The Effect of Seafood Processing Plant Effl uent on

Water Qual. Res. J. Canada, 2007 · Volume 42, No. 3, 172-183Copyright © 2007, CAWQ

The Effect of Seafood Processing Plant Effl uent on Sentinel Fish Spe-cies in Coastal Waters of the Southern Gulf of St. Lawrence, New

Brunswick

Marie-Hélène Thériault,1,2* Simon C. Courtenay,1,2,3 Kelly R. Munkittrick,3 and Alyre G. Chiasson2

1 Gulf Fisheries Centre, Fisheries and Oceans Canada, Moncton New Brunswick E1C 9B62 Department of Biology, Université de Moncton, Moncton New Brunswick E1A 3E9

3 Canadian Rivers Institute, University of New Brunswick, Fredericton and Saint John, New Brunswick E3B 6E1

This study evaluated effects of effl uents discharged by seafood processing plants on populations of fi sh living in shallow estua-rine waters of the southern Gulf of St. Lawrence. To monitor potential nutrient and/or toxicity impacts on fi sh populations living and possibly feeding in the effl uent, we measured indices of survival (age), growth (weight-at-age), reproduction (gonad weight), and energy storage (liver weight, condition factor) on mummichog (Fundulus heteroclitus) and Atlantic silverside (Menidia menidia) in spring, summer, and fall. Fish exposed to effl uents in three bays were compared to fi sh from a local reference site within the same bay and from regional reference sites in bays without seafood plants. Mummichog caught near seafood processing plants showed a number of differences from reference fi sh consistent with a localized nutrient enrichment effect including elevated growth (3 of 3 plants), liver size (2 of 3), and condition factor (1 of 3) in at least one of the months sampled. Female silverside caught near one of the three fi sh plants showed an elevated condition factor in spring, but other-wise silverside did not differ signifi cantly from all four reference sites. In a number of cases, fi sh exposed to effl uent differed from reference fi sh sampled from bays without fi sh plants but not from the local reference site, implying that the entire bay was affected either by the seafood processing plant or by some other factors. No harmful impacts such as reduced growth or survival were found in our study, possibly because the processing plants studied were relatively small and the amounts of waste discharged could be fl ushed by tides and currents and/or assimilated by the fi sh and other biota in the receiving environments.

Key words: sentinel species, seafood processing plant effl uent, enrichment effects

Introduction

Seafood processing effl uents are one of the princi-pal sources of organic input discharged into coastal waters of Atlantic Canada. In 2002, serious problems occurred at one of the largest fi sh processing plants in New Brunswick (NB) when high nutrient load-ing was associated with blooms of sea lettuce (Ulva lactuca) and depletion of dissolved oxygen in the water and sediments (Roy Consultants Ltd. et al. 2003).

Effl uents from fi sh and crustacean processing plants are generally characterized by high concentrations of nutrients, high levels of nitrogen content found as am-monia (NH3-N; 29 to 35 mg·L-1), high total suspended solids (0.26 to 125,000 mg·L-1), increased biological oxygen demand (10 to 110,000 mg·L-1) and chemical oxygen demand (496 to 140,000 mg·L-1), and by the presence of sanitizers (AMEC Earth and Environmental Limited 2003). Problems occur when the quantity of organic matter discharged exceeds the carrying capac-ity of the ecosystem and/or when its dispersion is con-strained within coastal waters. Excessive discharge of

* Corresponding author; [email protected]

organic nutrients into the marine environment can re-sult in reduction of dissolved oxygen in the water lead-ing to hypoxia or anoxia, increased ammonia concen-trations, overloads of nitrogen (N) and phosphate (P) causing excessive plant growth, variation in pH, and increased water turbidity (Tchoukanova et al. 2003).

To the best of our knowledge, no studies have exam-ined the impacts of nutrient loads emanating from sea-food processing plants on fi sh living in coastal receiving waters. However, several studies have characterized the effl uent from fi sh processing plants (Riddle and Shikaze 1973; Claggett and Wong 1974; NovaTec Consultants Inc. and EVS Consultants 1994), and numerous studies have shown that effl uents from some seafood process-ing plants fail toxicity tests, such as the 96 hour acute lethality test on threespine stickleback (Gasterosteus acu-leatus) and rainbow trout (Oncorhynchus mykiss), and microtox assays. These issues suggest possible acute and chronic toxicity problems for fi sh living in the receiving environment (Wells and Schneider 1975; NovaTec Con-sultants Inc. and EVS Consultants 1994; Jamieson 2006).

In Canada, certain land-based sources of aquatic pollution, such as pulp and paper mills and metal mines, are under strict regulations requiring them to conduct Environmental Effects Monitoring (EEM) in the aquatic

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Assessing Impacts of Seafood Plant Effluent

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environments receiving their effl uents (Lowell et al. 2003). EEM studies are conducted to determine whether exist-ing regulations adequately protect fi sh, fi sh habitat, and human uses of fi shery resources (Courtenay et al. 2002). The Canadian EEM program for pulp and paper mills includes an adult fi sh population survey that compares indices of growth, reproduction, and survival in exposed and unexposed wild fi sh populations (Lowell et al. 2003).

Standards like these have not yet been implemented for seafood processing plants but will almost certainly be considered during an ongoing reassessment of the regu-latory framework governing this industry. The present guidelines applied to Fish Processing Operations Liquid Effl uent were last promulgated in the mid 1970s (Envi-ronment Canada 1975) and specify: 1) removal of solids using a mesh screen size of 0.71 mm, 2) a well designed outfall discharging below low tide, and 3) recovery of high strength wastes associated with the fi sh meal processing (e.g., bloodwater, stickwater, pressliquor) (Environment Canada 1975). These guidelines are relatively minimal and until recently, compliance has not been monitored.

Our primary objective was to apply the adult fi sh population survey element of the Canadian Pulp and Paper Mill Effl uent Regulations EEM program to deter-mine whether fi sh chronically exposed to, and potentially feeding on, seafood plant effl uent showed signifi cant dif-ferences in survival, growth, reproduction, and energy storage relative to unexposed conspecifi cs living both within the same bays or estuaries (i.e., a local reference site), and from three other estuaries that did not receive anthropogenic effl uents (i.e., regional reference sites). We hypothesized that fi sh exposed to seafood plant ef-fl uent would be impacted by reduced growth, survival, or reproduction relative to unexposed conspecifi cs.

Fish selected for our study were the mummic-hog (Fundulus heteroclitus) and the Atlantic silverside (Menidia menidia), two of the most common and abun-dant fi sh found in coastal waters along the east coast of North America (Cadigan and Fell 1985; Ayvazian et al. 1992; Lazzari et al. 1999). Both species were found in high numbers near the outfalls of seafood processing plants in the southern Gulf of St. Lawrence (Thériault 2006). These two species also show optimal charac-teristics for being sentinel species because they can re-spond rapidly to changes in the environment due to their rapid growth rate and high fecundity (Kneib and Stiven 1978; Conover 1985; Eisler 1986; Conover and Present 1990). Furthermore, mummichog have a small home range (Lotrich 1975; Sweeney et al. 1998; Skinner et al. 2005), maximizing the probability of exposure in fi sh captured near effl uent outfalls and minimizing the po-tential of exposure in reference fi sh caught some distance away from the outfall but within the same bay or estu-ary. Atlantic silverside have a larger yearly home range than mummichog and, in some northern populations, also migrate to sea during winter months (Conover and Murawski 1982; Conover and Ross 1982; Griffi n and Valiela 2001). Nevertheless, Griffi n and Valiela (2001)

Study Sites

Fish were sampled within 15 m of the effl uent outfalls at three crustacean processing plants (Fig. 1). One proces-sor of cooked and raw lobster was located in the Scoud-ouc River estuary in Shediac (SFP = Scoudouc R. Estuary fi sh plant) and discharged approximately 568 m3 of ef-fl uent per day 15 m from shore (AMEC Earth and Envi-ronmental Limited 2003). A second processor of cooked and raw lobster and rock crab was located in Cocagne Harbour (CFP = Cocagne fi sh plant) and discharged ap-proximately 145 m3 of effl uent per day 15 m from shore (AMEC Earth and Environmental Limited 2003). The last fi sh plant was located in Baie du Village (BVFP = Baie du Village fi sh plant) and processed cooked and raw rock crab and lobster. The volume of effl uent is unknown in Baie du Village as this plant did not have a water meter, but was estimated to be intermediate to the two other plants because it processed approximately 2.3 million shellfi sh in 2004 compared with approximately 1.2 mil-lion shellfi sh in Cocagne. When in operation, from April to October, the three seafood processing plants discharge effl uent intermittently depending on the supply of shell-fi sh available for processing. Within each bay or estuary, a local reference site was selected (SRF = Scoudouc R. es-tuary reference; CRF = Cocagne reference; BVRF = Baie du Village reference) 0.5 to 2 km upstream from the out-fall at which distance we assumed there was negligible, if any, exposure to effl uent (Fig. 1). These local reference sites were also beyond the extent of the visible effl uent plume during all stages of tide. Local reference sites were chosen to have similar salinity, temperature, pH, and sediment type as the fi sh-plant sites. Three additional regional reference sites were sampled, one in each of three nearby estuaries without seafood processing plants. The three regional reference sites were selected based on similarity of habitat to the fi sh-plant sites minus the pres-ence of a plant itself and of any other anthropogenic pol-lution located within distances of the summer home range of mummichog and silverside. These regional reference sites were located at the mouth of Aboujagane/Kinnear

found that young of the year (YOY) Atlantic silverside born in Waquoit Bay, Massachusett, remained within that bay during their initial growing season from April to October. Therefore, we assumed that Atlantic silver-side are likely to remain within a single estuary during the summer months (i.e., May to September) when most fi sh processing plants operate, including those selected for this study. However, there is no way to know if the adult silverside captured in June in this study were ex-posed to seafood plant effl uent as YOY the year before. Furthermore, the Atlantic silverside is a short-lived spe-cies completing its life cycle in one year (Conover and Murawski 1982) with less than 1% of the breeding population reaching the two-year mark (Conover 1985).

Materials and Methods

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River (RF1= regional reference 1), Shediac River (RF2 = regional reference 2) and Kouchibouguac River (RF3 = regional reference 3) (Fig. 1). Fish sampled at the three regional reference sites provided a measure of natural background variance in endpoints and also verifi ed the independence of the local reference site from any infl u-ence of the fi sh plant located downstream. We adopted the sampling and analytical design of Sandström and Neuman (2003) who used both distant reference ar-eas and local reference areas to compare with a Baltic fi sh community exposed to bleached pulp mill effl uent.

Sampling of Fish

The mummichog were fi rst collected from 18 May to 2 June 2004 and the Atlantic silverside from 21 June to 5 July, targeting the period before fi rst spawning. Mum-michog and Atlantic silverside are known to be frac-tional spawners, with spawning events occurring on a semi lunar period for both the mummichog (Taylor and DiMichele 1980; Kneib 1986; Taylor 1986) and silver-side (Middaugh 1981; Conover and Kynard 1984; Hines

et al. 1985), making it diffi cult to estimate total annual reproductive effort (Leblanc and Couillard 1995). Mum-michog were sampled a second time in midseason from 6 to 14 July 2004, and a third time in the fall from 13 September to 7 October 2004. Silverside were sampled one last time in the fall from 5 to 27 October 2004.On each sampling occasion, we attempted to cap-ture 20 adult fi sh of each sex and each species per site using a 30 by 2 m beach seine with a 6 mm mesh size. Sexually mature fi sh were captured to be able to quantify reproductive indices. Sexually mature mum-michog were targeted to be equal to or over 3.5 cm in length (Fritz and Garside 1975; Kneib and Stiven 1978). Sexually mature silverside were targeted to be at least 8.0 cm (Jessop 1983; Cadigan and Fell 1985).

Length (total length for mummichog and fork length for silverside), total body weight, and gonad and liver weight for both species were measured to test if survival, growth, and reproduction differed be-tween fi sh exposed and not exposed to seafood pro-cessing plant effl uent. All fi sh were anesthetised with tricaine methanesulfonate (Western Chemical Inc.,

Fig. 1. Map showing the nine study sites on the eastern coast of New Brunswick sampled for mummichog and Atlantic silverside from May to October, 2004. RF1 = regional reference 1, RF2 = regional reference 2, RF3 = regional reference 3, SRF = Scoudouc River estuary local reference site, SFP = Scoudouc River estuary fi sh-plant site, CRF = Cocagne Harbour local reference site, CFP = Cocagne Harbour fi sh-plant site, BVRF = Baie du Village local reference site, BVFP = Baie du Village fi sh-plant site.

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Ferndale, Wash., U.S.A.; 160 mg/L for approximately 2 to 5 minutes) to determine the total length (± 0.1 cm) and the total body weight (± 0.01 g; Navigator balance, model N04120, Ohaus, Florham Park, N.J., U.S.A.). The fi sh were then sacrifi ced by severance of the spinal chord and dissected to determine the gonad and liver weights to the nearest 0.001 g (Denver Instrument bal-ance, model APX-200, Arvada, Colo., U.S.A.). Correct-ed body weight was calculated for the gonadosomatic index (GSI) by subtracting the gonad weight from the total body weight, and for liversomatic index (LSI) by subtracting the liver weight from the total body weight. GSI was estimated as (gonad weight/corrected body weight)·100. The LSI was determined as the (liver weight / corrected body weight)·100. Finally, the condition fac-tor (K) was estimated as (body weight/length3)·100.

Scales taken along the lateral line beneath the dor-sal fi n and otoliths taken from the head were removed from all fi sh for aging by North Shore Environmen-tal Services (Jon Tost, Thunder Bay, Ont.). Scales were used as the primary aging structure and otoliths were used as a back-up aging structure when scale read-ing was uncertain due to inconsistency among scales.

A total of 360 mummichog were aged in May and 360 more were aged in September. In June, 210 silver-side were aged and a subsample of 80 silverside, com-prising the longest and shortest fi sh, were aged in Octo-ber. Because 100% of silverside aged in June were one year old and 99% of the silverside population lives up to only one year, it was thought that the majority of the fi sh captured in October would be the same age. There-fore, a subsample of 80 silverside, comprising the lon-gest and the shortest fi sh (range: 5.0 to 12.1 cm), were aged in order to determine if the shortest fi sh were of age zero (i.e., YOY) or age one (i.e., adult). Out of the 80 silverside aged with scales, 71 were aged as YOY. Because yearlings were caught in such low numbers in October, only YOY fi sh identifi ed in our subsample as being less than 9.5 cm were analyzed. This fork length category comprised 90% of all silverside caught in Oc-tober (i.e., 273 silverside from a total of 302 captured).

Data Analyses and Interpretation

Fish sampled from all 9 sites (3 fi sh-plant sites, 3 local reference sites, 3 regional reference sites) were compared all at once for differences in survival (inferred from age structure), growth (weight-at-age), K, and LSI. Each of the three samples of mummichog (May, July, and September) and two samples of silverside (June and October) were analyzed separately as were male and female fi sh. Because the reproductive endpoint (GSI) varied signifi cantly with lunar cycle, we compared only samples collected on the same day which resulted in comparison of fi sh-plant sites to only their respective local reference site. Other endpoints showed no signifi cant relationship with lunar cycle. Analyses were designed to detect two response

patterns in fi sh exposed to effl uent and were deliberately conservative (i.e., risked missing an effect in order to minimize false positives) because preliminary analyses indicated high variance among reference sites. The fi rst response of interest was a nearfi eld fi sh-plant effect characterized by a signifi cantly greater, or lesser, measure in fi sh captured near the fi sh plant than fi sh from all three regional reference sites and the local reference site. For this paper, “nearfi eld” is defi ned as the immediate area of discharged effl uent where beach seining was completed, covering a surface area of approximately 225 m2. The second response of interest was a potential whole fi sh-plant bay effect, found when the fi sh caught near a seafood processing plant differed from the three regional reference sites but not from the local reference site. In such a case, our interpretation was that the whole fi sh-plant bay was different from other unimpacted bays, though we could not say whether this was due to the local seafood processing plant, some other factor, or a combination of factors. No direct measurements of the effl uent concentration, composition, or dispersion were made in the fi sh-plant bays, making it diffi cult for us to confi rm that absolutely no effl uent reached the local reference site. Furthermore, no measurements of the degree of movement of either sentinel species were made. The age at capture, indicating survival, was analyzed with a one-way ANOVA. The growth (i.e., weight-at-age) among the nine sites was analyzed using analysis of covariance (ANCOVA) with age as the covariate. Body weight alone was used to infer growth when fi sh were all of the same age, such as the silverside which were all age one in June and age zero (YOY) in October. The comparison of condition factor among the nine sites was made using ANCOVA with body weight as the dependent variable and length as the covariate. The LSI was evaluated among the nine sites using ANCOVA with liver weight as the dependent variable and adjusted body weight as the covariate. The GSI was evaluated between the fi sh-plant sites and local reference sites using ANCOVA with gonad weight as the dependent variable and adjusted body weight as the covariate. Before performing ANCOVAs, colinearity was tested using a general linear model. When an interaction between sites and covariate precluded the use of an ANCOVA, the interaction was removed by restricting the ANCOVA to a narrow range of the covariate. GSI calculated late in September for the mummichog and in October for the silverside were only analyzed when the gonad weight was over 1%; otherwise they were considered immature (Environment Canada 2005) and not analyzed. Data were verifi ed for homogeneity of variance using the Fmax test, and for normality with probability plots prior to analysis. Logarithmic transformations were used if data did not meet these assumptions. When signifi cant differences were found among sites, a Tukey multiple comparison test was employed. Analyses were performed using SYSTAT 11 (SPSS, Chicago, Ill., U.S.A.). The level of signifi cance was set at P < 0.05.


176

Results

Mummichog

Growth. Growth, inferred from weight-at-age, differed signifi cantly among sites for male and female mummi-chog caught in May (male F8,163 = 17.21, P < 0.01; female F8,170 = 29.12, P < 0.01) and September (male F7,105 = 6.96, P < 0.01; female F8,170 = 23.51, P < 0.01). In July, no growth was calculated since mummichog were not aged.

In the Scoudouc River estuary, male and female mummichog caught in May demonstrated a nearfi eld fi sh-plant effect; growth was signifi cantly higher near the fi sh-plant site than near the three regional reference sites and the local reference site (Table 1). No nearfi eld fi sh-plant effect or potential whole fi sh-plant bay ef-fect was observed in either sex in September (Table 1).

In Cocagne Harbour, female mummichog caught in May and September near the processing plant had signifi cantly higher growth than females from the re-gional reference sites and the local reference site (CRF), supporting a nearfi eld fi sh-plant effect (Table 1). Male mummichog caught in Cocagne Harbour did not show any fi sh-plant effect or potential whole fi sh-plant bay effect in either month sampled (Table 1).

In Baie du Village, female mummichog caught near the fi sh plant in May had signifi cantly higher growth than females from the regional reference sites, but did not dif-fer from females captured from the local reference site (BVRF) (Table 1). This response could indicate that the local reference site was affected by the fi sh plant, by oth-er anthropogenic factors, or by a combination of factors. In September, only females showed a nearfi eld fi sh-plant

effect; growth was signifi cantly higher near the fi sh plant than the regional reference sites and the local reference site. Male mummichog caught in September at BVFP had higher growth than males captured at the two regional reference sites sampled (i.e. RF1, RF2) but not the local reference site (i.e. BVRF), suggesting that the entire bay could be affected by the fi sh plant or other factors (Table 1).

Survival. Survival was calculated as the difference in mean age among all nine sites sampled. The mummichog were only aged in May and September, months during which age differed signifi cantly for both sexes among the sites (male, May F8,171 = 8.67, P < 0.01; female, May F8,171 = 8.23, P < 0.01; male, September F8,171 = 24.42, P < 0.01; female, September F8,171 = 28.94, P < 0.01). How-ever, there was no evidence of a nearfi eld fi sh-plant effect on survival at any of the sites for either sex or months sampled. Mummichog living near processing plants were neither signifi cantly younger nor older than conspecifi cs at all three regional reference sites and the local reference site in either May or September (Table 1). In May, average age was between two and three years old at all sites. In Sep-tember, the mean age varied between 1 and 2.5 years old.

Condition factor (K). Condition factor for male and female mummichog differed signifi cantly among the nine sites in May (male, F8,170 = 11.96, P < 0.01; female, F8,164 = 29.43, P < 0.01), July (male, F8,170 = 12.22, P < 0.01; female, F8,169 = 31.01, P < 0.01) and September (male, F8,170 = 6.95, P < 0.01; female, F8,170 = 8.94, P < 0.01). In May, female mummichog caught at BVFP

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and BVRF had signifi cantly higher K than at all three regional reference sites (Table 1). However, the K did not differ signifi cantly between the fi sh-plant site and the local reference site in Baie du Village, suggesting that the whole bay was potentially affected by either the processing plant or other factors. In July, male and fe-male mummichog living near the fi sh plant in Baie du Village had signifi cantly greater K values than females from the three regional reference sites and the local ref-erence site, consistent with a nearfi eld fi sh-plant effect (Table 1). No other nearfi eld fi sh-plant effects or poten-tial whole fi sh-plant bay effects on K were found in either Scoudouc River estuary or Cocagne Harbour (Table 1).

Liversomatic Index (LSI). The liversomatic index for male and female mummichog differed signifi cantly among the sites in May (male, F8,170 = 15.87, P < 0.01; female, F8,170 = 16.26, P < 0.01), July (male, F8,170 = 12.69, P < 0.01; female, F8,169 = 15.98, P < 0.01), and September (male, F8,170 = 8.64, P < 0.01; female, F8,170 = 17.70, P < 0.01).

In Scoudouc R. estuary, male and female mummichog caught near the fi sh plant in September showed signifi -cantly higher LSI than mummichog at the three regional reference sites but not at the local reference site suggesting a potential whole fi sh-plant bay effect, or that the local reference site was affected by other anthropogenic fac-tors (Table 1). No other nearfi eld fi sh-plant effect on the LSI was found in May or July in Scoudouc River estuary.

In Cocagne Harbour, the male mummichog caught near the fi sh plant in July had signifi cantly greater LSI than those from the three regional refer-ence sites and the local reference site, suggesting a nearfi eld fi sh-plant effect (Table 1). No other near-fi eld fi sh-plant effect was found in Cocagne Harbour.

In Baie du Village, a nearfi eld fi sh-plant effect was demonstrated. Male and female mummichog caught near the processing plant in May, July, and Septem-ber had signifi cantly greater LSI than fi sh from the three regional reference sites and from the local refer-ence site except for males in September, which showed a potential whole fi sh-plant bay effect since the LSI did not differ between BVFP and BVRF (Table 1).

Reproduction (GSI). Regression analyses indicated that male and female mummichog captured in May showed a signifi cant relationship between the gonad size and the number of days before the full moon (male, R2 = 0.67, F1,7 = 14.09, P < 0.01; female, R2 = 0.77, F1,7 = 23.86, P < 0.01). The same relationship between the gonad weight and lunar cycle was observed in July for both male and female mummichog (male, R2 = 0.61, F1,7 = 10.95 P = 0.01; female, R2 = 0.46, F1,7 = 6.05, P = 0.04). In September, no relationship between the go-nad weight and the lunar cycle was found, most prob-ably because mummichog were fi nished spawning by then (Scott and Scott 1988). This analysis showed that GSI was greatly infl uenced by the lunar cycle during the spawning period and that only sites sampled on the same day should be compared.

In the Scoudouc River estuary, GSI was signifi cantly higher near the seafood processing plant than at the local reference site in May for the males but not for the females (males, F1,37 = 4.28, P = 0.04). In July and September, male mummichog caught at the exposed site had signifi cantly lower GSI than males from the local reference site (male, F1,37 = 11.63, P < 0.01; male, F1,37 = 16.41, P < 0.01, respectively), and female showed signifi cantly lower GSI but only in September (female, F1,37 = 21.01, P < 0.01). No other signifi cant differences were found in Scoudouc River estuary for the GSI. In Cocagne Harbour, female mummichog had signifi cantly lower GSI near the seafood processing plant in July than females from the local reference site (female, F1,36 = 8.07, P < 0.01). No other signifi cant differences were found in Cocagne Harbour for the GSI. In Baie du Village, female mummichog captured near the seafood processing plant had signifi cantly lower GSI in May than females from the local reference site (female, F1,37 = 5.67, P = 0.02) and no signifi cant difference was found for the male mummichog captured in May. Signifi cantly higher GSI was seen for male mummichog caught in July and for female mummichog caught in September (male, F1,37 = 18.89, P < 0.01; female, F1,37 = 9.88, P < 0.01).

Atlantic Silverside

Growth. Signifi cant differences in body weight for male and female silverside were found among the sites in June (male, F5,99 = 8.33, P < 0.01; female, F5,112 = 3.60, P < 0.01) and October (male, F7,137 = 7.42, P < 0.01; female, F7,120 = 4.20, P < 0.01).

Male Atlantic silverside showed signifi cantly lower growth near the Scoudouc fi sh plant in October com-pared to males from all three regional reference sites (Table 2). No difference between SFP and SRF could be calculated since no silverside were caught at the lo-cal reference site (SRF) in October. No other evidence of a nearfi eld fi sh-plant effect was observed for the sil-verside of Scoudouc River estuary, Cocagne Harbour, or Baie du Village in either June or October (Table 2).

Survival. Survival could not be calculated for silverside because they were either all one-year-old in June or domin-ated by YOY aged 0 in October. However, silverside were caught at the fi sh-plant sites in both months sampled, argu-ing against both acute toxicity and avoidance behaviour.

Condition factor (K). The condition factor for adult male and female silverside captured in June differed signifi cantly among the sites (male, F5,98 = 18.33, P < 0.01; female, F5,111 = 12.66, P < 0.01). In October, K for YOY male silverside was not signifi cantly different among the sites (male, F7,129 = 1.25, P = 0.28) (Table 2), and differed so marginally for the females (female, F7,119 = 2.24, P = 0.03) that no signifi cant differences among sites could be detected by the Tukey test (Table 2).


178

In Scoudouc River estuary, condition factor could not be analyzed in June because no silverside were caught in this estuary at that time. In October, no sig-nifi cant differences were shown between the fi sh captured near the seafood processing plant and the fi sh from the three regional reference sites (Table 2).

In Cocagne Harbour, male silverside caught in June had signifi cantly higher K than males from the two regional reference sites sampled (RF2, RF3), but did not differ from males captured at the local ref-erence site suggesting a potential whole bay eleva-tion of K (Table 2). No other evidence of a nearfi eld fi sh-plant effect was observed in June or October.

In Baie du Village, female silverside caught in June near the fi sh plant had a signifi cantly higher K than fe-males from the regional reference sites sampled (RF2, RF3) and the local reference site, suggesting a near-fi eld fi sh-plant effect. Male silverside caught in June near the fi sh plant showed signifi cantly higher K than males from the two regional reference sites sampled but did not differ from those from the local reference site, suggesting a whole bay elevation of K (Table 2).

Liversomatic Index (LSI). The liversomatic index for male and female Atlantic silverside differed signifi cant-ly among the sites in June (male, F5,98 = 5.24, P < 0.01; female, F5,111 = 9.83, P < 0.01) and in October (male, F7,135 = 4.05, P < 0.01; female, F7,119 = 5.18, P < 0.01).

In Baie du Village, female silverside caught near the fi sh plant in June had signifi cantly higher LSI than females from the regional reference sites sampled (RF2, RF3), but did not differ from fi sh from the local reference site (BVRF) (Table 2), suggesting the whole bay was poten-tially affected by the fi sh plant or other factors. No other

patterns consistent with either a nearfi eld or a potential whole fi sh-plant bay effect on liver size were observed in either sex at any of the three bays with fi sh plants.

Reproduction (GSI). Silverside reproduction was ana-lyzed the same way as for mummichog because of the signifi cant relationship found between the gonad size and the number of days before a full moon. The GSI levels were not calculated for October because only YOY were found in suffi cient numbers to sample and their gonad weights were under 1% of their total body weight and con-sidered sexually immature (Environment Canada 2005).

In Scoudouc River estuary, no silverside were caught at the local reference site. Therefore, the fi sh located near the fi sh plant in Scoudouc R. estu-ary could not be compared to the local reference site.

In Cocagne Harbour, the female silverside caught at the local reference site had signifi cantly higher GSI than the female fi sh caught near the fi sh plant in Cocagne (fe-male, F1,37 = 19.69, P < 0.01). The male GSI did not differ between the local reference site and the fi sh-plant site.

In Baie du Village, male and female GSI did not differ between the fi sh-plant site and the local reference site within the same bay.

Discussion

Fish Response to Effluent

Mummichog and Atlantic silverside collected within the effl uent plumes of three seafood processing plants from May to October 2004 showed no evidence of reduced growth, survival, or reproduction relative to unexposed or less exposed conspecifi cs. What they did show was

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evidence of nutrient enrichment. Growth rate, condition factor, and LSI of exposed fi sh were often elevated relative to fi sh collected from reference sites within and beyond the fi sh-plant bay. We hypothesize that these increases in growth and energy reserves near processing plants are a response to nutrients in the discharge effl uent. It should be noted that effl uents from these seafood plants added no major heat to the water which might have elevated growth (Thériault 2006). However, it is not clear whether fi sh are ingesting the pieces of lobster and crab which are evident in the effl uent, or are benefi ting indirectly by feeding on other consumers of the effl uent nutrients as has been reported with sewage effl uents (Otway et al. 1996). Future research could include analyses of gut contents or of stable isotopes to verify if fi sh living in the receiving environment of seafood processing plant ingest effl uent. Other studies of the littoral fi sh communities living in the St. Lawrence River showed that sewage-enriched sites had an increased predominance of larger fi sh (deBruyn et al. 2002), and that primary and secondary consumers revealed a substantial uptake of sewage-derived resources within the plume, up to 10 km from the sewage outfall (deBruyn et al. 2003).

The quantity, quality, and accessibility of food are major habitat characteristics affecting health indices of fi sh (Gibbons and Munkittrick 1994). Increased food availability may allow fi sh to allocate resources to en-ergy storage (i.e., higher lipid storage and condition fac-tor) and to increased growth and reproduction (Adams et al. 1992; Gibbons and Munkittrick 1994). Increased availability of resources can occur for two reasons: 1) a decrease in population size due to the removal of adult fi sh by exploitation (Colby and Nepszy 1981) or due to a recruitment failure which has been documented in a population of fi sh exposed to pulp and paper mill effl u-ent (Adams et al. 1992); and 2) an increase in the amount of available habitat and food resources (Trippel and Harvey 1987; Munkittrick and Dixon 1989). We have documented that there were actually more mummichog and silverside, including YOY, near these fi sh plants than elsewhere within these estuaries or within other estuaries (Thériault 2006). These results argue against a decrease in population size near fi sh plants, but rather support a greater availability of food, which could attract certain fi sh species. Tober et al. (2000) demonstrated that abun-dance of Fundulus heteroclitus was greater in estuaries with higher nitrogen loading rates. However, growth rates of F. heteroclitus obtained from growth rings on scales and otoliths did not vary among estuaries of Wa-quoit Bay, Mass., that were subject to different rates of land-derived nitrogen loading (Tober et al. 2000).

The mummichog caught near the crustacean pro-cessing plants demonstrated a fi sh-plant effect in at least one endpoint measured during one or more months sampled at all three sites. Nearfi eld fi sh-plant effects were shown eight times in Baie du Village, three times in Cocagne Harbour, and twice in Scoudouc River es-tuary. Potential whole fi sh-plant bay effects were found four times in Baie du Village, twice in Scoudouc River

estuary, and never in Cocagne Harbour. All 19 cases were consistent with a nearfi eld or potential whole bay nutrient enrichment effect showing increased growth, K, or LSI near the seafood processing plants.

Baie du Village was the site which most often showed a nearfi eld fi sh-plant effect. A consistent response was in-creased LSI in mummichog near the fi sh plant on all three sampling occasions. This increased liver weight could in-dicate a nutrient effect or a toxic response. Elevated LSI in combination with elevated condition factor is gener-ally associated with a nutrient effect, together with an increase in other endpoints such as growth and gonad weight (Lowell et al. 2005). Chemical toxicity may oc-casionally lead to increased liver size, as part of the de-toxifi cation mechanism, and a decrease in the other end-points (Lowell et al. 2005). Because elevated LSI in fi sh living near the processing plant was coupled with higher K for both males and females in July and higher growth for females in September, we conclude that it was a nutri-ent effect rather than a toxic response. This is an impor-tant distinction because both responses might be elicited by fi sh plant effl uent which contains chlorinated cleans-ers and disinfectants (Morry et al. 2003; Jamieson 2006).

In Cocagne Harbour, evidence of a nutri-ent enrichment effect was that female mummichog caught near the processing plant had higher growth in May and September, and male mummichog had higher LSI in July compared with fi sh from the re-gional reference sites and the local reference site.

In Scoudouc River estuary, the evidence of an enrich-ment effect was found in May when male and female mummichog living near the crustacean processing plant showed increased growth compared with fi sh from the regional and local reference sites. In September, male and female mummichog caught near the Scoudouc processing plant showed signifi cantly greater LSI than those from the three regional reference sites but did not differ from fi sh captured at the local reference site (SRF). Such a re-sponse could indicate that mummichog in the entire estu-ary were affected by the processing plant, either because effl uent was being carried upstream on fl ood tides or be-cause mummichog were moving between the local refer-ence site and the fi sh-plant site in September. Alternatively, some other source of nutrients might have been affecting the whole estuary such as agricultural runoff, or input of sewage generated by a secondary treatment sewage plant located 7 km upstream or by a primary treatment sew-age plant located 18.7 km upstream in Scoudouc River.

Nearfi eld fi sh-plant effects were found less often with the silverside than the mummichog. The one and only nearfi eld fi sh-plant effect, as defi ned in our study, was found in Baie du Village where female silverside cap-tured near the fi sh plant had higher K than females from the regional and local reference sites in June. Also at this site in June, an increased K for the male silverside and an increased LSI for female silverside relative to fi sh from the regional reference sites but not local reference site (BVRF) suggested that the entire bay could be affected


180

by the crustacean processing plant or another factor such as a suspended bag oyster aquaculture farm located in the same bay approximately 200 m away from the outfall. Furthermore, silverside did not show increased growth near the fi sh plants and, in one sample, showed a decrease: male silverside living near SFP in October had a smaller body weight than conspecifi cs sampled in three other regional bays. No difference between SFP and SRF could be calculated because no silverside were caught at the local reference site (SRF) in Octo-ber. Therefore, it is unclear whether the reduced growth was restricted to the fi sh-plant site or was a more gen-eral characteristic of the entire Scoudouc estuary. This was the only observation suggesting reduced growth at a fi sh plant, and may have resulted from factors other than a direct effect of effl uent. Young-of-the-year silver-side sampled near the seafood processing plant in Scou-douc River estuary in October may have been affected by increased competition for food due to the high abun-dance of fauna near the outfall (Thériault et al. 2006).

The silverside appeared to be a less suitable sentinel species than the mummichog for studies of point source impacts for a number of reasons. First, unlike mummic-hog, they were not found in suffi cient numbers at every site. Silverside are also a short-lived species (Conover and Murawski 1982; Conover 1985) and so cannot demon-strate a cumulative effect over a number of years as can the mummichog which can live up to fi ve years (Eisler 1986). Thirdly and perhaps most importantly for ex-plaining the lack of effects observed in the present study, silverside appear to move more extensively than the sedentary mummichog (Skinner et al. 2005) within the reproductive season, and migrate offshore for overwin-tering (Conover and Murawski 1982; Conover and Ross 1982; Griffi n and Valiela 2001). Silverside may there-fore be less exposed than mummichog to point source impacts such as fi sh plant effl uents, and may be more likely to move between point sources of interest and local reference sites that are relatively nearby as in our study.

Finally, the GSI comparisons between the mummic-hog captured near seafood processing plants and their respective local reference site showed no signifi cant dif-ferences 10 out of 18 times. When a signifi cant difference occurred, it was almost evenly split between a higher and lower GSI at the fi sh-plant site than at the local reference site (3 and 5 times respectively). For the silverside, only 1 of 4 comparisons showed a signifi cantly lower GSI be-tween the fi sh-plant site and the local reference site for female silverside in Cocagne Harbour sampled in June. Therefore, there was no compelling evidence of a fi sh-plant effect on reproduction of fi sh living in these estuar-ies. That said, our sampling design was not well suited to quantify reproductive investment or expenditure in these fractional spawners. More intense research, sampling fi sh at a higher rate living near seafood plant effl uent, is need-ed to understand this response and confi rm that the de-crease in GSI is defi nitely not related to fi sh-plant effl uent.

Methodological Considerations

When indices of energy storage, growth, or repro-duction differed between bays with and without fi shplants and did not differ between the two sites sampled within the fi sh-plant bay, the difference was always consistent with nutrient enrichment in the bays withfi sh plants (6 of 6 comparisons for mummichog and 3 of 3 comparisons for silverside). However, this cannot be interpreted as evidence that nutrients from the fi sh plant affected the whole bay because of a pervasive, and largely unavoidable, confounding factor in the study de-sign. The bays with fi sh plants that were studied in this survey also had other potential sources of nutrient en-richment such as agricultural runoff and municipal and septic system wastes (Scoudouc), municipal wastes and a boat marina (Cocagne), and septic system wastes and local concentration of nutrients by cultured oysters (Baie du Village). By contrast, the three regional reference sites were selected for their lack, not only of fi sh plants, but also of any other obvious anthropogenic inputs. There-fore, indices of elevated nutrient storage and/or expen-diture in the local reference fi sh of Scoudouc, Cocagne, and Baie du Village probably do refl ect nutrient enrich-ment in these estuaries, but the degree to which that en-richment was caused by the local fi sh plant is unknown.

In addition to the bays differing in anthropogenic activities and impacts, they differed in mummichog bi-ology as has been reported previously for this species in adjacent estuaries (Leamon et al. 2000). Dynamics of mummichog reproduction, including onset, dura-tion, intensity, and cessation, may have differed among bays, which may in turn affect not only indices of re-production such as GSI, but also indices of growth (weight-at-age) and energy storage (K, LSI). Such dif-ferences among sites have been reported previously for mummichog within the southern Gulf of St. Lawrence (Leblanc and Couillard 1995; Leblanc et al. 1997).

Multiple spawners, like mummichog, present chal-lenges for quantifying reproduction and related end-points that single spawners do not. There is some evi-dence from our study, and better evidence from Leblanc et al. (1997), that timing of reproduction may vary not only between estuaries but also among sites within the same estuary, complicating the comparisons made for the GSI index among the sites. For example, mummichog from the Miramichi estuary living near a bleached kraft pulp and paper mill showed a delayed onset of spawn-ing compared with fi sh living downstream (Leblanc et al. 1997). Once begun, though, investment in reproduc-tion was greater in the upstream mummichog so that the total reproductive output (GSI, fecundity, and breeding effort) was greater than that of the downstream mum-michog (Leblanc et al. 1997). This pattern was only ob-served because of repeated, frequent sampling; no single sampling would have accurately characterized reproduc-tive output in these fi sh and the impact of exposure to pulp mill effl uent. Therefore, in addition to sampling

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multiple reference sites within a bay or estuary, fractional spawners require sampling at frequent intervals during the spawning season. Potential asynchrony in repro-duction among and within estuaries greatly weakenedcomparisons of GSI results in this study because only one reference site was sampled within the exposed bay, and fi sh were only sampled twice during the reproduc-tive period for mummichog (i.e., May to July) and once during the silverside reproductive period (i.e., June).

In addition to frequent sampling and multiple refer-ence sites, it is important that, when sampling sites are to be compared, they be sampled simultaneously. One clear pattern observed in our GSI data was a strong lunar cycle of increasing gonad size as the full moon was approached during the beginning of the spawning season for both spe-cies. By analyzing the sites that were sampled only on the same day, we were able to eliminate this source of variance.

Because environmental conditions and fi sh biol-ogy may differ among bays, our interpretation frame-work for the present study was conservative and may have missed some fi sh-plant effects. For example, female silverside sampled in June showed higher growth (i.e., weight) at the Baie du Village fi sh-plant site than at the local reference site (BVRF), consistent with a nutrient enrichment effect. However, fi sh from one of the two regional reference sites sampled showed simi-larly high growth as fi sh from the fi sh-plant site, so we concluded that there was no compelling evidence of a fi sh-plant effect on growth. A less parsimonious expla-nation could be that fi sh in Baie du Village as a whole have lower growth than some other estuaries and that this effect was being mitigated by the fi sh plant. The pos-sibility of bay-wide differences in endpoints would argue for comparing a potentially impacted site to a number of reference sites within the same bay rather than from different bays. Evaluating the potential for caging senti-nel species in the effl uent and local reference site could also address potential fi sh residency issues within a bay.

Nearfi eld, or potential whole bay, effects of fi sh plant effl uents on fi sh were sometimes seen in one sampling period at a given site, but not in subsequent periods. For example, male and female mummichog in Scoudouc R. estuary exhibited a local fi sh-plant growth effect in May but not in September. Female and male mummichog in Baie du Village showed increased condition factor at the fi sh plant in July but not in September. This could be ex-plained by the fact that these small seafood processing plants rely on local fi sheries for product and do not nec-essarily operate every day between May and September. Therefore, some receiving environments and fauna living within them may be more affected by effl uent at certain times than others explaining in part why cumulative effects may not be shown consistently in fi sh captured later in the season. As well, fi sh may move around more in some months than others, which could make it dif-fi cult to detect any distinction between the fi sh-plant site and the local reference site, or could even completely re-move any effect if immigrants replace previous residents.

In our study, the organisms living in the waters receiving fi sh plant effl uent seemed to have the capac-ity to assimilate the amount of waste coming from the processing plants, or, at least the wastes that were notfl ushed from the bay by tides and currents. The waste effl uent did not show obvious negative impacts on fi sh populations, such as a delayed gonadal development, re-cruitment failure, lower fecundity, or metabolic disrup-tion, as has been reported in fi sh living near some pulp and paper mills (Munkittrick et al. 1991; 1994). How-ever, the results of this study may not be easily extrapo-lated to larger processing plants or different process lines because the effects of effl uent discharged may vary with volume of effl uent, the type of species processed, tech-nologies used to treat the effl uent, and dilution rates in the receiving environment (AMEC Earth and Environ-mental Limited 2003; Morry et al. 2003). Larger seafood processing plants may discharge wastes beyond the ca-pacity of the environment to absorb, leading to serious problems, such as the kind of eutrophication observed in Lameque Bay, N.B. (Morry et al. 2003; Roy Consultants et al. 2003). Nevertheless, the results of the present study will prove helpful in designing appropriate surveillance and monitoring for these more challenging situations.

Acknowledgments

We would like to thank Monica Boudreau, the Shediac Bay Watershed Association, the “Pays de Cocagne” Sus-tainable Development Group, the Richiboucto River Association and the numerous others that helped with the fi eld work. Thanks to G. Maillet, T. Burns, A. King and N. LeBlanc for their collaboration while sampling around their seafood processing plant. We are also grateful to Jon Tost from North Shore Environmental Services for aging the fi sh. This study was funded by DFO, the University of Moncton merit scholarship and the Sustainability Scholarship awarded by the South-ern Gulf of St. Lawrence Coalition on Sustainability.

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