Aquaculture 241 (2004) 207–218 www.elsevier.com/locate/aqua-online

Effect of Musculista senhousia mats on mortality and growth: much ado about nothing?

Michele Mistri*

Department of Biology, University of Ferrara, via L. Borsari 46, I-44100 Ferrara, Italy Received 18 November 2003; received in revised form 29 April 2004; accepted 21 July 2004

Abstract

By means of manipulative experiments, growth and mortality of the Tapes decussatus and Ruditapes philippinarum were assessed in the presence and absence of Musculista senhousia (Mytilidae) in its mats. The experiment was arranged as a randomized complete block design, with eight blocks of nine cages each: four blocks contained T. decussatus, and four blocks R. philippinarum. The experimental units received one of the following treatments: T. decussatus (or R. philippinarum) with no mats, with mats of M. senhousia in high density, with mats in low density. The experiment ran for 100 days. The growth of both clam species was not affected by the presence of mats. Mortality was higher for T. decussatus than for R. philippinarum, but the presence of mats, both in high and low density, seemed to exert no significant effect on clam mortality. It is hypothesized that deeper-dwelling species, as the carpet-shell and the Manila clam, are much less affected than other bivalves by mussel mats. D 2004 Elsevier B.V. All rights reserved.

Keywords: Growth; Mortality; Ruditapes philippinarum; Tapes decussatus; Musculista senhousia

1. Introduction

Tapes decussatus and Ruditapes philippinarum are among the most popular and profitable molluscs of lagoonal and coastal fishery in Italy. The Manila clam, R.

* Tel.: +39 532 291736; fax: +39 532 249761. E-mail address: [email protected].

0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2004.07.022 208 M. Mistri / Aquaculture 241 (2004) 207–218 philippinarum, was introduced in northeastern Italy in the early 1980s (Lagoon of Venice: 1983; Sacca di Goro: 1984), for the relaunching of national mollusc fishery after the considerable stock reductions experienced by the native carpet-shell clam, T. decussatus,a less-tolerant and -resistant species (Breber, 1985; Pellizzato and Mattei, 1986; Paesanti, 1990; Rossi, 1992). The Manila clam showed a great capacity to adapt to the new environment, and almost entirely occupied the ecological niche of the native clam, which is now poorly present and only in very restricted areas (Marin et al., 2003). Conversely, in suitable environments on the western Italian coasts, where R. philippinarum was not introduced, populations of the carpet-shell clam are still exploited. In Italy, the commercial exploitation of either native or introduced clams generally involves natural harvesting or planting seed (naturally caught or hatchery reared) into the sediment for ongrowing to the marketable size. Efficient culture-based fishery requires, among the others, the enhance- ment of seed survival and growth through relaxing predation pressure and competition (Cigarrı´a and Ferna´ndez, 2000). The Asian date mussel Musculista senhousia is an Indo-Pacific mytilid that was unintentionally introduced in the early 1990s in the north-eastern Adriatic Sea (Sacca di Goro), and actually occurs with large populations also in Tyrrhenian (Gulf of Olbia) and Ionian (Mar Piccolo) coastal areas. (Mistri et al., 2004). live semiburied in subtidal soft sediments, secrete byssal threads to attach to conspecifics, and build extended mats that alter the nature of the sediment (Crooks, 1998; Mistri et al., 2003) inhabited by commercial infaunal bivalves. Because large areas of Sacca di Goro and of the Gulf of Olbia are dedicated to the culture of Manila and carpet-shell clams, respectively, the presence of mussel mats has been claimed to create heavy impacts on exploitation through the reduction of shellfish growth and survival, becoming even a local newspapers topic. Nevertheless, the effect(s) of M. senhousia mats on clam culture has never been specifically addressed. In this paper, the hypothesis that mats of the Asian date mussel play a role on growth and mortality of the two clam species reared in Italy, T. decussatus and R. philippinarum, was tested experimentally.

2. Materials and methods

Experiments were carried out at the CRIM Laboratory (Goro; 44850V575UN, 12817V348UE); the lab is located a few hundred meters from the shoreline of the lagoon, thus receiving, through a pumping system, natural water directly from the Sacca.

2.1. Pilot experiment

A pilot experiment was carried out from 11 July to 12 November 2002 (123 days). The experiment was aimed to determine the effect of three types of treatment with mussel mats on the mortality of the Manila clam, Ruditapes philippinarum.A7878 cm, flow-through tank was filled at half with natural sediment and unfiltered, running brackish water. Twelve cages were placed into the tank, and four Ruditapes philippinarum (27.7F1.9 mm SL, Ntot=96 clams) were allowed to bury into each cage. Then, cages randomly received one of the following treatments: (1) no mussel mat (control, CRp), (2) approximately 50 g wet M. Mistri / Aquaculture 241 (2004) 207–218 209

weight (M. senhousia at low density, LRp) and (3) 300 g wet weight (M. senhousia at high density, HRp) of natural mussel mat. At the end of the pilot experiment, clam mortality was determined as the number of clams found dead in each cage. After 123 days, clam mortality was: CRp=12.5%, LRp=0%, HRp=12.5%. Data were analyzed through one-way analysis of variance (ANOVA; F2,9=1.5; p=0.27). Then, the number of replicates per treatment necessary for b=0.20 (at a=0.05) were estimated iteratively (Sokal and Rohlf, 1995a) through Pearson–Hartley charts (Sokal and Rohlf, 1995b). In the calculation, a minimum difference in mortality between treatments of 15% was considered satisfactorily meaningful for the usefulness of the experimental purpose. A satisfactory power of 1b=0.84 could have been achieved with 15 replicates per treatment.

2.2. Experimental design

In the manipulative experiment, growth and mortality of the clams T. decussatus and R. philippinarum were assessed in the presence and absence of M. senhousia in its mats. Clams used were of marketable size; mean shell length of T. decussatus and R. philippinarum was 28.76 mm (F3.52 mm S.D.) and 32.14 mm (F1.87 mm S.D.), respectively. Technical constraints did not allow 15 replicates per treatment, but only 12; statistical power was then lowered to about 0.70. The experiment was arranged as a randomized complete block design, with eight blocks of nine cages each. Each block consisted of a flow-through rectangular (7878 cm) tank, containing a 15-cm-deep layer of natural, unsieved sediment, which allowed ample burrowing depth for clam species, and which contained no detectable bivalves, large predatory gastropods or crabs, and unfiltered, running brackish water to a level about 25 cm above the sediment surface. Four out of eight blocks contained T. decussatus, while the other four blocks contained R. philippinarum. The experimental units were topless mesh (1 cm) cages (15 cm in diameter and 30 cm deep) that were placed in the sediment down to the bottom of tanks, with approximately 15 cm of projecting fence edge. The experimental units received one of the following treatments: (1) five T. decussatus with no M. senhousia mats (control, CTd), (2) five T. decussatus with mats of M. senhousia in high density (approx. 100 mussels per cage, HTd), (3) five T. decussatus with mats of M. senhousia in low density (approx. 40 mussels per cage, LTd), (4) three R. philippinarum with no M. senhousia mats (CRp), (5) three R. philippinarum with mats of M. senhousia in high density (HRp), and finally (6), three R. philippinarum with mats of M. senhousia in low density (LRp). Different numbers of the two clam species were chosen to grossly have the same bclam biomassQ in each cage because R. philippinarum specimens were slightly larger than T. decussatus ones. Prior to the experiment, clams were numbered with water-resistant red ink and were measured for shell length, height and width with a caliper to the 0.05 mm. After allowing sufficient time for clam acclimatization (30 days), one randomly selected cage in each block received the mussel treatment. To best represent natural conditions, mussels in their unaltered byssal mats, containing sediments, detritus, small organisms and algae, were placed in one cage in each of the eight blocks. The experiment with mussel mats began on 31 March 2003 and ran until 8 July 2003 (i.e., 100 days). This period of the year was chosen because from spring to summer, date mussels show the fastest growth and mat formation (Mistri, 2002); at the same time, it is the most critical period for clams because they undergo gamete 210 M. Mistri / Aquaculture 241 (2004) 207–218 maturation (Sbrenna and Campioni, 1994; Rodrı´guez-Moscoso and Arnaiz, 1998). During the course of the experiment, cage walls were weekly cleared of algae, and the control cages were checked for eventual naturally recruiting mussels. At the end of the experiment, the contents of cages were collected. The response variables in the experiment were growth increments and percent mortality of T. decussatus and R. philippinarum. Clams found alive at the end of the experiment were again measured with a caliper, and growth (if any) was assessed. Mortality was determined as the number of clams found dead in each cage, divided by the total number of live plus dead clams.

2.3. Data treatment

Two-way ANOVA was used to test for statistical differences in growth and mortality, with blocks considered as random effect and treatments as fixed factor. Prior to analysis, data were checked for homoscedasticity (Levene’s test), and logarithmic (for growth increments) or arcsine (for mortality data) transformation was used whenever necessary (Underwood, 1997). The power of each performed ANOVA was assessed a posteriori through the calculation of the noncentrality parameter / (Sokal and Rohlf, 1995a), and Pearson–Hartley charts (Sokal and Rohlf, 1995b), under a=0.05. Because the experimental design suffered of a reduced power when analyzed through ANOVA, and thus of a greater risk of Type II error, a multivariate approach to data treatment was adopted through the analysis of similarity (ANOSIM; Clarke and Warwick, 2001). ANOSIM is a nonparametric test based on Mantel permutation combined with a general Monte Carlo randomization approach (Clarke and Green, 1988). Briefly, a nonparametric test statistics (R) reflecting the observed differences between treatments contrasted with differences among replicates within treatments is computed. Then, R is recomputed under permutation of the sample labels, with hi ðÞkn ! ðÞn! k k! distinct ways of permuting the labels for n replicates in each of k treatments; in other words, the labels (e.g., CRp, HRp, LRp, etc.) are randomly reshuffled, R recalculated and the process repeated a large number of times. Finally, the significance level of the test is calculated by referring the observed value of R to its permutation distribution: if the null hypothesis (e.g., no mortality difference due to treatments) is true, the likely spread of values of R is given by the random rearrangements, so that if the true value of R looks unlikely to have come from this distribution, there is evidence to reject the null hypothesis (Clarke and Warwick, 2001). A two-way crossed ANOSIM, with three treatments per four blocks per three replicates in each block for each species, was then performed using the PRIMER v5 software (Clarke and Gorley, 2001).

3. Results

In the manipulative experiment, the transplants of M. senhousia in their mats persisted well, with the majority of live mussels and well-developed mats. During the experimental M. Mistri / Aquaculture 241 (2004) 207–218 211

Table 1 Two-way ANOVA on Tapes decussatus growth Factor df F p 1b Shell length Block 3, 195 4.99 0.01 0.60 Treatment 2, 6 1.88 0.23 BT 6, 195 1.14 0.34

Shell height Block 3, 195 1.61 0.19 0.80 Treatment 2, 6 2.27 0.19 BT 6, 195 1.02 0.41

Shell width Block 3, 195 5.41 0.01 1.0 Treatment 2, 6 5.98 0.04 BT 6, 195 0.43 0.86 period, salinity ranged from 22.5 (March) to 26.5 (July) psu, while water temperature ranged from 15.5 (March) to 33 8C (July). Manila clams grew faster than carpet-shell clams. Significant differences were detected through one-way ANOVA between the two clam species (data pooled) regarding growth in shell length ( F1,283=111.98; pb0.001), shell height ( F1,283=22.43; pb0.001), and shell width ( F1,283=48.19; pb0.001). Conversely, the growth of both clams, T. decussatus and R. philippinarum, did not seem to be significantly affected by the presence of mussel mats. Table 1 reports two-way ANOVAs for T. decussatus growth, while Fig. 1 shows the results of the experiment testing the effects of M. senhousia on the carpet-shell clam growth. Table 2 reports two-way ANOVAs for R. philippinarum growth, while Fig. 2 shows the effects of M. senhousia mats on the growth of Manila clam. During the 100 days of experimentation, mortality for T. decussatus was higher than for R. philippinarum (pooled data, 30.0% vs. 1.4%; one-way ANOVA: F1,70=70.16;

Fig. 1. Effect of the presence of Musculista senhousia mats on the growth of the carpet-shell clam, Tapes decussatus, over the 100-days period (H: mats in high density; L: mats in low density; C: no mats; bar is standard deviation). 212 M. Mistri / Aquaculture 241 (2004) 207–218

Table 2 Two-way ANOVA on Ruditapes philippinarum growth Factor df F p 1b Shell length Block 3, 132 2.38 0.07 0.60 Treatment 2, 6 1.72 0.26 BT 6, 132 1.16 0.33

Shell height Block 3, 132 2.85 0.04 0.60 Treatment 2, 6 4.09 0.08 BT 6, 132 0.67 0.67

Shell width Block 3, 132 1.86 0.14 0.97 Treatment 2, 6 5.51 0.04 BT 6, 132 0.88 0.51 pb0.001), but no significant differences in mortality were found due to treatments. In Table 3, ANOVA results for T. decussatus mortality are shown; average mortality for the carpet-shell clam was: HTd=38.8%; LTd=27.5%; CTd=23.9%. R. philippinarum mortality was: HRp=2.1%; LRp=0%; CRp=2.1%; ANOVA results are given in Table 4.InFig. 3, the effect of the presence of M. senhousia mats on the mortality of T. decussatus and R. philippinarum are summarized. The ANOSIM R statistics can never technically lie outside the range (1, 1): if the null hypothesis is true, R takes approximately the value of 0 (Clarke and Warwick, 2001). For both species, the observed R values (T. decussatus: Rbetween treatments=0.001,

Fig. 2. Effect of the presence of Musculista senhousia mats on the growth of the Manila clam, Ruditapes philippinarum, over the 100-days period (bar is standard deviation). M. Mistri / Aquaculture 241 (2004) 207–218 213

Table 3 Two-way ANOVA on Tapes decussatus mortality Factor df F p 1b Block 3, 24 2.05 0.13 0.65 Treatment 2, 6 1.81 0.24 BT 6, 24 1.66 0.17

Rbetween blocks=0.023; R. philippinarum: Rbetween treatments=0, Rbetween blocks=0) provide evidence that there are neither block nor treatment effects. As an example, the simulated distribution of the test statistics R for T. decussatus is shown in Fig. 4: the observed Rbetween treatments falls well within its simulated distribution.

4. Discussion

Aquacultural research has become increasingly dependent on statistical inference. Statistical power is the probability of not committing a Type II error (i.e., accepting a false null hypothesis) when inferences are made from the ANOVAs of experimental data. Power in ANOVA of aquacultural studies has recently received attention (Searcy-Bernal, 1994; Ling and Cotter, 2003). In this study, the experimental treatments seemed to have little or no effect on the response variables, and nonsignificant results were obtained. Thus, a valid assertion of these negative results is only possible if the analytical power was high. Unfortunately, the number of replicates chosen per each treatment led to a higher probability of committing a Type II error than the conventional minimum desiderable. Moreover, the a posteriori power analysis evidenced that even if M. senhousia mats had an effect on, e.g., Manila clam mortality, the experiment would have a 50% chance of not detecting it. It should be said, however, that the smallest true difference in mortality desidered to detect, when planning the experiment (i.e., 15%), was fairly higher than the difference in mortality actually observed, especially for the Manila clam (2.1%). Because the experiment was designed to detect at least such difference, it is not surprising that, dealing with a much lower effect size, the a posteriori analysis evidenced an unsatisfactory power. Yet, through an alternative statistical approach, i.e., nonparametric analysis, the fact that M. senhousia mats may have very little effect on adult T. decussatus and R. philippinarum mortality, at least on a 100-days period, seemed reasonably hypothesizable. Only clams of marketable size were used, and the effect of the mussels on other, smaller clam sizes was not tested. Indirect evidences can yet be drawn from a study carried out in 2003 in the Sacca di Goro (Munari and Mistri, in preparation), where, at a site locally called Spiaggina (44849V042UN, 12820V268UE), macrofaunal assemblages were sampled

Table 4 Two-way ANOVA on Ruditapes philippinarum mortality Factor df F p 1b Block 3, 24 0.67 0.58 0.50 Treatment 2, 6 0.43 0.67 BT 6, 24 1.17 0.37 214 M. Mistri / Aquaculture 241 (2004) 207–218

Fig. 3. Results of the experiment testing the effects of Musculista senhousia on mortality of the clams Tapes decussatus and Ruditapes philippinarum (bar is standard deviation). within four large patches of mussel mats and on between patches, bare substrata. While in March 2003, the number of small Manila clams (SL comprised between 2 and 10 mm) did 2 not differ (Nwithin=27.53F17.3, Nbetween=20.03F8.5 clams 0.027 m ; t-test: p=0.47), in the following July, clams were significantly more abundant (t-test, pb0.05) within mats 2 (Nwithin=33.3F15.5 clams 0.027 m ) than on bare substrata (Nbetween=4.5F3.0 clams 0.027 m2). While these data confirm previous observations, i.e., that mussel mats may constitute a refuge for juvenile clams thus reducing predation impact (Mistri, 2004), also seem to suggest that mortality of juvenile R. philippinarum (Nwithin March vs. Nwithin July: t-

Fig. 4. Simulated distribution (999 permutations) of the test statistics R, under the null hypothesis of bno treatment-to-treatment changesQ in Tapes decussatus mortality (treatments are: mats in high density; mats in low density; no mats). The true value of Rbetween (0.001, broken line on the histogram) falls within the simulated range. M. Mistri / Aquaculture 241 (2004) 207–218 215 test, pb0.05), at least at the study site and in period March–July, is not enhanced by the presence of even thick mats.

4.1. Effects on clam growth

At the end of the 100-days experimental period, mean growth increments in shell length for both species were within the range of those reported in literature for specimens of the size used (Bodoy et al., 1980; Breber, 1991; Robert et al., 1993). Mean growth increments were higher in R. philippinarum than in T. decussatus. Differences in the growth of molluscs have often been associated with differences in the amount of food available, but this was not the case because it is well known that, over a wide range of temperatures, Manila clams grow faster and more efficiently than T. decussatus (Laing et al., 1987). In this experiment, the hypothesis tested was that date mussels may interfere with the filtering ability of clams, through competition for phytoplankton. The presence of even thick mussel mats seemed to have undetectable effects on clams growth. M. senhousia is a filter-feeding bivalve which preferentially ingests active phytoplankton (Inoue and Yamamuro, 2000). Conversely, clams are nonselective filter-feeders with quite a wide range of food types accessible: bacteria, cyanobacteria, green algae, benthic diatoms; and rotifers can be consumed, digested and assimilated (Sorokin and Giovanardi, 1995). It has been recently shown (Mistri et al., 2003) that the presence of mussel mats greatly increases the amount of microphytobenthic carbon available on the sediment. M. senhousia is typically raised several millimeters relative to ambient sediments, and this biogenic structure may potentially alter hydrodynamic features on flat bottoms. Consequently, it may trap a range of living materials, leading to an increase in their rate of accumulation in the mat and, thus, to very high values of microphytobenthic carbon. Such an increase in benthic high-quality food could counterbalance the eventual stress given to clams by mussel competition for phytoplankton.

4.2. Effects on clam mortality

Mortality was higher for T. decussatus than for R. philippinarum. This was not surprising because Manila clam is more ruderal and resistant than T. decussatus (Breber, 1985, 1991). The Asian date mussel is a gregarious species that modifies benthic habitats through the creation of structurally complex mats. It is known that the mat structure may facilitate many macrofaunal taxa, such as gastropods, polychaetes and crustaceans (Crooks, 1998; Crooks and Khim, 1999; Mistri, 2002, 2003). Conversely, observations from Yokosuka Harbor (Japan) led Ito and Kajihara (1981) to conclude that date mussels may outcompete other bivalve species like Meretrix sp. and Scapharca sp. From manipulative experiments carried out in Mission Bay (California, USA), it is also known that some other bivalve species (the surface-dwelling Chione undatella and Chione fluctifraga) are inhibited by the presence of the mussel and its mats: survivorship of these cockles was less than 50% when mats were present, and growth of the survivors was significantly reduced (Crooks, 2001). Conversely, in the same subtidal habitat, the deeper- dwelling bent-nosed clam, Macoma nasuta, was neither inhibited nor its growth reduced in the presence of thick mussel mats (Crooks, 2001). Both T. decussatus and R. philippinarum are relatively deep-dwelling species provided with broad extendible 216 M. Mistri / Aquaculture 241 (2004) 207–218 siphons, with the former species burrowing deeper (up to 15 cm) than the latter (up to 8 cm) in the sediments. From these and the aforementioned observations, it is hypothesizable that deeper-dwelling bivalve species are less affected than more surfacial bivalves by mussel mats. M. senhousia, Chione spp., Meretrix sp. and Scapharca sp. all occupy the same, shallow depth horizon, and the fast-growing mussel may well outcompete the other bivalves for space or food because they all filter in the water column. Sugawara et al. (1961) and Uchida (1965) reported that date mussels may cause mortality on R. philippinarum natural populations. M. senhousia, both in native and introduced range, thrives mostly in eutrophized environments (lagoons and estuaries) affected by excessive nutrient loads and, often, nitrophilic macroalgal blooms. In such environments, dystrophy and anoxia are quite common, thus causing mortality events in the benthic macrofauna and, thus, in clam stocks. The Asian date mussel is unable to survive in anoxic conditions (Yamamuro et al., 1998). In shallow-water, dystrophic lagoons and estuaries, summer high temperatures and excessive nutrients lead to anoxic crises that may cause high mortalities of M. senhousia (Mistri, 2002), and its decaying biomass (as well as macroalgal biomass; Tagliapietra et al., 1998; Mistri et al., 2002) can further exacerbate the problem through production of toxic sulfide and ammonia. This can reasonably lead to an increase in clam mortality (R. philippinarum is more resistant than mussels), but the triggering events are likely to be the physicochemical conditions of such environments, not the presence of mussel mats. Major economic damages can be associated to the establishment of allochtonous, invasive pests (e.g., the zebra mussel, Dreissena polymorpha, and the Asian clam, Corbicula fluminea, in the U.S. aquatic ecosystems, whose damages have been estimated in some hundreds millions U.S. dollars; Pimentel, 2002). Invader effects, however, may be confounded by biotic responses to other potentially interrelated changes in ecosystems, including resource overexploitation, pollution and habitat deterioration (Ruiz et al., 1997). This is probably the case with the alien mytilid M. senhousia, at least in two Mediterranean water bodies.

5. Conclusion

The role of the nonindigenous mytilid M. senhousia on the growth and mortality of two species of clams reared in Italy, T. decussatus and R. philippinarum, was assessed. R. phippinarum grew faster than T. decussatus, but the growth of both clams did not seem affected by the presence of M. senhousia in its mats. In addition, mortality was higher for T. decussatus when compared to R. philippinarum, but also in this case, the mussel did not seem to play any role in differential mortality. Paraphrasing Friar Francis, one could say bDid I not tell you she was innocent?Q (W. Shakespeare, act 5, scene 4).

Acknowledgements

This study is part of a topic bALIENQ (Impatto della specie alloctona Musculista senhousia su allevamenti di bivalvi di interesse commerciale nell’Alto Adriatico e M. Mistri / Aquaculture 241 (2004) 207–218 217 strategie di contenimento) supported by MiPAF, the Italian Ministry for Agricultural and Forest Policies, VI Triennial Programme for Fishery and Aquaculture. Thanks are due to Cristina Munari, Lucia Sgro, and Monica Tiso (University of Ferrara) for valuable help during the experiments, to Edoardo Turolla (IDEA, Comacchio) for lab facilities in Goro, and to three anonymous reviewers for constructive criticism and helpful suggestions.

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