Benthic organic enrichment from suspended mussel (Mytilus edulis) culture in Prince Edward Island, Canada

Aquaculture 292 (2009) 189–196

Contents lists available at ScienceDirect

Aquaculture j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / a q u a - o n l i n e

Benthic organic enrichment from suspended mussel (Mytilus edulis) culture in Prince Edward Island, Canada P.J. Cranford ⁎, B.T. Hargrave, L.I. Doucette Ecosystem Research Division, Department of Fisheries and Oceans, Bedford Institute of Oceanography, Dartmouth, Nova Scotia, Canada B2Y 4A2

a r t i c l e

i n f o

Article history: Received 12 February 2008 Received in revised form 22 April 2009 Accepted 23 April 2009 Keywords: Shellfish culture Biodeposits Benthic impacts Sulfide Redox

a b s t r a c t The effects of increased biodeposition within mussel (Mytilus edulis) farms on the benthic environment were investigated using surface sediment samples collected from 11 coastal embayments in Prince Edward Island (PEI), Canada. The degree of organic enrichment, determined using geochemical indicators (total free sulfides (S), redox potentials (EhNHE), water content (WC) and organic matter (OM)), was significantly greater in mussel leases compared to reference sites located both outside lease boundaries and in inlets not used to culture mussel (MANOVA, p b 0.001). Post-hoc tests showed that mean WC and OM, EhNHE potentials and S concentration were all significantly different between lease and reference sites (p ≤ 0.009). Temporal changes in organic enrichment conditions were detected by comparing our 2001 data to those previously reported from a 1997 survey of the same sampling sites (MANOVA, p b 0.001). This multivariate effect resulted primarily from a 39% increase in mean S concentration between 1997 and 2001 (p = 0.029). Surface sediment variables at reference sites were similar between years. Benthic conditions were discriminated along an oxic–anoxic enrichment gradient using multidimensional scaling analysis. Mussel lease sites sampled in 1997 were clustered within predefined oxic sediment classifications along with the majority of reference sites, but were grouped farther along the enrichment gradient in 2001. The significant increase in hypoxic and sulfidic sediments within mussel farms between 1997 and 2001 is consistent with the 43% increase in PEI mussel production—a classic response to excessive organic biodeposition in shallow coastal inlets with relatively low dispersive capacity. Crown Copyright © 2009 Published by Elsevier B.V. All rights reserved.

1. Introduction High density populations of bivalve filter-feeders residing in shallow coastal waters may influence ecosystem structure and function by exerting both “top down” grazing control on the phytoplankton and “bottom-up” nutrient control via excretion of ammonia and the biodeposition of organic matter (Dame, 1996; Souchu et al., 1998; Christensen et al., 2003; Newell, 2004; Cranford et al., 2007). The increased organic loading of sediments from biodeposition may, under certain conditions, affect energy flow and nutrient cycling at the coastal ecosystem scale (e.g. Newell, 2004; Cranford et al., 2007). The annual global production of cultured bivalves has increased by 40% in the past decade at a rate of approximately 4.7 × 105 t y− 1 (1995 to 2004 data from the FAO; http://www.fao.org/fi/statist/summtab/default.asp). A fundamental understanding of the influence of this expanding industry on coastal ecosystems, as well as interactions with other anthropogenic stressors, is needed to develop strategies for sustainable aquaculture and integrated coastal zone management.

⁎ Corresponding author. Tel.: +1 902 426 3277; fax: +1 902 426 2256. E-mail address: [email protected] (P.J. Cranford).

Studies of shellfish aquaculture impacts on the benthic environment and macrobenthic communities have provided a continuum of results from observations of no, or minimal, negative effects (Baudinet et al., 1990; Grenz et al., 1990; Hatcher et al., 1994; Grant et al., 1995; Shaw, 1998; Chamberlain et al., 2001; Crawford et al., 2003; Hartstein and Rowden, 2004; Anderson et al., 2005; Mallet et al., 2006; Miron et al., 2005; Lasiak et al., 2006) to significant positive (Inglis and Gust, 2003; Clynick et al., 2008; D'Amours et al., 2008) and negative changes within farms (Dahlbäck and Gunnarsson, 1981; Mattsson and Linden, 1983; Kaspar et al., 1985; Tenore et al., 1985; Jaramillo et al., 1992; Chililev and Ivanov, 1997; Mirto et al., 2000; Stenton-Dozey et al., 1999, 2001; Chamberlain et al., 2001; Christensen et al., 2003; Smith and Shackley, 2004; Hartstein and Rowden, 2004; Giles et al., 2006; Metzger et al., 2007) and at the coastal ecosystem scale (Hargrave et al., 2008a). The extent and magnitude of benthic effects is always site specific with vulnerability depending on factors controlling waste organic matter input (scale, duration and intensity of shellfish production, husbandry practices, seston concentration, and food utilization rate and efficiency) and hydrographic and physical factors controlling the assimilative capacity of the local environment (water depth, sedimentation rate, current and wind speed). The only recorded far-field benthic effects of shellfish culture come from Tracadie Bay, Prince Edward Island, Canada (PEI; Fig. 1).

0044-8486/$ – see front matter. Crown Copyright © 2009 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2009.04.039

190

P.J. Cranford et al. / Aquaculture 292 (2009) 189–196

Fig. 1. Location of Prince Edward Island and the coastal embayments sampled in August 2001.

The low-energy hydrodynamic features of this shallow semi-enclosed lagoon, the large proportion of the bay leased for suspended mussel (Mytilus edulis) culture, and nutrient enrichment from land-use combine to result in high susceptibility to habitat alterations and, consequently, the documented pelagic (Cranford et al., 2007; Grant et al., 2008) and benthic effects (Hargrave et al., 2008a). Many shallow barrier beach lagoons and coastal plain estuaries in PEI support the suspended (long-line) culture of mussels. The PEI mussel industry expanded rapidly in the 1990s, stabilized at approximately 17,000 t y− 1 after 2000 (Fig. 2), and has supplied the majority of the total Canadian mussel production for four decades (Statistics Canada, 2005). A benthic survey of geochemical variables and benthic communities in 20 PEI embayments in 1997 (Shaw, 1998) showed general eutrophication effects from excess nutrient run-off from agriculture, but no apparent additional effects from mussel aquaculture. Annual mussel production has since expanded by

approximately 40% (Fig. 2) and the increased organic biodeposition may have exceeded the capacity of these inlets to disperse and assimilate organic wastes via tidal flushing and aerobic re-mineralization processes. In the present study, sediment cores and grabs were collected in 2001 from 11 PEI embayments to investigate benthic geochemical conditions inside mussel farms (leases) and at reference sites to test hypotheses on effects of increased aquaculture production and organic matter loading on the benthic environment. 2. Materials and methods A survey of seabed geochemical conditions was conducted in 11 Prince Edward Island embayments (Tracadie Bay, Savage Harbour, St. Peters Bay, New London Bay, March Water, Darnley Basin, St. Marys Bay, Montague River, Brudenell River, Mill River and Foxley River) between August 21 and 30, 2001 (Fig. 1). A total of 72 sampling stations were visited (Table 1) with positions provided by a Trimble

Table 1 Number of sites in Prince Edward Island embayments sampled in August, 2001.

Fig. 2. Annual aquaculture production of mussels (Mytilus edulis; ■) and total bivalves (▲) in Prince Edward Island (Source: Statistics Canada, 2005). The vertical lines indicate years that benthic geochemical surveys were conducted (Shaw, 1998, and present study).

Embayment

R

L1

L2

F

Tracadie Bay Savage Harbour St. Peters Bay Montague/Brudenell River New London Bay March Water Darnley Basin St. Marys Mill River Foxley River Total

4 3 2 4 (2) 4 2 3 5 – – 27 (2)

1 4 – – 4 – 2 3 – – 14

3 (3) 2 (2) 2 (1) 6 (5) 2 2 3 1 – – 21 (11)

– – – – – – – – 5 5 10

Site categories defined in the text are reference (R), mussel lease (L), lease containing small (b2 cm) first-year mussels (L1), lease with second year mussels (L2) and culturefree embayment (F). The number in parenthesis is the number of sites observed to contain white sulfur (Beggiatoa spp.) bacterial mats on the sediment surface.

P.J. Cranford et al. / Aquaculture 292 (2009) 189–196

model 200D differential GPS system. The sampling stations included 48 locations previously sampled by Shaw (1998), including mussel lease stations (n = 23) and reference stations located in mussel culture-free inlets (n = 6) and in inlets with mussel culture (n = 19). Reference stations were selected in areas that exhibited similar depth and bottom type as the lease stations and, due to space limitations in some aquaculture inlets, were located as close as 10 m to lease boundaries. Sampling at lease stations was conducted between the mussel long-lines. Additional stations were added in the present study as a result of changes in the locations of some mussel leases. Not all of the Shaw (1998) stations were sampled due to time constraints and weather conditions. Seabed video was collected at each station prior to sampling to record general seabed conditions (i.e. presence of epifauna and flora and sediment appearance) using a down-looking Sony CCD camera held in a pressure case and powered from the surface. Approximately 30 s of digital video was recorded at each site in Mini-DV format (Canon ZR25MC recorder). The presence/absence of white sulfur (Beggiatoa spp.) bacterial mats was determined at each station from both the bottom video and also by SCUBA divers. Additionally, SCUBA diver observations of cultured mussel shell size were used to characterize the area adjacent to each lease station as containing first or second year mussels. Surficial sediment was collected using three types of samplers (‘wedge’ corer, Eckmann grab and core tube) to assess the potential influence of collection method on measurements of total free sulfides (S = H2S, HS− and S=), redox potentials (EhNHE), water content (WC) and organic matter (OM). A single sediment sample was collected at each designated station with each sampler. A wedge corer (17.5 × 15 cm) constructed of clear acrylic (Wildish et al., 2003) was deployed by divers at all stations, except those in the Mill and Foxley River estuaries where an Eckmann grab (15 × 15 cm) was used. Eckmann grab and wedge cores were both collected at 8 sampling stations distributed throughout the other embayments for comparison of results. Immediately after collection, surface water was carefully siphoned off each grab or core aboard the vessel without disturbing the sediment surface. Three replicate 5 mL sub-samples (one replicate for both EhNHE and S analysis, one for both WC and OM determinations and one archive) were immediately collected from the wedge core or grab sample using cut-off 5-mL plastic disposable syringes filled by withdrawing the barrel as the syringe was inserted horizontally into the upper 2 cm surface layer. Syringes were tightly closed using a plastic cap to avoid exposure to air and stored on ice until analysis (12–24 h). Additional sediment samples were collected at 24 stations using clear acrylic core samplers (6.5-cm inside diameter, 50-cm length). The divers collected sediment cores up to 40 cm long by pushing the coring tubes into the sediment and capping the bottom and top before withdrawing from the seabed. The cores were labeled and transported to the laboratory upright in a chilled cooler within a few hours of collection. Cores were handled carefully to maintain an undisturbed sediment-water interface. Sub-samples from the top 0–2 cm of sediment for S, WC and OM measurements were collected by lateral insertion of 5-ml cut-off disposable plastic syringes through the side of the acrylic core tube via pre-drilled ∼1.5 cm diameter holes covered by duct tape. Core subsampling and electrode measurements (below) were conducted within 24 h of core collection. EhNHE potentials were determined in 5.0 mL of sediment extruded from one of the syringe sub-samples from the wedge and Eckmann grabs into a 100 mL plastic beaker using a Pt ion-specific combination electrode (Orion 96-78-00) containing an internal Ag/AgCl reference electrode filled with 4M KCL (Orion 900011). An Accumet model 1000 pH/mV meter (Fisher Scientific) was used to measure potentials (mV) that usually stabilized within 1–3 min. EhNHE was calculated by addition of the normal hydrogen electrode (NHE) potential of the reference electrode at the sample temperature as described in Wildish

191

et al. (1999). EhNHE potentials in core samples were measured by inserting the Pt electrode horizontally into the upper 2 cm sediment layer of sediment via the holes in the side of each acrylic core. S was measured on the same 5.0 mL of sediment immediately after EhNHE measurements by adding 5.0 mL of sulfide antioxidant buffer solution (SAOB) containing NAOH, EDTA and ascorbic acid (Thermo Electron Corp., 2003) to the sample and a glass stirring rod was used to mix the SAOB-sediment slurry. S concentration was read immediately (b2 min) using an Accumet model 1000 meter with an Orion Ag+/S= combination ionplus® electrode (96-16N) filled with Orion Optimum “A” filling solution. A three-point electrode calibration was conducted with Na2S·9H2O (Wildish et al., 1999; Thermo Electron Corp., 2003). Stable readings were usually obtained within 1–2 min. S concentrations were expressed as µM based on total sediment volume (5 mL). Since the Ag+/S= electrode responds only to free ions, corrected concentrations in pore water (Spc)(µM mL− 1) were calculated as: Spc = S = ðWC = 100Þ

ð1Þ

This correction accounts for dilution of S in pore water by addition of the buffer solution since sample and SAOB volumes were both 5.0 mL and WC was measured as follows in all samples. WC and OM were determined using 1.0 mL of wet sediment sample extruded from a second 5 mL syringe into a pre-weighed scintillation vial. Vials were tightly capped to prevent dehydration until weighed using a Mettler AE balance (±0.05 mg). After drying to a constant weight (60 °C, 24 h) and re-weighing, WC was determined as percent weight loss. The sample was then pulverized using a mortar and pestle, placed on pre-ashed and pre-weighed aluminum foil (∼ 2 cm2), combusted in an ashing oven (550 °C, 4 h) and OM calculated from weight loss as a percent of sample dry weight. WC, OM and EhNHE in surface sediment were used to derive a Benthic Enrichment Index (BEI; Hargrave, 1994) that decreases with increasing organic enrichment. Since we measured organic matter and not organic carbon, a molar conversion of 36 rather than 12 was used to calculate BEIOM as: BEIOM = ððððð100 − WCÞ = 100Þ⁎10; 000Þ⁎ðOM = 100ÞÞ = 36Þ⁎EhNHE ð2Þ Statistical analysis was conducted using SYSTAT Version 12 (SPSS, Inc., Chicago, IL). The alternate hypothesis was accepted if the p-value was greater than 0.05. Prior to analysis, logarithmic or square-root data transformations were conducted to achieve normality as confirmed from probability plots and Shapiro–Wilk tests. Equality of variance was determined from residual plots. These tests indicated that two of the 72 sites contained outlier data that had to be omitted from hypothesis testing to meet normality and homoscedasticity assumptions. Mean geochemical conditions in surface seabed samples collected using the different sampling methods (wedge core, core and Ekmann grab) were compared using one-way MANOVA based on the Pillai Trace test statistic. The five dependent variables employed in this multivariate analysis were WC, OM, EhNHE, S and Spc. Geochemical conditions in August 2001 were also compared across the different site categories using a one-way MANOVA. The same five dependent variables were included, and the four site categories were mussel culture free (F); reference (R), lease with first year mussels (L1), and lease with second year mussels (L2). In the case of a significant MANOVA result, post-hoc multiple comparison tests were conducted to contrast site categories and to discern which variables accounted for the overall difference. Differences between site categories were detected using multivariate F-tests while the variable(s) involved in a significant MANOVA result were determined from univariate F-tests provided along with the MANOVA results. Comparisons of surface seabed conditions (WC, OM, EhNHE, S, and Spc) observed in August 2001 with those previously recorded in August/September, 1997 (Shaw, 1998) were also conducted using

192

P.J. Cranford et al. / Aquaculture 292 (2009) 189–196

3. Results 3.1. Influence of sampling methodology Surface sediment conditions in samples collected using the different sampling methods (wedge core, standard core and Ekmann grab) provided similar results. One-way MANOVA showed that the multivariate mean was not significantly different for contrasts of geochemical data obtained using wedge and standard coring methods (DF = 4, 41; p = 0.110) and using wedge cores and Eckman grabs (DF = 4, 11; p = 0.410). Consequently, for stations where replicate samples were taken using these different methods, average geochemical values for each station were used in all subsequent statistical analysis. 3.2. Site classification and surface sediment features

Fig. 3. Average (± 2SE) geochemical characteristics of surface seabed sediments (0–2 cm depth) from Prince Edward Island coastal embayments in August, 2001. Sites are grouped as: mussel culture free (F, n = 10); reference (R, n = 25); lease containing small (b 2 cm) first-year mussels (L1, n = 14); and lease containing second year mussels (L2, n = 21). Variables are water content (WC), organic matter (OM), redox potential (EhNHE), Benthic Enrichment Index (BEIOM), and sulfide concentration based on sediment volume (S) and in pore water (Spc).

one-way MANOVA and post-hoc comparisons, except with sampling date (1997 and 2001) as the factor. Only those locations sampled in both studies, and where the site classification remained the same, were included in this analysis (n = 40). S and WC content data provided by Shaw (1998) were used to calculate Spc according to Eq. (1). Shaw (1998) used only one lease site classification, so the three site categories tested were culture free (F), reference (R) and mussel lease (L). A fully factorial two-way (station category and date factors) MANOVA was not employed as contrasts between station categories have already been reported for the 1997 data (Shaw, 1998) and was conducted separately for the full 2001 data set (see above). Non-metric multi-dimensional scaling (MDS), based on a Kruskal loss function and a correlation matrix of Euclidean distances, was used to further contrast geochemical conditions between site categories and sampling dates. A single MDS analysis was conducted using data from all sites sampled in 1997 and 2001 (n = 184 sites) with untransformed values of WC, OM, EhNHE and S. Spc is calculated from WC and S (Eq. (1)) and was therefore excluded from MDS.

Surficial sediment geochemical conditions within the 11 Prince Edward Island coastal inlets during the August 2001 survey generally indicated moderate to high benthic enrichment, including sites within the two mussel culture-free (F) estuaries (Foxley and Mill River) and reference (R) sites located in all inlets. For example, mean S exceeded 1200 µM within all site categories (Fig. 3). Culture-free inlets, on average, contained the least enriched sites and exhibited positive EhNHE and BEIOM mean values. Reference sites within mussel culture embayments had similar WC and OM content as the culture-free sites, but mean EhNHE and BEIOM were negative and mean S and Spc were elevated. Sediment collected from within mussel leases exhibited the highest mean WC, OM, S, and Spc and lowest EhNHE and BEIOM of all the site categories. Lease sites containing first- (L1) and second-year (L2) mussels were similarly enriched, albeit with slightly lower organic enrichment (lower mean WC, OM and S; Fig. 3) at the former sites. Of the 27 reference sites sampled, 8% contained white sulfur (Beggiatoa spp.) bacterial mats on the sediment surface, while mats were present at 52% of the second year mussel sites (Table 1). The results of MANOVA comparisons across the four station categories are given in Table 2. The overall MANOVA of the 2001 data revealed a significant multivariate difference between station classifications (p b 0.001) and the post-hoc protected F procedure on each of the dependent variables showed that WC, OM, EhNHE, and S were responsible for this difference. Planned post-hoc contrasts between specific site classifications showed a significant difference in multivariate means between R and L2 sites, largely due to differences in WC, OM, and S (Table 2). However, the multivariate contrast between R and L1 sites was equivocal (p = 0.055). The contrast between mean geochemical conditions at F and R sites, and between L1 and L2 sites were not significantly different (p N 0.102). This allowed pooling of data into control (R + F sites) and mussel lease (L1 + L2) categories to increase sample size and statistical power. One-way MANOVA on these pooled data (site classification factor with two levels and same five dependent variables) showed a significant multivariate difference between control and lease sites (p b 0.001) with post-hoc tests

Table 2 Summary table of results from one-way multivariate analysis of variance (MANOVA) on surficial sediment geochemical conditions in PEI inlets during August, 2001. Hypothesis F = R = L1 = L2 F=R R = L1 R = L2 L1 = L2 F + R = L1 + L2

Multivariate test statistics

Univariate F-test p-values

Pillai Trace

F-ratio

DF

p

WC

OM

EhNHE

S

Spc

0.597 0.260 0.269 0.371 0.219 0.363

3.239 2.040 2.432 4.483 1.517 7.061

15, 166 5, 29 5, 33 5, 38 5, 27 5, 62

0.000⁎ 0.102 0.055 0.003⁎ 0.218 0.000⁎

0.001⁎ – – 0.003⁎ – 0.000⁎

0.001⁎ – – 0.000⁎ – 0.000⁎

0.000⁎ – – 0.068 – 0.000⁎

0.001⁎ – – 0.001⁎ – 0.000⁎

0.055 – – 0.064 – 0.009⁎

The station classification factor had four levels; mussel culture free (F), reference (R), mussel lease (L), and lease with first (L1) and second year mussels (L2). Variables included are; water content (WC, %), organic matter (OM, %), redox potential (EhNHE, mV), sulfide concentration based on sediment volume (S, µM); and in pore water (Spc, µM mL− 1). The hypotheses indicated were tested by multivariate F-tests based on the Pillai Trace statistic. Post-hoc multivariate comparison tests between station classifications and univariate F-tests for each variable were only performed following a significant MANOVA result. ⁎p ≤ 0.05.

P.J. Cranford et al. / Aquaculture 292 (2009) 189–196

Fig. 4. Average (± 2SE) geochemical characteristics of surface seabed sediments (0–2 cm depth) measured at the same sites in Prince Edward Island coastal inlets in August/September, 1997 (data from Shaw, 1998; shaded bars) and August 2001 (this study; white bars). Sites are grouped as mussel culture free (F; n = 6), reference (R; n = 14), and mussel lease (L; n = 20). Variables are water content (WC), organic matter (OM), redox potential (EhNHE), Benthic Enrichment Index (BEIOM), and sulfide concentration based on sediment volume (S) and in pore water (Spc).

showing highly significant differences between control and mussel lease sites for all five variables (p b 0.009).

3.3. Temporal variations in sediment geochemical conditions Average sediment conditions at 40 stations sampled both in August/September 1997 (data from Shaw, 1998) and August 2001 are shown in Fig. 4 and results of the one-way MANOVA comparison between years are presented in Table 3. MANOVA indicated an overall significant multivariate mean difference between sampling dates (p b 0.001) and post hoc univariate tests showed this effect was largely the result of differences in mean sulfide concentrations (p b 0.005 for S and Spc). Average S and Spc increased by 39 and 31%, respectively, between 1997 and 2001 (Fig. 4). Multi-dimensional scaling of data from all stations sampled in PEI inlets in 1997 and 2001 provided additional insight into differences between station categories and sampling dates (Fig. 5). The MDS

193

Fig. 5. Two-dimensional ordination generated by non-metric multidimensional scaling (stress = 0.001) of surface sediment geochemical conditions (water content, organic matter, redox potentials, and total sulfides) at all Prince Edward Island sites (n = 184) sampled in August–September, 1997 (bottom: data from Shaw, 1998), and August, 2001 (top). Both plots represent the same multivariate space defined by a single analysis. Symbols are culture-free (♦), reference (■) and mussel lease (○) sites. Vertical dashed lines separate organic enrichment zones defined in Hargrave et al. (2008b).

analysis mapped results from all the sampling sites in 2-dimensional space, such that dissimilarity of geochemical conditions between sites is represented by the distance between points on an X–Y plot. S accounted for all of the variance in Dimension 1 (X axis) and other variables contributed to variability along the Dimension 2 axis. A high inverse correlation between S and Dimension 1 (r 2 = 1.000) allowed the degree of organic enrichment at each site to be classified on the MDS plot based on the S concentration thresholds given in Hargrave et al. (2008b). Sampling sites were mapped on the MDS plot along a continuum of organic enrichment, with Oxic A (b750 µM S) sites located on the right side of the plot and Hypoxic B (3000–6000 µM S) conditions to the left (Fig. 5). The cluster of R and F sites was similarly positioned on the 1997 and 2001 MDS plots, but the clustering of L sites changed between years, indicating increased dissimilarity in geochemical conditions. Mussel leases in 1997 are clustered primarily within the Oxic A and B (750–1500 µM S) regions of the MDS plot, while the 2001 data are grouped mainly in the Hypoxic A region (1500–3000 µM S).

Table 3 Summary table of results from one-way multivariate analysis of variance (MANOVA) on surface sediment geochemical conditions at 40 stations in PEI inlets sampled both in August/ September, 1997 and August, 2001. Hypothesis 1997 = 2001 F1997 = F2001 R1997 = R2001 L1997 = L2001

Multivariate test statistics

Univariate F-test p-values

Pillai Trace

F-ratio

DF

p

WC

OM

EhNHE

S

Spc

0.337 0.834 0.309 0.342

7.515 6.010 1.968 3.534

5, 5, 5, 5,

0.000⁎ 0.025⁎ 0.184 0.000⁎

0.389 0.575 – 0.720

0.144 0.367 – 0.135

0.844 0.843 – 0.453

0.005⁎ 0.591 – 0.029⁎

0.003⁎ 0.675 – 0.016⁎

74 6 22 34

The date factor has two levels (1997 and 2001) and the variables are water content (WC, %), organic matter (OM, %), redox potential (EhNHE, mV), and sulfide concentration based on sediment volume (S, µM) and in pore water (Spc, µM mL− 1). MANOVA compared data from all sites between dates and at culture-free (F), reference (R) and mussel lease (L) sites. The indicated hypotheses were tested by multivariate F-tests based on the Pillai Trace statistic. Post-hoc univariate F-tests for each variable were only performed following a significant multivariate result. ⁎p ≤ 0.05.

194

P.J. Cranford et al. / Aquaculture 292 (2009) 189–196

4. Discussion Investigations of potential benthic effects have been a major emphasis of studies on the ecological impacts of intensive shellfish farming. The concern is that sediment organic loading from biodeposition may cause alterations in the benthic environment with subsequent changes in macrofaunal communities. Our study of sediment organic enrichment in Prince Edward Island coastal embayments showed a significant increase in hypoxic and sulphidic sediments both within mussel farms relative to the reference sites (Figs. 3–5; Table 2) and within farms in 2001 relative to the same farm stations in 1997 (Fig. 5; Table 3). Surface sediment variables within mussel leases exhibited typical conditions associated with sulphate reduction. EhNHE potentials and values for the Benthic Enrichment Index shifted towards increasingly negative values, S concentration in pore water almost doubled owing to the predominance of sulphate reduction, and white filamentous mats of sulphide-oxidizing bacteria (Beggiatoa spp.) became more prominent than at the reference stations (Table 1, Fig. 3). Beggiatoa requires both oxygen and H2S for metabolism and the presence of mats indicates that reducing conditions reach the sediment/water interface. Our conclusion that the benthic environment inside mussel leases in 2001 was significantly degraded relative to reference sites is in contrast to results from a 1997 survey of many of the same PEI inlets and sampling stations using the same methods employed in our study (Shaw, 1998). There are several potential explanations for a significant increase in hypoxic and sulphidic conditions in surface sediments during this four-year period. Agriculture is an important industry in PEI and the use of synthetic fertilizer results in substantial nutrient run-off that supports a large proportion of the biological productivity of coastal waters (Meeuwig, 1999) which helps sustain the mussel culture (Cranford et al., 2007). Agriculture is an important source of benthic organic enrichment in PEI inlets as indicated by relatively low EHNHE and high sulfide concentration across most reference sites (Fig. 3). Although MANOVA indicated an overall significant difference in surface sediment conditions between 1997 and 2001 at stations in mussel culture-free inlets, post-hoc tests showed no difference in any of the measured variables and mean values indicated both slight increases (S) and decreases (WC, OM and EHNHE) in organic enrichment over time (Table 3, Fig. 4). There was no apparent change in benthic organic enrichment at reference sites that could be related to nutrient run-off. In fact, total agricultural farm area has remained stable and PEI farmers are involved in nutrient management initiatives including reduction in nitrogen application (Statistics Canada, 2004). Extensive sampling in Tracadie Bay (Fig. 1) has shown that benthic organic enrichment from run-off is greatest near the freshwater outflow and decreases to seaward (Hargrave et al., 2008a). This is in contrast to the observed spatial distribution of benthic effects attributed to mussel culture that were greatest in the outer part of the Bay adjacent to the primary mussel grow-out areas. Mass balance and lower trophic level box model results for Tracadie Bay indicate that mussel biodeposition is the major pathway for benthic enrichment relative to other supply pathways (Dowd, 2005; Cranford et al., 2007). The 43% increase in PEI mussel production between 1997 and 2001 (Fig. 2; Statistics Canada, 2005) would result in a proportional increase in organic matter biodeposition and is the apparent cause for the significantly elevated hypoxic and sulphidic benthic conditions occurring within the sampled PEI mussel leases. There are two factors related to sampling design that complicate assigning causality to the observed enrichment effects under shellfish farms. The first stems from not having data on benthic conditions prior to the start of culture activities. These data are needed to confirm that reference and lease sites were initially identical with respect to natural variations in geochemical conditions. Unfortunately, a BACI sampling design has seldom been utilized in shellfish culture impact studies (Lasiak et al., 2006). The approach of Shaw (1998), which we replicated in time, was to sample reference sites in mussel culture-free

inlets with similar depth and sediment type to minimize the potential for this type of error. That study showed that conditions at reference and lease sites were not significantly different and therefore established the pre-impact conditions needed for the present study to identify changes coincident with mussel industry expansion. The second confounding factor in the experimental design is the possible organic enrichment of reference sites from the advection of mussel biodeposits from leased areas. The reality of such far-field effects on organic enrichment was previously documented for Tracadie Bay (Hargrave et al., 2008a). Although there was some evidence of enhanced enrichment at reference stations on our study (Fig. 3), no significant difference between the culture-free and reference stations was observed in 2001 (Table 2) or previously by Shaw (1998). We therefore feel confident in assigning causality to excessive biodeposition from mussel culture for the significant increase in hypoxic and sulphidic sediments in mussel farms between 1997 and 2001. The results of the present study parallel those at finfish farms in that they demonstrate that the measured geochemical variables are effective and sensitive indicators of benthic habitat and community modifications stemming from increased biodeposition (Wildish et al., 2001). Although direct observations of biological community effects are generally preferred over chemical indicators in environmental monitoring programs, the former measures are costly and require specialized facilities, technical expertise and considerable time and effort for taxonomic analysis and to interpret results; all of which tend to result in small sample size in field experimental designs and subsequent reduction in statistical power for addressing hypotheses. The foundation for assigning a relative level of disturbance to benthic communities, based on the results of sediment geochemical analysis, is the Pearson and Rosenberg (1978) enrichment-disturbance model. Reduced oxygen availability and increased toxic free sulfide levels in organically enriched sediments are major factors controlling the structure and function of benthic communities (e.g. Pearson and Rosenberg, 1978; Diaz and Rosenberg, 1995; Nilsson and Rosenberg, 2000). While moderate organic enrichment can stimulate an increased biomass of opportunistic species, increasing levels of organic enrichment leads to the progressive reduction in species richness, reduced body size and a transition from suspension- to deposit-feeding organisms (Diaz and Rosenberg, 1995; Hyland et al., 2005; Miron et al., 2005; Kalantzi and Karakassis, 2006). Sediment organic enrichment and/or alterations in benthic fauna in mussel farm areas have not always been detected (Baudinet et al., 1990; Grenz et al., 1990; Hatcher et al., 1994; Grant et al., 1995; Chamberlain et al., 2001; Crawford et al., 2003; Hartstein and Rowden, 2004; Anderson et al., 2005; Mallet et al., 2006; Da Costa and Nalesso, 2006; Lasiak et al., 2006). Most of these studies were conducted in areas with relatively deep water and high current velocity. On the other hand, where currents are weak, or water depth is relatively shallow, biodeposits accumulate and contribute to the formation of hypoxic conditions in sediments, resulting in alteration of benthic infaunal assemblages (Mattsson and Linden, 1983; Kaspar et al., 1985; Tenore et al., 1985; Jaramillo et al., 1992; Chililev and Ivanov, 1997; Mirto et al., 2000; Stenton-Dozey et al., 1999, 2001; Chamberlain et al., 2001; Christensen et al., 2003; Smith and Shackley, 2004; Hartstein and Rowden, 2004; Callier et al., 2007; Giles et al., 2006; Hargrave et al., 2008a). The magnitude and severity of effects of shellfish culture vary substantially between study sites depending on the outcome of a complex interplay between many operational and environmental factors, with the local hydrodynamic regime having a major influence. Other factors that may alter, ameliorate or hinder detection of the classic benthic response to organic enrichment, include spatial variations in grain size, the presence of Zostera beds (Hargrave et al., 2008a), cumulative effects from different stressors, and/or the presence of an “unstable” benthic community. The intensity of shellfish culture operations is an important factor in determining the degree of benthic organic enrichment and

P.J. Cranford et al. / Aquaculture 292 (2009) 189–196

Crawford et al. (2003) attributed the absence of infaunal disturbances inside farms in a sheltered, low-energy coastal area to low shellfish stocking density. Some studies have noted that farms supporting higher levels of production had a greater influence on the benthic environment (Richard et al., 2006, 2007; Hargrave et al., 2008a). Differences in mean organic content and sulfide concentrations in sediments within leases containing first- and second-year mussels provide evidence of elevated organic enrichment inside farms containing a greater biomass of mussels (Fig. 3), but the difference was not significant (Table 2). However, the large change in mussel biomass between 1997 and 2001 (Fig. 2) was apparently sufficient to result in a significant increase in hypoxic and sulphidic sediments. Previous studies of sediment geochemical conditions at salmonid and mussel aquaculture sites (Wildish et al., 2001, 2004; Schaanning and Kupka Hansen, 2005; Holmer et al., 2005; Hargrave et al., 2008a) provided ranges of S concentrations used to assign organic enrichment classifications to each of our sampling sites. These were used along with a multivariate ordination technique (MDS) to compare site conditions and changes in enrichment classification over time (Fig. 5). MDS alone provides only a relative scale of site similarity–dissimility that might lead to subjective interpretations of results. Benthic organic enrichment conditions in PEI embayments in 2001 covered a wide range of enrichment classifications from Oxic A (8 control sites) to Hypoxic B (3 lease sites) (Fig. 5). On average, the reference sites exhibited surface sediment conditions within Oxic B thresholds, while average conditions in mussel leases in 2001 can be classified as Hypoxic A (Fig. 5). Mussel leases presently occupy an area of ∼42 km2 of PEI coastal and estuarine waters (Department of Fisheries and Oceans Licensing, Charlottetown). A description of marine benthic fauna changes that may be expected across these enrichment classifications is provided in Hargrave et al. (2008b). Annual production rates of PEI mussel farms are relatively low compared with those in many other regions where significant environmental effects have been observed (Crawford et al., 2003; Mallet et al., 2006). The presence of the reported benthic effects can largely be attributed to the relatively limited capacity for dispersal of biodeposits in these shallow, sheltered and poorly-flushed embayments. Empirical results on the scale and magnitude of benthic organic enrichment effects resulting from different levels of mussel production help to facilitate; (1) the development of generic impact assessment approaches (i.e. risk assessment and prognostic modeling), (2) the identification of pragmatic and effective monitoring indicators and aquaculture management decision thresholds, (3) the design of farm sampling/monitoring programs, and (4) identification of appropriate impact mitigation measures. These aquaculture and habitat management initiatives are intended to ensure sustainability and to maintain habitat, biodiversity and ecosystem productivity. To achieve these goals in PEI, and elsewhere, an appropriate balance between mussel production and the dispersive and assimilative capacity of the surrounding area needs to be established. Acknowledgements We thank S. L. Armsworthy, V. Burdette-Coutts, B. Law, C. Léger, T. Milligan, and A. Stewart for assistance during field work and G. A. Phillips for support in the laboratory. This paper benefited from comments provided by C. DiBacci and M. Wong and three anonymous reviewers. This work was funded by Fisheries and Oceans Canada through the ESSRF program. References Anderson, M.R., Tlusty, M.F., Pepper, V.A., 2005. Organic enrichment at cold water aquaculture sites—the case of coastal Newfoundland. In: Hargrave, B.T. (Ed.), Environmental Effects of Marine Finfish Aquaculture. Hdb. Environ. Chem., vol. 5. Springer, Berlin, pp. 99–113.

195

Baudinet, D., Alliot, E., Berland, B., Grenz, C., Plante-Cuny, M., Plante, R., Salen-Picard, C., 1990. Evidence of mussel culture on biogeochemical fluxes at the sediment–water interface. Hydrobiologia 207, 187–196. Callier, M.D., McKindsey, C.W., Desrosiers, G., 2007. Multi-scale spatial variations in benthic sediment geochemistry and macrofaunal communities under a suspended mussel culture. Mar. Ecol. Prog. Ser. 348, 105–115. Chililev, S., Ivanov, M., 1997. Response to the Arctic benthic community to excessive amounts of nontoxic organic matter. Mar. Poll. Bull. 35, 280–286. Chamberlain, J., Fernandes, T.F., Read, P., Nickell, T.D., Davies, I.M., 2001. Impacts of deposits from suspended mussel (Mytilus edulis L.) culture on the surrounding surficial sediments. ICES J. Mar. Sci. 58, 411–416. Christensen, P.B., Glud, R.N., Dalsgaard, T., Gillespie, P., 2003. Impacts of long line mussel farming on oxygen and nitrogen dynamics and biological communities of coastal sediments. Aquaculture 218, 567–588. Clynick, B.G., McKindsey, C.W., Archambault, P., 2008. Distribution and productivity of fish and macroinvertebrates in mussel aquaculture sites in the Magdalen islands (Québec, Canada). Aquaculture 283, 203–210. Cranford, P.J., Strain, P.M., Dowd, M., Hargrave, B.T., Grant, J., Archambault, M.-C., 2007. Influence of mussel aquaculture on nitrogen dynamics in a nutrient enriched coastal embayment. Mar. Ecol. Prog. Ser. 347, 61–78. Crawford, C.M., MacLeod, C.K.A., Mitchell, I.M., 2003. Effects of shellfish farming on the benthic environment. Aquaculture 244, 117–140. D'Amours, Olivier, Archambault, P., McKindsey, C.W., Johnson, L.E., 2008. Local enhancement of epibenthic macrofauna byaquaculture activities. Mar. Ecol. Prog. Ser. 371, 73–84. Da Costa, K.G., Nalesso, R.C., 2006. Effects of mussel farming on macrobenthic community structure in southern Brazil. Aquaculture 258, 655–663. Dahlbäck, B., Gunnarsson, L.A.H., 1981. Sedimentation and sulfate reduction under a mussel culture. Mar. Biol. 63, 269–275. Dame, R.F., 1996. Ecology of Marine Bivalves: An Ecosystem Approach CRC Marine. Diaz, R.J., Rosenberg, R., 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioural response of benthic macrofauna. Oceanogr. Mar. Biol. Ann. Rev. 33, 245–303. Dowd, M., 2005. A biophysical model for assessing environmental effects of marine bivalve aquaculture. Ecol. Model. 183, 323–346. Giles, H., Pilditch, C.A., Bell, D.G., 2006. Sedimentation from mussel (Perna canaliculus) culture in the Firth of Thames, New Zealand: impacts on sediment oxygen and nutrient fluxes. Aquaculture 261, 125–140. Grant, J., Hatcher, A., Scott, D.B., Pocklington, P., Schafer, C.T., Winters, G.V., 1995. A multidisciplinary approach to evaluating impacts of shellfish aquaculture on benthic communities. Estuaries 18 (1A), 124–144. Grant, J., Bacher, C., Cranford, P.J., Guyondet, T., Carreau, M., 2008. A spatially explicit ecosystem model of seston depletion in dense mussel culture. J. Mar. Syst. 73,155–168. Grenz, C., Hermin, M., Baudinet, D., Daumas, R., 1990. In situ biochemical and bacterial variation of sediments enriched with mussel biodeposits. Hydrobiologia 207, 153–160. Hargrave, B.T., 1994. A benthic enrichment index. Can. Tech. Rep. Fish. Aquat. Sci. 1949, 79–91. Hargrave, B.T., Doucette, L.I., Cranford, P.J., Law, B.A., Milligan, T.G., 2008a. Influence of mussel aquaculture on benthic organic enrichment in a nutrient-rich coastal embayment. Mar. Ecol. Prog. Ser. 365, 137–149. Hargrave, B.T., Holmer, M., Newcombe, C.P., 2008b. Towards a classification of organic enrichment in marine sediments based on biogeochemical indicators. Mar. Poll. Bull. 56, 810–824. Hatcher, A., Grant, J., Schofield, B., 1994. Effects of suspended mussel culture (Mytilus spp.) on sedimentation, benthic respiration and sediment nutrient dynamics in a coastal bay. Mar. Ecol. Prog. Ser. 115, 219–235. Hartstein, N.D., Rowden, A.A., 2004. Effect of biodeposits from mussel culture on macroinvertebrate assemblages at sites of different hydrodynamic regime. Mar. Environ. Res. 57, 339–357. Holmer, M., Wildish, D., Hargrave, B.T., 2005. Organic enrichment from marine finfish aquaculture and effects on sediment processes. In: Hargrave, B.T. (Ed.), Environmental Effects of Marine Finfish Aquaculture. Hdb. Environ. Chem., vol. 5. Springer, Berlin, pp. 181–206. Hyland, J., Balthis, L., Karakassis, I., Magni, P., Petrov, A., Shine, J., Vestergaard, O., Warwick, R.M., 2005. Organic carbon content of sediments as an indicator of stress in the marine benthos. Mar. Ecol. Prog. Ser. 295, 91–103. Inglis, G.J., Gust, N., 2003. Potential indirect effects of shellfish culture on the reproductive success of benthic predators. J. Appl. Ecol. 40, 1077–1089. Jaramillo, E., Bertran, C., Bravo, A., 1992. Mussel biodeposition in an estuary in southern Chile. Mar. Ecol. Prog. Ser. 82, 85–94. Kalantzi, I., Karakassis, I., 2006. Benthic impacts of fish farming: meta-analysis of community and geochemical data. Mar. Pollut. Bull. 52, 484–493. Kaspar, H., Gillespie, P., Boyer, I.C., MacKenzie, A.L., 1985. Effects of mussel aquaculture on the nitrogen cycle and benthic communities in Kenepuru Sound, Marlborough Sounds, New Zealand. Mar. Biol. 85, 127–136. Lasiak, T.A., Underwood, A.J., Hoskin, M., 2006. An experimental assessment of the potential impacts of longline mussel farming on the infauna in an open coastal embayment. Aquatic Conserv.: Mar. Freshw. Ecosyst. 16, 289–300. Mallet, A.L., Carver, C.E., Landry, T., 2006. Impact of suspended and off-bottom eastern oyster culture on the benthic environment in eastern Canada. Aquaculture 255, 362–373. Mattsson, J., Linden, O., 1983. Benthic macrofauna succession under mussels, Mytilus edulis L. (Bivalvia), cultured on hanging long-line. Sarsia 68, 97–102. Metzger, E., Simonucci, C., Viollier, E., Sarazin, G., Prévot, F., Jézéquel, D., 2007. Benthic response to shellfish farming in Thau lagoon: pore water signature. Estuar. Coast. Shelf Sci. 72, 406–419.

196

P.J. Cranford et al. / Aquaculture 292 (2009) 189–196

Meeuwig, J.J., 1999. Predicting coastal eutrophication from land-use: an empirical approach to small non-stratified estuaries. Mar. Ecol. Prog. Ser. 176, 231–241. Miron, G., Landry, T., Archambault, P., Frenette, B., 2005. Effects of mussel culture husbandry practices on various benthic characteristics. Aquaculture 250, 138–154. Mirto, S., Rosa, R.L., DanoVaro, R., Mazzola, A., 2000. Microbial and meiofaunal response to intensive mussel-farm biodeposition in the coastal sediments of the Western Mediterranean. Mar. Pollut. Bull. 40, 244–252. Newell, R.I.E., 2004. Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J. Shellfish Res. 23, 51–61. Nilsson, H.C., Rosenberg, R., 2000. Succession in marine benthic habitats and fauna in response to oxygen deficiency: analysed by sediment-profile imaging and by grab samples. Mar. Ecol. Prog. Ser. 197, 139–149. Pearson, T.H., Rosenberg, R., 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceangr. Mar. Biol. Ann. Rev. 16, 229–311. Richard, M., Archambault, P., Thouzeau, G., McKindsey, C., Desrosiers, G., 2006. Influence of suspended scallop cages and mussel lines on pelagic and benthic biogeochemical fluxes in havre-aux-Maisons lagoon, Îles-de-la-Madeleine (Québec, Canada). Can. J. Fish. Aquat. Sci. 64, 1491–1505. Richard, M., Archambault, P., Thouzeau, G., Desrosiers, G., 2007. Summer influence of 1 and 2 yr old mussel cultures on benthic fluxes in Grande-Entrée lagoon, Îles-de-laMadeleine (Québec, Canada). Mar. Ecol. Prog. Ser. 338, 131–143. Schaanning, M.T., Kupka Hansen, P., 2005. The suitability of electrode measurement for assessment of benthic organic impact and their use in a management system for marine fish farms. In: Hargrave, B.T. (Ed.), Environmental Effects of Marine Finfish Aquaculture. Hdb. Environ. Chem., vol. 5. Springer, Berlin, pp. 381–408. Shaw, K.R., 1998. PEI benthic survey. Tech. Rep. Environ. Sci. 4 iv+95 pp. Smith, J., Shackley, S.E., 2004. Effects of a commercial mussel Mytilus edulis lay on a sublittoral, soft sediment benthic community. Mar. Ecol. Prog. Ser. 282, 185–191.

Souchu, P., Gasc, A., Collos, Y., Vaquer, A., Tournier, H., Bibent, B., Deslous-Paoli, J.M., 1998. Biogeochemical aspects of bottom anoxia in a Mediterranean lagoon (Thau, France). Mar. Ecol. Prog. Ser. 164, 135–146. Statistics Canada, 2004. Fertilizer and pesticide management in Canada, vol. 1. No. 3. Catalogue no. 21-021-MIE—No. 003. www.statcan.ca. Statistics Canada, 2005. Aquaculture Statistics. Catalogue no. 23-222-XIE. www.statcan.ca. Stenton-Dozey, J.M.E., Jackson, L.F., Busby, A.J., 1999. Impact of mussel culture on macrobenthic community structure in Saldanha Bay, South Africa. Mar. Pollut. Bull. 39, 357–366. Stenton-Dozey, J., Probyn, T., Busby, A., 2001. Impact of mussel (Mytilus galloprovincialis) raft-culture on benthic macrofauna, in situ oxygen uptake, and nutrient fluxes in Saldanha Bay, South Africa. Can. J. Fish. Aquat. Sci. 58, 1021–1031. Tenore, K.R., Corral, J., Gonzalez, N., 1985. Effects of intense mussel culture on food patterns and production in coastal Galicia, NW Spain. ICES CM. 1985/F. 62. Thermo Electron Corporation, 2003. Orion silver/silver sulfide electrode instruction manual. Beverly MA USA, 1–67 pp. Wildish, D.J., Akagi, H.M., Hamilton, N., Hargrave, B.T., 1999. A recommended method for monitoring sediments to detect organic enrichment from mariculture in the Bay of Fundy. Tech. Rep. Fish. Aquat. Sci. 2286, iii+31. Wildish, D.J., Hargrave, B.T., Pohle, G., 2001. Cost effective monitoring of organic enrichment resulting from salmon mariculture. ICES J. Mar. Sci. 58, 469–476. Wildish, D.J., Hargrave, B.T., MacLeod, C., Crawford, C., 2003. Detection of organic enrichment near finfish net-pens by sediment profile imaging at SCUBA-accessible depths. J. Exp. Mar. Biol. Ecol. 285–286, 403–413. Wildish, D.J., Hughes-Clarke, J.E., Pohle, G.W., Hargrave, B.T., Mayer, L.M., 2004. Acoustic detection of organic enrichment in sediments at a salmon farm is confirmed by independent groundtruthing methods. Mar. Ecol. Prog. Ser. 267, 99–105.