Growth and Condition Index of Mussel Mytilus Galloprovincialis in Experimental Integrated Aquaculture

Aquaculture Research, 2007, 38, 1714^1720 doi:10.1111/j.1365-2109.2007.01840.x

Growth and condition index of mussel Mytilus galloprovincialis in experimental integrated aquaculture

Melita Peharda1, Ivan %upan2, Lav Bavc›evicŁ3, Anamarija FrankicŁ4 & Tin Klanjsflc›ek5 1Institute of Oceanography and Fisheries, Setalisfl te Ivana Mesfl trovicŁ a, Split, Croatia 2Convento Albamaris, Augusta Senoe, Biograd, Croatia 3Croatian Agriculture Extension Institute, Ivana Ma&uranicŁ a, Zadar, Croatia 4University of Massachusetts Boston, EEOS Department, Boston, MA, USA 5Ru:er Bosfl kovicŁ Institute, Bijenic› ka, Zagreb, Croatia

Correspondence: M Peharda, Institute of Oceanography and Fisheries, Setalis› te Ivana Mes› trovicŁ a 63, 21000 Split, Croatia. E-mail: [email protected]

Abstract Introduction Integrating mussel and ¢n¢sh aquaculture has been Simultaneous culture of several species in the same recognized as a way to increase pro¢ts and decrease water body with the objective of optimizing the use environmental impacts of ¢n¢sh aquaculture, but of space and nutrients is termed integrated aquacul- not enough is known about the e¡ects of ¢n¢sh aqua- ture, polyculture or co-culture. Integrated aquacul- culture on mussel growth. Here we present a pilot ture is traditionally used in the fresh-water pond study aimed at determining how distance from ¢n- aquaculture (Marcel 1990; Landau 1992). Recently, ¢sh aquaculture a¡ects mussel growth. To this end, potential for integration of marine ¢sh and bivalve we measured growth and condition index of mussel aquaculture is being assessed (Jones & Iwama 1991; (Mytilus galloprovincialis) at three di¡erent distances Taylor, Jamieson & Carefoot 1992; Stirling & Okumus (0, 60 and 700 m) from ¢n¢sh aquaculture in the 1995; Mazzola, Favaloro & SaraØ1999; Mazzola & SaraØ eastern Adriatic Sea. There was a statistically signi- 2001; Cheshuk, Purser & Quintana 2003; Gao, Shin, ¢cant di¡erence in growth of tagged mussels with Lin, Chen & Cheung 2006; Martinez-Cordova & Mar- respect to site. Average measured lengths of mussels tinez-Porchas 2006). at sites 1, 2 and 3 after the 10 months of the experi- Croatia’s aquaculture production in 2005 was ment were 57.60, 62.73 and 58.66 mm. Mussels grew 6425 t of marine ¢sh and 2600 t of bivalves (Jahutka, fastest from March to May, and slowest from July to Misﬂ ura & SuicŁ 2006). Only a small fraction of this September, regardless of their position. Condition production is from integrated aquaculture. The stra- index showed spatial and temporal variations tegic goal of the Republic of Croatia is to reach an an- with higher values during fall and winter ( 23), nual production of 10000 t of ¢sh and 20 000 t of and lower values during spring and summer bivalves from aquaculture operations in this decade ( 20). Our results show that production cycle in (KatavicŁ ,Bo&anicŁ , CetinicŁ , Dujmusﬂ icŁ , FilicŁ ,Kuc› icŁ ,Vo- areas traditionally considered suboptimal for aqua- dopija & Vrgoc› 2002). Meeting this goal requires culture can be equivalent to the cycle in areas either expanding areas devoted to aquaculture or a traditionally considered optimal for mussel aquacul- shift towards integrated aquaculture. ture if mussel aquaculture is integrated with ¢n¢sh Expanding aquaculture operations in coastal aquaculture. waters is restricted due to con£icts with other human activities in the coastal zone. Large aquaculture op- Keywords: integrated aquaculture, polyculture, erations reduce the area available for other activities, mussel, Adriatic Sea while in£ux of organic matter into the water column

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(eutrophication) resulting from ¢sh farming can have producing an additional 80^90 tons of ¢sh. During unacceptable adverse impacts on the oligotrophic the experiment, ¢sh were fed with extracted pellets community of the Adriatic Sea. Hence, integrated produced by BioMar or Aller. Temperature was mea- aquaculture has been suggested as a preferred option sured once a week, while mussels were sampled (Frankic & Hershner 2003). around 15th of the month. M. galloprovincialis from In a bivalve and ¢sh-integrated aquaculture, ¢sh fouling communities found at the ¢sh aquaculture aquaculture provides organic matter for bivalves to structures was used to set up the experiment. feed on (Chan1993; Stickney & McVey 2002). Bivalves For growth experiment, shell lengths (N 5 297) remove the organic matter from the water, thus redu- were measured with vernier calipers to the nearest cing the environmental impact of ¢sh aquaculture 0.1mm and shells were individually marked with (Naylor, Goldburg, Primavera, Kautsky, Beveridge, mollusc tags (HALL PRINT, Victor Harbour, South Clay, Folke, Lubchenco, Mooney & Troell 2000). Such Australia, Australia) in November 2005. The mean a con¢guration increases biomass production while initial length of mussels used in growth experiment decreasing eutrophication of the water column was 39.4 1.8 mm and they were six to eight (Brooks, Mahnken & Nash 2002). months old. Marked shells were divided into three Mussel Mytilus galloprovincialis Lamarch 1819 is a samples, placed in square-shaped plastic baskets natural choice for a bivalve species in integrated (35 55 cm) commonly used in the Adriatic for oy- aquaculture in the Adriatic Sea because it is native ster aquaculture and suspended at 2.5 m depth at to the region, fast growing and commercially viable. three di¡erent sites. Site 1 was immediately neigh- Mussel seed is collected in wild by ropes and after bouring ¢sh cages, site 2 was 60 m away from the about 6 months mussels are transferred to nylon cages and site 3 was 700 m away from the cages. mesh nets hanging from lines. Production cycle is be- After 2 months, mussels were removed from the tween year and a half and two years (Hrs-Brenko & water, their lengths were measured and they were FilicŁ 1973; BenovicŁ 1997; Jasprica, CaricŁ , Bolotin & Ru- suspended again in the water column. This proce- denjak-Lukenda1997). dure was repeated every 2 months on the same mus- Previous studies have demonstrated that in£uence sels. A total of 33 (11%) mussels were found empty of ¢sh cages is localized (Magill,Thetmeyer & Cromey during the experiment and manyof them had preda- 2006; MatijevicŁ ,Kusﬂ pilicŁ &BaricŁ 2006) and it is the tion marks on their shells, which we presume were question, especially in oligotrophic environment, at made by sea bream. Majority of them died before which distance from ¢sh cages mussel culture needs March 2006. In addition, tags have been missing to be placed and what quantities of mussels can be from 86 mussels (29%) and these disappeared in dif- supported by the ¢sh farm. Here we present the pilot ferent phases of the experiment. Because of poach- study dealing with determining the viability of bi- ing, mussels were not recovered from site 2 in valve and the ¢sh integrated aquaculture and opti- November 2006. Only mussels that survived the mal placement of mussels relative to ¢sh cages. We whole experiment were used in the analysis, that is analysed spatial and temporal di¡erences in M. gallo- 77 mussels at site1,55 at site 2 and 44 at site 3. provincialis shell growth and condition index, and For condition index analyses, mussels were kept in discuss implications of our ¢ndings for integrated nylon mesh nets (22 mm opening) at the above-de- aquaculture and future experiments aimed at under- scribed sites.The base population used for measuring standing the optimal placement of mussel relative to condition index was about 700 animals at each site. ¢sh cages. Each month 30 mussels were removed from each site and frozen for later laboratory analysis. Condition index was determined as the ratio between cooked meat weight and the sum of cooked meat weight and Material and methods shell weight according to Davenport and Chen (1987). The pilot study was carried out from August 2005 to Before the analysis data were tested for homogene- November 2006 on an aquaculture farm of sea bass ity of variance, growth increments were analysed Dicentrarchus labrax (Linnaeus, 1758) and sea bream using repeated measures ANOVA on animals that sur- Sparus aurata (Linnaeus, 1758) located on the south vived the experiment. With respect to condition in- side of Pasﬂ man island, middle Adriatic Sea (Fig. 1). dex, one-way analysis of variance was applied for This farm produces about 90^100tons of ¢sh an- data analysis when variances were homogeneous, nually. There are also two smaller nearby farms while non-parametric Kruskal^Wallis test was used

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Figure 1 Map of the studyarea: (a) Adriatic Sea, (b) area around Pasﬂ man island, (c) Location of ¢sh farm and sampling sites. for analysis of data that did not have homogenous growth was observed for mussels placed 60 m away variances. Tukey and Mann^Whitney tests were ap- from the ¢sh cages at site 2 (x 5 23.46 4.25 mm/2 plied for post hoc comparison respectively.Length-at- months, N 5 55), while mussels placed at ¢sh cages age data were analysed using the FiSAT II statistical (x 518.26 4.59 mm/2 months, N 5 78) and those package (v.1.2.2.) and the asymptotic length (La)and placed at site 3 placed 700 m away from the ¢sh cages the curvature parameter (k) parameters of the Berta- (x 519.24 5.21 mm/2 months, N 5 54) grew k(t t0) lan¡y growth equation Lt 5 L1 (1^e ) were slower. Average measured lengths of mussels at sites determined separately for each study site (Gayanilo, 1, 2 and 3 after the 10 months of experiment were Sparre & Pauly 2005). 57.60,62.73 and 58.66 mm.With respect to length fre- quency distribution and site, 42%, 80% and 53% of mussels were above the commercial size of 6 cm as Results de¢ned in the O⁄cial Gazzet (96/2005). After 12 months, 59% of mussels at site 1 and 70% of mussels Temperature at site 3 were above the commercial size. As mussels Temperature at ¢sh aquaculture site ranged from used for the start of the experiment were 6^8 months 10.4 1C(February2006)to24.01C(August2006). old, we conclude that the production cycle of mussels Temperature was below 13 1C in a period from Janu- placed at site 2 is between 18 and 20 months, while ary to March, while values above 21 1C were recorded the production cycle of those placed at sites 1 and 3 in a summer period, from July to September (Fig. 2). is around 24 months. The highest growth rates were recorded in a period from March to May (x 5 6.4 2.2 mm/2 months, N 5 220), while the mussels grew slowest from July Growth rate to September (x 51.5 1.2 mm/2 months, N 5187). There was a statistically signi¢cant di¡erence in The estimated asymptotic length was largest for mus- growth of tagged mussels with respect to site and sels from site 2 (L1 5 83.13mm), while those for sites period (Fig. 3, Table 1). In a 10-month period, fastest 1(L1 5 66.94 mm) and 3 (L1 5 68.78 mm) were

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Figure 2 Seasonal variation in temperature.

Site 1 9 Site 2 Site 3 8

Growth in two months (mm) 3

Figure 3 Average growth incre- 1 ment and standard deviation of tagged mussels that survived the 0 whole study according to site and Nov-Jan Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov sampling period. 2005 | 2006 smaller and similar to each other.Values of curvature Table 1 Growth increment analysis using repeated mea- parameter (k) were 0.96,1.44 and1.32 respectively. sures ANOVA and post hoc Tukey test

Factor d.f. FP Post hoc comparison Condition index Site 2 26.70 o0.001 1 5 3o2 The condition index showed spatial and temporal Ã Period 4 156.43 o0.001 EoA 5 DoBoC variations (Fig. 4, Table 2). The highest mean condi- Interaction 8 10.22 o0.001 tion index values were recorded at site 1 in a period Error 865 from September 2005 to January 2006 (range 28.0^ ÃA, November^January; B, January^March; C, March^May; D, 31.0), while the lowest mean value was recorded in May^July; E, July^September. March 2006 at site 3 (11.3 1.7). There was a statistically signi¢cant di¡erence in condition indices re- from site 1 had signi¢cantly higher condition index corded at di¡erent sites in the same period. In a than either mussels at sites 2 or 3, except for in Feb- period from September 2005 to April 2006, mussels ruary 2006. In February, mussels from sites 1 and 3

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Site 1 Site 2 Site 3 30

20 Condition index

Figure 4 Average monthly condi- 10 Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov tion index and standard deviation 2005 | 2006 according to sampling site.

Table 2 Analysis of condition index according to sampling Discussion site and month In the eastern Adriatic Sea, mussel aquaculture is Month ANOVA/KW Post hoc comparison traditionally placed in coastal areas with reduced

September F 5 4.30Ã 142 5 3 salinity and large primary productivity to maximize October F 5 30.09ÃÃÃ 142 5 3 mussel production. The bulk of the Croatian mussel November F 5 5.13ÃÃ 142, 2 5 3, 1 5 3 aquaculture is in the areas of the Lim channel, Krka ÃÃÃ December H 5 31.57 142 5 3 estuary and Mali Ston Bay, which are moderately eu- January F 5 69.82ÃÃÃ 142 5 3 trophic areas compared with the otherwise mainly February H 5 44.63ÃÃÃ 1 5 342 March H 5 59.76ÃÃÃ 14243 oligotrophic coastal waters (Vilic› icŁ 1989). Production April F 5 12.42ÃÃÃ 142 5 3 cycle in those areas range from 1.5 to 2 years (Hrs- Ã May F 5 3.79 243, 1 5 2, 1 5 3 Brenko & FilicŁ 1973; BenovicŁ 1997; Jasprica et al.1997). 5 June F 0.72 NS – Our results show that integrating ¢sh and mussel July F 5 0.98 NS – August F 5 6.83ÃÃ 241, 2 5 3, 1 5 3 aquaculture can o¡er the same mussel production cy- September F 5 16.08ÃÃÃ 241 5 3 cle in areas traditionally considered suboptimal for October F 5 0.60 NS – mussel growth. The growth patterns observed in our ÃÃÃ November F 5 43.47 2 5 341 pilot study are consistent with previously measured Ã o0.05. rates of mussel growth in monoculture conditions in ÃÃ o0.01. the eastern Adriatic Sea. For example, growth of ÃÃÃ o0.001. 23.6 mm in 10 months at site 2 compares well with NS, not signi¢cant. growth in Mali Ston Bay where mussels grew an aver- One-way ANOVA and Kruskal^Wallis test, Post hoc comparison ^ Tukey and Mann^Whitney tests, respectively. age of 27.3 mm in 12 months (Jasprica et al.1997).The rate of growth of mussels at site 2 implicates that mus- had a higher condition index than mussels from site sels at this site would be at least as large as the mussels 2, but the condition index of mussels from sites1and in Mali Ston had they been growing the additional two 3 did not signi¢cantly di¡er from each other. In May, months. Jones and Iwama (1991) observed enhanced August and September, mussels collected from site 2 growth of oyster Crassostrea gigas (Thunberg, 1793) had the highest condition index. In November 2006, next to a salmon farm, supporting our claim that inte- indices of mussels from sites 2 and 3 were similar, grated aquaculture improves bivalve production. and both were higher than indices from site1. No sta- Growth rates at all sites were lowest during the tistically signi¢cant di¡erences in condition indices summer months (July and August) when water were observed in June, July and October 2006. temperature ranged between 21 1Cand241C, and

r 2007 The Authors 1718 Journal Compilation r 2007 Blackwell Publishing Ltd, Aquaculture Research, 38, 1714^1720 Aquaculture Research, 2007, 38, 1714^1720 Mytilus galloprovincialis in integrated aquaculture M Peharda et al. highest during March and April, when the water (1991) who found that proximity to Chinook salmon temperature was as low as 10 1C. Mussels exhibited Oncorhynchus tshawytscha (Walbaum, 1792) farm in- intermediate growth rates during all other periods. creases the oyster C. gigas condition index. The observed pattern of mussel growth can partially Our study suggests that placement of mussels rela- be explained by the temperature dependence of mus- tive to ¢sh cages considerably in£uences mussel size, sel growth rate. For example, a stationary phase in duration of the production cycle and ^ consequently mussel growth during summer (July and August) ^ pro¢ts from the aquaculture. This contrasts with was also recorded in France where water tempera- Cheshuk et al. (2003), who found no important di¡er- tures during the summer reach 25.9 1C (Gangnery, ences in growth and condition index of mussels My- Bacher & Buestel 2004), but not in Scotland where tilus planulatus (La ma rck, 1819) plac e d at d i ¡ e re nt water temperatures reach only 16.3 1C(Karayˇcel& distances from Atlantic salmon Salmo salar (Lin- Karayˇcel 2000). Almada-Viella, Davenport and naeus, 1758) culture. The di¡erences in observations Gru¡ydd (1982) analysed the temperature depen- may come from di¡erences in cultured ¢sh, mussels dence of mussel Mytilus edulis Linnaeus 1758 or primary productivity in the area. growth: growth rate increases logarithmically be- A number of other factors that may a¡ect bivalve tween 3 1Cand201C, but declines sharply above growth include depth, position of ropes on rafts and 20 1C. The sharp decline above 20 1C could explain position of bivalves relative to currents. There is no the slow growth and low condition index during the conclusive evidence as to how mussel growth de- warmest months, but not the growth rate pattern ob- pends on depth: some studies suggest that deeper served during the other periods. If mussel growth mussels grow faster (Mazzola et al. 1999), in others were dictated by temperature only,growth rates dur- mussels placed shallower grew faster (Fuentes, Gre- ing the colder months (January through April) would gorio, Giraldez & Molares 2000), while some studies be smaller than during the periods with moderate found no signi¢cant e¡ect of depth on mussel growth water temperature (October through December and (Jasprica et al.1997; Karayˇcel & Karayˇcel 2000). Si- May through July). We, however, observed larger milarly, evidence is not conclusive regarding the ef- growth rates during colder months (especially dur- fect of position. Karayˇcel and Karayˇcel (2000) ing March and April).Therefore, mussel growth must found that in monoculture conditions position of the be a¡ected by something other than the temperature. mussel on the raft signi¢cantly in£uenced its growth The period of fastest growth coincides with the per- rate, while according to Fuentes et al. (2000) it was of iod of highest primary productivity in the Adriatic Sea lesser importance.To properly resolve these issues, as (MarasovicŁ , Ninc› evicŁ ,Kusﬂ pilicŁ ,MarinovicŁ &Marinov well as better determine the optimum position of 2005), suggesting that the higher growth rate may be mussel relative to ¢sh aquaculture, we plan to devise a result of increased food availability.The decrease of a much broader experiment guided by this pilot study. growth rates in the period after the highest primary productivity,even though growth rate increase due to Acknowledgments increase in temperature was expected, suggests that mussels are food-limited during large parts of the year. We are indebted to ADRIA-OCTOPUS ¢sh farm com- We observed highest condition indices in the peri- pany from Biograd n/m for allowing us to set up this od from October to February at all sites, suggesting experiment and giving us required technical sup- that the end of autumn and winter period is the opti- port. Research was ¢nanced by Croatian Ministry of mum time for harvest. The market demand for sea- Science, Education and Sport, project number 001 food in Croatia is, however, linked to the summer 3077 0532. Tin Klanjsﬂ c› ek’s work has been supported tourist season, thus forcing mussel harvest in inte- by NZZ, grant number 02.03/16. grated aquaculture at a biologically sub-optimal time. Creating year-long processing facilities would help mitigate the problem by improving the winter References market for mussels. Our results show that position Almada-Viella P.C., Davenport J. & Gru¡ydd L.L.D. (1982) The did not consistently in£uence condition indices of e¡ects of temperature on the shell growth of young Myti- mussels. This is in accordance with Taylor et al. lus edulis L. Journal of Experimental Marine Biology and (1992), who did not ¢nd a link between distance from Ecology 59,275^288. the salmon farm and the condition index of mussel BenovicŁ A. (1997) The history,present condition, and future M. edulis either, but contrasts with Jones and Iwama of the molluscan ¢sheries of Croatia. In: The History,

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