster population demographics have been truncated by
disease and environmental conditions such that 3–4 yr olds are rare (Harding et
al. 2010a; Mann et al. 2009a, b; Southworth et al. 2010), and the existing shell
base lacks the fundamental contribution originally made by larger, older individuals
(DeAlteris 1988, Mann et al. 2009b). Annual variability in recruitment
or replacement ratios (Harding et al. 2010a, Mann et al. 2009a, Southworth
et al. 2010) also skews oyster population demographics within Virginia traptype
estuaries like the Piankatank and Great Wicomico rivers (Andrews 1979).
Even within trap-type estuaries where hydrodynamics facilitate recruitment,
defensible stock-recruit relationships based on long-term (>10 yr) data sets are
absent (Harding et al. 2010a, Southworth et al. 2010) and indicative of the wide
interannual fluctuations in natural recruitment that have been observed since at
least the 1930s (e.g., Galtsoff et al. 1947). Natural oyster reef development and
maintenance (= accretion) require longer time frames, broad population demographics,
and relatively high replacement ratios (Harding et al. 2010a; Mann et
al. 2009a; Powell et al. 2009a, b; Southworth et al. 2010).
The Commonwealth of Virginia has included construction of three-dimensional
oyster shell sanctuary reef as part of its long-term oyster resource
rehabilitation and fishery management program since the early 1990s. The
term “reef” is used here in reference to a shell-based structure with vertical
relief, while the term “bar” is used to refer to a shell-based structure that is
2012 J.M. Harding, M.J. Southworth, R. Mann, and J.A.Wesson 629
subtidal with limited, if any, vertical relief. Since construction of Palace Bar
reef in the Piankatank River (Fig. 1) in 1993 (Bartol and Mann 1997), more
than 50 similar reef structures have been built in the Virginia portion of the
Chesapeake Bay. The resulting reefs were intended to mimic the original,
natural reefs that developed on hard substrate during the Holocene epoch (e.g.,
DeAlteris 1988, Hargis 1999, Smith et al. 2003) and restore relief or replace
Figure 1. Map of the Virginia portion of the Chesapeake Bay showing the reef and bar
locations studied in the Great Wicomico (A) and Piankatank (B) rivers. Site abbreviations
are as follows: CC = Crane’s Creek bar, CCR = Crane’s Creek reef, SB = Shell Bar, SBR
= Shell Bar reef; Bl = Bland Point bar; BlR = Bland Point reef, Bu = Burton Point bar
(equal to Burton Point 1 in Harding et.al. [2010a]), BuR = Burton Point reef, CT = Cape
Toon bar, CTR = Cape Toon reef, PB = Palace Bar, PBR = Palace Bar reef, V = VIMS
oyster pier.
630 Northeastern Naturalist Vol. 19, No. 4
reefs that have been reduced or destroyed by a combination of environmental
and anthropogenic factors (Hargis and Haven 1999, Wesson et al. 1999).
The stated goals for Virginia’s oyster reef construction program include the
establishment of self-sustaining oyster populations on the constructed reefs.
Regular recruitment is a requirement for self-sustaining oyster populations.
Oyster reef restoration efforts have often been examined in the context of the
resulting ecological services (e.g., Breitburg 1999; Coen and Luckenbach 2000;
Coen et al. 1999, 2007; Kennedy 1996; Peterson et.al. 2003). Reef construction
is usually described as “restoration”, but these projects are rarely evaluated
quantitatively in terms of subsequent sustainability and biogenic carbonate production.
Live oyster density, biomass, and/or demographics (e.g., Luckenbach et
al. 2005, Powers et al. 2009) have been proposed as metrics of restoration success.
While these are certainly relevant criteria, they do not directly address the
maintenance and growth of biogenic shell habitat with time that is fundamental
to the persistence of self-sustaining reef structures across multiple years (Mann
and Powell 2007). Constructed three-dimensional sanctuary reefs are essentially
thick (>50 cm) intertidal shell plants or shell layers spread evenly over the target
bottom (Haven et al. 1978, Kennedy and Sanford 1999). Over time, the composite
shells are redistributed by wave action or settle or subside, resulting in
subtidal structures in the absence of continued shell addition by either natural or
artificial processes. In addition to leveling out, spaces between the shells fill with
biodeposits, sediment, and other materials including shell fragments (Abbe 1988,
O’Beirn et al. 2000, Powell et al. 2006).
Oyster shell is a limiting resource for modern Virginia oyster replenishment
and management programs (Hargis and Haven 1999, Wesson et al. 1999). If there
are no differences in oyster recruitment between three-dimensional constructed
reefs and two-dimensional natural bars, then the limited shell resource may be
more cost effectively used to cover larger spatial areas as shell plants. Shell
plants 20–30 cm thick are a proven strategy to encourage and sustain oyster recruitment
in the Chesapeake Bay (Abbe 1988; Harding et al. 2010a; Hargis and
Haven 1999; Haven et al. 1978, 1981; Mann et al. 2009b; Southworth et al. 2010)
as well as other estuaries (Kennedy and Sanford 1999, Moore 1897).
Natural subtidal oyster bars adjacent to constructed reefs provide a baseline
from which to evaluate the performance of constructed reefs with regard
to recruitment. Six oyster reefs built in Virginia between 1993 and 1998 are in
proximity to natural oyster bars (Fig. 1). Annual estimates of oyster spat density,
a descriptor of recruitment success, are available for both reefs and bars from
reef construction through 2006, including at least 9 yr of data for each reef-bar
pair. Evaluation of recruitment trends must include multi-year time scales that are
long enough to encompass oyster life-span (3–6 yr; Harding et al. 2010, Powell
and Cummings 1985, Southworth et al. 2010), oyster generation time (≈1 yr;
Harding et al., in press), and shell half-life (3–6 yr; Harding et al. 2010a, Powell
and Klink 2007, Southworth et al. 2010) within these rivers.
We compared spat densities (number of spat m-2) between 6 constructed threedimensional
reefs and adjacent natural two-dimensional bars to quantitatively
2012 J.M. Harding, M.J. Southworth, R. Mann, and J.A.Wesson 631
test the hypothesis that three-dimensional constructed reef structures have enhanced
recruitment (higher spat densities) relative to natural oyster bars over
multi-year time scales. We pose this hypothesis to test the assumption that observed
recruitment trends at a location are driven by substrate availability rather
than larval supply. Recruitment trends within each of these rivers are widely
variable from year to year (Harding et al. 2010a, Haven et al. 1978, Southworth
et al. 2010). Given that the reef-bar pairs are in proximity, the point is to compare
the 2 habitat types (constructed 3D vs. natural 2D) as recruitment habitat. If both
provide similar recruitment (spat density) signals, then both are an equally good
use of shell resource. If one habitat provides a signal that shows higher recruitment
in terms of annual numbers, long-term consistency or both, then the use of
that habitat is a better investment.
Materials and Methods
Study sites
The Piankatank and Great Wicomico rivers (Fig. 1, Table 1) were chosen as
sites for three-dimensional reef construction because of their history as trap-type
estuaries (Andrews 1979) and seed-production rivers (Hargis and Haven 1988,
Haven and Whitcomb 1986, Haven et al. 1978). By design, reef-construction
sites were located on the geologic footprints of natural oyster reefs delineated
by the Baylor survey (1896) and adjacent to public oyster grounds resurveyed
by Haven et al. (1981; also Haven and Whitcomb 1986). These natural bars have
been actively managed by the Virginia Marine Resources Commission (VMRC)
since at least 1963 (Haven et al. 1981). The reef/bar names used herein match the
historic names used by Baylor (1896) and Haven et al. (1981).
A total of 4 reefs were built in the Piankatank River between 1993 and 1995
(Fig. 1, Table 1): Palace Bar Reef (June 1993, reef footprint = 8.1 x 103 m2) and
Bland Point Reef, Cape Toon Reef, and Burton Point Reef (all June 1995, 4.05
x 103 m2 each). Subsequently, 2 reefs were built in the Great Wicomico River
(Fig. 1, Table 1): Shell Bar Reef (summer 1996, 8.1 x 103 m2) and Crane’s Creek
Table 1. Summary of site-specific information for the constructed reef-natural bar pairs examined in
the Great Wicomico River and Piankatank River, VA. Details for site-specific replenishment measures
are provided in text. Yr RC = year of 3D reef construction. Areas are reported as m2. Burton
Point bar is equal to Burton Point 1 in Harding et al. (2010a).
Reef Bar
River/site Yr RC abbreviation Reef area abbreviation Bar area
Great Wicomico
Crane’s Creek 1998 CCR 8.10 x 103 CC 5.08 x 104
Shell Bar 1996 SBR 8.10 x 103 SB 7.16 x 104
Piankatank
Bland Point 1995 BlR 4.05 x 103 Bl 1.01 x 105
Burton Point 1995 BuR 4.05 x 103 Bu 1.58 x 105
Cape Toon 1995 CTR 4.05 x 103 CT 1.68 x 105
Palace Bar 1993 PBR 8.10 x 103 PB 1.66 x 105
632 Northeastern Naturalist Vol. 19, No. 4
Reef (summer 1998, 8.1 x 103 m2). All reefs were built at water depths of ≈3 m
with reef shells extending from the substrate through the water column to the airwater
interface.
Each constructed reef was located within 1 km of a natural two-dimensional
oyster bar that supported a self-sustaining oyster population throughout the time
period examined (Piankatank bars: Harding et al. 2010a; Great Wicomico bars:
Southworth et al. 2010). Note that Burton Point bar in the Piankatank River referenced
here corresponds to the bar referred to as Burton Point 1 in Harding et
al. (2010a). Natural bars varied in size from 5.08 x 104 to 1.68 x 105 m2 (Table 1).
Maximum water depths over the subtidal natural bars were also ≈ 3 m.
Oyster and/or shell resources on constructed three-dimensional reefs and
natural bars were supplemented periodically from 1993 through 2006 (Table 2).
Repletion activities included additions of wild broodstock oysters, cultured individual
oysters (hereafter cultchless oysters), clean oyster shell, and/or shell to
which cultured oysters have been allowed to metamorphose in high density via
remote setting (hereafter spat on shell).
Temperature and salinity data
Hydrographic conditions at Palace Bar reef (Fig. 1) and Shell Bar reef (Fig. 1)
are representative of ambient hydrographic conditions at the natural bars and
constructed reefs examined in the Piankatank and Great Wicomico rivers, respectively
(Harding et al. 2010a, Southworth et al. 2010). Weekly water temperature
and salinity data were calculated from bottom-water temperature (ºC) and salinity
data recorded by automated monitoring stations (15-minute intervals) on Palace
Bar reef (Piankatank River) and Shell Bar reef (Great Wicomico River) from June
Table 2. Summary of replenishment activity on natural bars (B) and constructed reefs (R) including
shell planting (SP), addition of wild broodstock or cultchless oysters (Oy), and addition of
spat-on-shell (SOS). “C” indicates the year of construction for reefs. * indicate years prior to reef
construction. - indicates years in which no replenishment activity occurred.
Site
Crane’s Creek Shell Bar Bland Point Burton Point Cape Toon Palace Bar
Year B R B R B R B R B R B R
1993 * * * * * * * * * * - C
1994 * * * * * * * * * * - -
1995 * * * * - C - C - C - -
1996 * * - C,Oy - - - - - - - -
1997 * * SP Oy - - - - - - - Oy
1998 - C, Oy SP Oy SP - - - - - SP Oy
1999 SP - SP Oy SP Oy SP Oy - Oy SP Oy
2000 - - - Oy SP Oy SP Oy - Oy SP Oy
2001 - - - Oy SP - - - - - SP Oy
2002 - Oy - Oy - - - Oy - - - Oy
2003 - SP Oy SP - - - - - - -
2004 - Oy SP Oy SP Oy - - - Oy SP -
2005 - - SP Oy - SOS SP - - - SP -
2006 - - SP Oy - Oy, SOS SP - - - - SOS
2012 J.M. Harding, M.J. Southworth, R. Mann, and J.A.Wesson 633
2005 through December 2006. Average weekly water temperatures and salinities
at both reefs prior to 2005 were predicted using measured temperatures and
salinities from a similar station deployed in the York River (Fig. 1, Gloucester
Point VA, 37º14'47"N, -76º30'23"W, VIMS Data archive) with linear regressions
from Southworth et al. (2010, Shell Bar reef) and Harding et al. (2010a, Palace
Bar reef).
Predicted measurements were supplemented with water temperature and
salinity data collected weekly at reefs and bars (n > 3) from June through September
(Piankatank: 1993–2006, Great Wicomico: 1998–2006). From 1993–2004,
water samples were collected approximately 0.5 m off the bottom. Temperature
was measured with an alcohol thermometer within 5 minutes of water-sample
collection and salinity was measured with a hand-held refractometer. Beginning
in 2005, water temperature and salinity were measured with a hand-held digital
probe suspended 0.5 m from the bottom.
Oyster spat surveys
Natural recruitment on natural oyster bars was surveyed each fall (November,
1995–2006) following the methods described by Mann et al. (2009a,
James River), Southworth et al. (2010, Great Wicomico River), and Harding
et al. (2010a, Piankatank River). Oysters were collected from the R/V J.B.
Baylor with a hydraulic patent tong using a random sampling design. The open
dimensions of the tong were such that it sampled one square meter of bottom
to a depth of 30 to 50 cm through the oxic or taphonmically active layer
(Davies et al. 1989). Upon retrieval of each sample (= patent tong grab; n >
7 bar-1 yr-1), the longest dimension from the hinge to the growth margin was
measured (shell height [SH] in mm) for all oysters. Oysters <50 mm SH were
subsequently categorized as spat. Thus, we define an oyster spat as a youngof-
the-year animal that has a maximum dimension from hinge to growth
edge of less than 50 mm (shell height) and does not have a cupped left valve.
Standardized quantitative surveys were not conducted prior to 1995 on either
natural bars or constructed sanctuary reefs.
Beginning in September 1995, natural spat densities (number m-2) on constructed
reefs were determined using an annual dive survey. Divers randomly
placed a 0.25-m2 quadrat on the reef surface and then removed all material
(live oysters and oyster shell) within the quadrat to a depth of at least 30 cm.
All material was subsequently examined on board the survey vessel, and live
spat were enumerated for each quadrat sample (n > 6 reef-1 yr-1). The number
of spat observed per 0.25-m2 sample were multiplied by 4 to yield spat densities
m-2.
Data analyses
Annual spat densities (number m-2) were compared for each constructed reefnatural
bar pair using reef-bar pair and year-specific two-tailed non-parametric
Mann-Whitney U tests. Mann-Whitney U tests were used because the data were
not normally distributed and included large ranges of observed spat densities.
Significance levels were established at alpha = 0.05 a priori.
634 Northeastern Naturalist Vol. 19, No. 4
Within a site, the average annual change in observed spat density was calculated
by taking the average of spat densities within year 1 and subtracting the
average density in year 1 from the average density in year 2 and so on. Differences
in average annual changes in spat density between reef-bar pairs were also
evaluated with Mann-Whitney U tests for consecutive years in which there were
data available for both reefs and bars.
Results
Temperature and salinity data
Water temperatures in the Piankatank and Great Wicomico rivers followed
similar trends from 1993–2006 (Fig. 2) with observed seasonal minima of ≈0–4
°C and maxima of 28–30 °C. Great Wicomico water temperatures measured during
July and August were 1–2 °C warmer than Piankatank water temperatures
in 2000, 2001, 2003, and 2004. The summers of 1996 and 1997 were relatively
cooler than other years.
Salinities in both rivers were generally 8–20 psu (Fig. 3). Observed minima
(5–10 psu) generally occurred during the late winter/early spring wet period.
Observed salinity maxima (18–26 psu) corresponded to lower rainfall conditions
Figure 2. Weekly average water temperature (°C) in the Piankatank and Great Wicomico
rivers from 1993 through 2006. Predicted values from 1993 through May 2005 were
estimated from York River (V in Fig. 1) measurements using Harding et al. (2010a) and
Southworth et al. (2010), respectively, as described in text. Year-round measurements at
Shell Bar and Palace Bar reefs are available from June 2005 through December 2006.
Measured values during May through September of 1993 through 2006 are averages from
a minimum of 3 bars within each system.
2012 J.M. Harding, M.J. Southworth, R. Mann, and J.A.Wesson 635
typically observed during late summer and fall in the Chesapeake region. Salinities
measured during summer and fall of 1999 and 2002 were higher than
predicted but similar between rivers. Relatively low salinities were observed
during summer and fall of 1996 and 2004.
Spat density
Oyster spat densities on the reefs and bars have been described with quantitative
surveys since 1995. Annual fall surveys on both reefs and bars provide
quantitative estimates of recruitment for each habitat type. Patent tong survey
data were not available for any Piankatank River bars in 1997 and for Burton
Point Bar and Cape Toon Bar in 1999.
Oyster recruitment onto constructed reefs was high during the reproductive
season immediately following reef construction (Fig. 4). The highest recruitment
observed throughout the study at Crane’s Creek Reef and Shell Bar Reef occurred
immediately after the reefs were built (Fig. 4). A strong recruitment signal was
also evident on the three Piankatank reefs built in June 1995 (Bland, Burton,
Cape Toon) when they were surveyed in September 1995 (Fig. 4). The initial
recruitment event was not sustained at any of these reefs during the second year
Figure 3. Weekly average salinities in the Piankatank and Great Wicomico rivers from
1993 through 2006. Predicted values from 1993 through May 2005 were estimated from
York River (V in Fig.1) measurements using Harding et al. (2010a) and Southworth et
al. (2010), respectively, as described in text. Year-round measurements at Shell Bar and
Palace Bar reefs are available from June 2005 through December 2006. Measured values
during May through September of 1993 through 2006 are averages from a minimum of
3 bars within each system.
636 Northeastern Naturalist Vol. 19, No. 4
post-construction. Spat densities on constructed reefs were significantly higher
than spat densities on adjacent natural bars during the first 1 to 6 yrs post construction
for these 5 reef-bar pairs (all but Palace Bar; Fig. 4, Table 3). By 6–7
yr post reef construction, observed spat densities on the constructed reefs were
not significantly different than those recorded on adjacent natural bars. The recruitment
observed on Shell Bar, Bland Point, and Cape Toon reefs during 2006,
after the addition of large numbers of broodstock oysters to each of these sites
(Table 2, Fig. 4), is the exception to this trend (Table 3).
River and year-specific variations in recruitment are evident in the observed
patterns of recruitment on both bars and reefs. Recruitment in both the Great
Wicomico and Piankatank Rivers was unusually high during 2002 (Harding et al.
2010a; Southworth et al. 2003, 2010) and the strength of this year class was evident
at all reefs and bars (Fig. 4). Recruitment onto natural bars in the Piankatank
River during 2002 was the highest observed between 1995 and 2006 for Bland
Point, Burton Point, and Cape Toon bars (Fig. 4C, D, E) and the second highest
bar recruitment for Palace Bar (Fig. 4F). Recruitment on the natural oyster
bar at the Palace Bar site was highest during 1999 (Fig. 4F) commensurate with
Figure 4. Average spat density (m-2, standard deviation) for each reef-bar pair by year
from reef construction (RC) through 2006. Crane’s Creek (A) and Shell Bar (B) are in the
Great Wicomico River. Bland Point (C), Burton Point (D), Cape Toon (E), and Palace Bar
(F) are in the Piankatank River. No data (ND) were available for Palace Bar or Palace Bar
reef (F) in 1993 and 1994, all of the natural bars in the Piankatank River during 1997, and
Burton Point (D) and Cape Toon (E) bars in 1999. Years in which replenishment activities
on reefs were completed are indicated by shaded rectangles.
2012 J.M. Harding, M.J. Southworth, R. Mann, and J.A.Wesson 637
another strong recruitment signal throughout the Piankatank system (Harding et
al. 2010a). In the Great Wicomico River, the highest observed recruitment for
the two natural bars (Crane’s Creek Bar and Shell Bar) was in 2006 (Fig. 4A, B).
Recruitment was relatively high throughout the Great Wicomico River in 2006
(Southworth et al. 2007, 2010).
After initial construction, all of the reef-bar combinations examined received
at least one addition of clean shell and/or live oysters to the bar, the
reef, or both within the same year during the 8–9 year study period (Table 2,
Fig. 4). However, repletion activity was not always followed by an increase
in site-specific recruitment within the same year (Figs. 4, 5). The Palace Bar
(Piankatank) and Shell Bar (Great Wicomico) reef-bar pairs serve as good
examples. The reefs at each site are two of the earliest reefs built and have received
regular replenishment since construction. The adjacent bars have also
received regular repletion during the study period (Table 2; also Harding et al.
2010a, Southworth et al. 2010). When repletion activity coincided with years
of system-wide high recruitment (1999, 2002, 2006 as discussed above), the
replenished sites showed an increase in observed recruitment relative to the
previous year (Figs. 4, 5). During years when system-wide recruitment was not
high, recruitment levels at replenished sites were approximately the same or
less (Fig. 5) than those observed in the previous year. Decreases in recruitment
observed on Palace Bar in 2000 and 2001 after replenishment were lower in
magnitude than those observed on Palace Bar reef (Fig. 5).
Oyster recruitment onto constructed reefs should at least be equal to recruitment
observed on the adjacent natural bar within the same year (1:1 relationship,
diagonal dashed line in all Fig. 6 panels). If reefs receive higher recruitment
than bars, the data points will all be above the 1:1 line. If bars receive higher
Table 3. Summary of P values resulting from year- and site-specific Mann-Whitney U tests comparing
constructed reefs (R) with adjacent natural bars (B). No data = no data available from either
reef or bar. ns = not significant. R > B or B > R = bar or reef data all zero while the other site was
non zero. NC = no comparison because data from both reef and bar were all 0.
Site
Year Crane’s Creek Shell Bar Bland Point Burton Point Cape Toon Palace Bar
1993 No data
1994 No data
1995 R > B R > B R > B R > B
1996 No data <0.01 <0.01 <0.01 <0.01
1997 <0.01 No data No data No data No data
1998 <0.01 <0.01 <0.01 <0.01 <0.01 <0.01
1999 <0.01 <0.01 <0.01 No data No data ns
2000 ns ns ns <0.01 <0.01 <0.01
2001 0.02 ns <0.01 <0.01 <0.01 ns
2002 <0.01 ns 0.01 <0.01 <0.01 ns
2003 0.05 ns ns NC B > R B > R
2004 R > B ns ns R > B NC B > R
2005 ns ns ns ns ns B > R
2006 ns 0.03 <0.01 ns <0.01 ns
638 Northeastern Naturalist Vol. 19, No. 4
recruitment than the reefs, data points will all be below the 1:1 line. If oyster populations
receive regular recruitment, data points should either stay approximately
equal or increase moving forward in time. Examination of natural recruitment
onto reef-bar pairs for the decade post-reef construction reveals several trends.
None of the reefs show either a stable number of recruits or a regular increase
in recruitment from the year of construction forward (Fig. 6). Reef and bar spat
densities vary from year to year regardless of repletion and river. Even with additions
of shell, live oysters, or both to all reefs and bars, the spat densities on
constructed reefs in 2006 are less than the spat densities observed in the year of
construction and are within the same order of magnitude as spat densities on the
adjacent bars (all reefs but Palace Bar; Fig. 6).
Figure 5. Trends in spat density and repletion activity in one year with regard to the
observed spat density in the previous year where no repletion occurred for Palace
Bar and Palace Bar reef (Piankatank River) and Shell Bar and Shell Bar reef (Great
Wicomico River).
Figure 6 (opposite page). Comparison of average spat density (SE, standard error)
on natural bars with adjacent constructed reefs for Crane’s Creek (A), Shell Bar (B),
Bland Point (C), Burton Point (D), Cape Toon (E), and Palace Bar (F). The diagonal
line indicates the location where bar and reef spat densities are equal (1:1 relationship).
Observed densities of zero oysters were changed to densities of 0.001 oysters to allow
presentation on a logarithm scale. Data points in years where bars and reefs, bars only,
and reefs only received repletion are indicated by a black-bordered rectangle, a dark
grey rectangle, or a light grey rectangle, respectively. Arrows indicate the passage of
time from one year to the next.
2012 J.M. Harding, M.J. Southworth, R. Mann, and J.A.Wesson 639
At multi-year time scales, annual changes in spat density between reef-bar
pairs were not significantly different (Mann-Whitney U: P > 0.05) indicating the
reefs did not provide enhanced settlement habitat relative to the bars, and that
larval supply rather than substrate limitation drives the observed recruitment
trends within these rivers.
640 Northeastern Naturalist Vol. 19, No. 4
Discussion
At decadal time scales, constructed oyster reefs did not show enhanced recruitment
relative to adjacent natural oyster bars. Recruitment on the constructed
reefs was enhanced relative to the bars in the years immediately following reef
construction and immediately following addition of supplemental shell or oysters
as a repletion strategy. However, in the absence of continued addition of shell
and/or live oysters, spat densities on constructed reefs declined until they were
equivalent to spat densities observed on natural oyster bars that did not receive
shell. The time course for the observed decline in reef recruitment was 1–7 yr
post-reef construction. This time frame is approximately equal to the oyster shell
half-life of 3–6 yr reported by Powell et al. (2006) and commensurate with the
modern life span (2–3 yr) of oysters within these rivers (Harding et al. 2010a,
Southworth et al. 2010).
The observed decline in recruitment onto constructed reefs likely corresponds
to the condition of the shell resource. Immediately after construction, the clean
shell provides available habitat for oysters as well as other epibenthic taxa
including barnacles, bryozoans, and macroalgae (Luckenbach et al. 2005, Rheinhardt
and Mann 1990). The timing of reef construction and shell planting with
regard to the timing of oyster recruitment within the system is important. If clean
shell is planted after the peak of oyster recruitment within a system, the shell will
be colonized by other taxa. Oyster settlement in subsequent years may be limited
by the availability of suitable substrate.
Oyster shells are degraded through physical and biological processes. In a
natural reef, living oysters maintain their shells and thus the interstitial reef matrix,
and increase the available shell surface area through individual growth. When an
oyster dies, its shell begins to erode through chemical and mechanical processes.
Cliona spp. (boring sponges) have been regularly observed at all six of the sites
studied (reefs and bars) since 1995. On constructed reefs, when shells are deployed
as single valves rather than incorporated into a heterogenous matrix, valves may be
rolled or moved by waves and mobile fauna, hastening the mechanical breakdown
of the shell. Pieces that have broken off shells combine with biodeposits within the
interstitial spaces of the reef matrix (DeAlteris 1988). In a living oyster reef, reef
accretion or expansion of the growth edges into the water column is greater than
the infilling or biofouling of the interstitial shell matrix maintaining or increasing
the availability of interstitial habitat. Interstial spaces may fill quickly in constructed
shell habitats as planted shells erode, subside, and compact (Abbe 1988,
Nestlerode et al. 2007, O’Beirn et al. 2000). If the reef interstitial matrix has filled,
only substrate on the exterior of the reef is available as recruitment habitat, drastically
reducing the available settlement surface and increasing the risk of predation
(Bartol and Mann 1999, Bartol et al. 1999).
The Great Wicomico and Piankatank rivers have a history of regular recruitment,
and both of these rivers have been described as substrate limited
rather than recruit limited since at least 1963 (Harding et al. 2010a, Haven
et al. 1978, Southworth et al. 2010), although Galtsoff et al. (1947) describe
2012 J.M. Harding, M.J. Southworth, R. Mann, and J.A.Wesson 641
substrate limitation in the Piankatank River during the 1930s. The initial positive
effects of the constructed reef habitats were reduced as the initial shell
plants aged in the absence of sustained recruitment and the development of
resident oyster populations with a multi-year demographic that enhances
interstitial habitat. The observed 1–7-year time course for the decay of the recruitment
signal post reef construction is also related to the life expectancy of
oysters within these rivers. In general, the age structure of the oysters within
these rivers is truncated by the diseases Dermo and/or MSX. Oysters greater
than 3 years old are rare in both systems (Harding et al. 2010a, Southworth et
al. 2010). Thus, oysters from recruitment events within 1–2 yr of shell planting
grew, maintained the shell base, and then died. Occlusion and degradation
of their shells after death resulted in poor substrate condition in the absence of
continued recruitment or replenishment.
Recruitment variability between years further compounds the living oysteroyster
shell dynamic. While oyster generation time in these rivers is as little as
1 yr, the observed interannual recruitment variability within these systems often
spans at least an order of magnitude (Galtsoff et al. 1947, Harding et al. 2010a,
Haven et al. 1978, Southworth et al. 2010). If shells are planted or added in a year
of poor recruitment, the shells will degrade prior to oyster settlement, although
there is no guarantee that a low recruitment year will be followed by a year
of high recruitment. Since spat recruit to shell, the lack of multiple successful
recruitment events to a shell plant within the 1–7-year window will result in a
decrease in available habitat as the shell base degrades. Substrate availability is
a dynamic process whereby it is gained through recruitment, growth, and replenishment,
but lost through mortality, occlusion, and degradation.
The reduction in larger, older oysters observed within these populations (Harding
et al. 2010a, Southworth et al. 2010) reduces habitat heterogeneity (Paynter et
al. 2010, Powell et al. 2006) and the availability of healthy oyster growth edges
that may enhance settlement. The presence of very large broodstock oysters on
Shell Bar Reef in 1997 (Southworth and Mann 1998) may have contributed to
the intense recruitment event observed during 1997, which remains the highest
observed recruitment event observed at that reef to date. The contribution of
larger, older oysters to the reef shell surface layer, interstitial matrix, and base is
fundamental to habitat stability over time and the continued reef accretion process
(Mann et al. 2009b, Powell and Klinck 2007).
There appears to be a requirement for continued replenishment activity to
maintain the habitat heterogeneity of the shell surface on these constructed
reefs, contrary to the dynamics of a healthy natural oyster population. While
the reefs and resident oysters provide ecosystem services (Beck et al. 2011,
Coen and Luckenbach 2000, Coen et al. 2007) for a variety of associated species
(e.g., Breitburg 1999; Coen et al. 1999; Harding and Mann 1999, 2001,
2003, 2010; Harding et al. 2010b; Wenner et al. 1996), these constructed reefs
do not provide enhanced habitat for oysters over the long term relative to existing
natural bars. Given the large volume of shell required to build each reef
642 Northeastern Naturalist Vol. 19, No. 4
and the current paucity of shell available for oyster repletion and habitat rehabilitation,
these data support as the most cost effective use of shell continued
two-dimensional oyster shell planting in Virginia with coverage on the order of
the traditional range of 5,000–10,000 bu acre-1 (Haven et al. 1978) or approximately
20 L m-2 (Harding et al. 2010a, Mann et al. 2009a) rather than creation
of additional intertidal constructed reefs. Such shell planting would increase
the spatial footprint for oyster habitat rehabilitation well beyond that possible
if three-dimensional reefs were built. The effectiveness of shell planting as an
oyster replenishment strategy may be further enhanced when planting is followed
by deployment of spat-on-shell, given the potential for spat-on-shell to
increase habitat complexity akin to a natural living reef matrix (e.g., O’Beirn et
al. 2000, Rodney and Paynter 2006).
Acknowledgments
This research was supported by funds from the Commonwealth of Virginia to the
Virginia Institute of Marine Science and the Virginia Marine Resources Commission.
We thank the many individuals who assisted in field work, especially the late Reinaldo
Morales-Alamo, Kenneth Walker, Ian Bartol, Richard Takacs, Alan Godshall, Vernon
Rowe, John Ericson, Adam Crockett, and Erin Reilly. Todd Nelson designed the hydrographic
monitoring stations and assisted with station deployment and maintenance. This
is Contribution Number 3228 from the School of Marine Science, Virginia Institute of
Marine Science.
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