Substrate preference in settling zebra mussels ...

Arch. Hydrobiol.

159

2

263–270

Stuttgart, February 2004

Substrate preference in settling zebra mussels Dreissena polymorpha Marcin Czarno€¸eski1 *, ukasz Michalczyk2 and Agnieszka Pajdak-Stós 1 Jagiellonian University With 1 figure and 1 table

Abstract: In a field experiment we compared recruitment of zebra mussels on two types of substrate surface, one flat and the other complex, imitating the heterogeneity of the surface between aggregated mussels. Concrete blocks, each presenting both types of substrate, were suspended horizontally or vertically in the water column along a lake shore. The density of recruits varied from 0 to 1.5 individuals/cm2 across 92 experimental substrates. Density was not affected by substrate orientation; it was significantly higher on complex than on flat substrates (median 0.32 vs. 0.18 mussels/ cm2). This indicates that besides the commonly suggested chemical cues, the complicated surface of mussel aggregates itself may elicit settling on conspecifics. We stress that gregariousness in Dreissena polymorpha may be an evolved antipredation strategy rather than a result of hyperproduction of larvae competing for scarce substrates. Key words: substrate selection, substrate complexity, larval settlement, antipredator strategy.

Introduction Barnacles and sessile mussels typically live in multilayered clumps and beds ´ (Stanczykowska 1964, Bertness & Grosholz 1985, Okamura 1986, Clare & Matsumura 2000). Although such phenomenon might be treated as a mere consequence of producing large numbers of mobile larvae that compete for settling on scarce substrates, it may be rooted in a preference for living in 1

Authors’ addresses: Department of Hydrobiology, Jagiellonian University, Gronostajowa 3, 30-387 Kraków, Poland. * E-mail: [email protected] 2 Department of Zoopsychology, Jagiellonian University, Ingardena 6, 30-060 Kraków, Poland. DOI: 10.1127/0003-9136/2004/0159-0263

0003-9136/04/0159-0263 $ 2.00

ã 2004 E. Schweizerbart’sche Verlagsbuchhandlung, D-70176 Stuttgart

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Marcin Czarno€¸eski, ukasz Michalczyk and Agnieszka Pajdak-Stós

´ the vicinity of adult conspecifics (Stanczykowska 1964, Rodriquez et al. 1993, Chase & Bailey 1996, Reimer & Tedengren 1997, Côté & Jelnikar 1999, Clare & Matsumura 2000). The chemical, physical and biological characteristics of the substrate surface may influence the settling decision, but the exact mechanisms of substrate discrimination are still poorly understood. Experiments on the freshwater mussel Dreissena polymorpha (Pallas, 1771) suggest that the young life stages use chemical cues in searching conspecifics for settlement (Chase & Bailey 1996, Wainman et al. 1996). It remains unresolved whether the surface heterogeneity produced by the mussels serves as an attractant. Testing whether surface complexity affects recruitment, in a field experiment we compare recruitment of D. polymorpha on artificial surfaces, one flat and the other complex, resembling the space between the shells of clumped zebra mussels.

M ethods The experiment consisted of 51 experimental units, each consisting of a concrete block anchored to a weight and suspended from a float (Fig. 1A). Each block presented a flat surface structurally resembling smooth rock, and a complex surface intended to mimic the complexity of space between aggregated mussels; the two surfaces were side by side on the same face of the block (Fig. 1B). The complex substrate was stamped in the concrete while it was still soft, with a V-grooved metal plate (Fig. 1 C). There was a 20 mm gap between the two tested surface types. Crawling mussels could move freely across this gap. To protect the mussels from predators, the blocks were surrounded with 11 mm wire mesh. The mesh was arranged at least 50 mm above the experimental substrates and 20 mm away from their edges, to minimise its own influence as a colonisation substrate on the rates of recruitment measured (Fig. 1 C). Of the 51 units, 31 were prepared for horizontal and 20 for vertical orientation in the water column. There were more horizontal units because they were more likely to accumulate mud on their surface, which would eliminate them as potential settlement substrates. The area of the grooved substrate (140.2 cm2) was calculated from measurements of the plate used to mould it. The area of the flat settlement substrate was fixed at the end of the experiment by placing a plastic frame on the flat surface to delimit the area in which the mussels were counted (67.2 cm2 on horizontal, 44.2 cm2 on vertical units, Fig. 1B). The experimental units were deployed in mid-May 2002 in the nearshore area of Lake Majcz Wielki, northeastern Poland, and retrieved in mid-September 2002. Dreissena larvae are most abundant from June to August in the lake (Lewandowski 1982 a). Scuba divers laid out the units randomly with respect to their horizontal or vertical orientation, at approximately 20 m intervals along 1 km of the lake shore, and 30 – 50 m from the shore. The blocks were anchored to sacks of stones and suspended at a depth of 3 m, 1m above the bottom (Fig. 1 A). After retrieval, all mussels seen by eye on experimental areas were detached and counted in situ. The number of individuals per cm2 was estimated. Because the density data had a right-skewed distribution,

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Fig. 1. Design of experimental units and scheme of their deployment in the lake. Part A shows the concrete blocks suspended horizontally or vertically in the water column. Part B shows the design of the blocks. Each block presented flat and complex (V-grooved) substrate areas, from which the attached mussels were counted (within the area of the rectangles). Note that in the vertical units the grooves run vertically. Blocks were surrounded by wire mesh. Part C shows a cross section of a block. Measurements in parts B and C are given in millimetres.

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Marcin Czarno€¸eski, ukasz Michalczyk and Agnieszka Pajdak-Stós

Table 1. Results of mixed-model nested ANOVA of density of zebra mussel recruits on different types of substrates (number of mussels/cm2). Prior to analysis, the density data were rank-transformed. Source of variance

Effect

SS

Orientation of block (horizontal vs. vertical) Shape of settlement surface (complex vs. flat) Concrete block (nested in ‘Orientation of block’) Error

Fixed

1670.0

Fixed Random

df

F

P

1

1.458

0.23

2761.0

1

12.356

< 0.002

50386.5

44

5.125

< 0.001

10055.5

45

they were rank-transformed, and the ranks were analysed with mixed-model nested ANOVA in the Statistica 6.1 package, StatSoft (Quinn & Keough 2002). We tested for the effects of the shape of the settlement surface (V-grooved vs. flat) and the orientation of the surface in the water column (horizontal vs. vertical). The concrete blocks were treated as random factors nested within the surface orientation. Homogeneity of variance was checked on ranks with Bartlet t’s test.

Results We obtained data from 27 horizontal and 19 vertical units (92 settlement substrates); 4 blocks were lost, and 1 block found at the bottom was excluded from the analysis. The density of recruits varied from 0 to 1.5 individuals/cm2 across 92 experimental areas. ANOVA results (Table 1) indicated that the complexity of the settlement surface significantly influenced recruitment (ANOVA, F = 12.356 p < 0.002). During the four months of the experiment, the mussels on the V-grooved surface attained significantly higher density (median 0.32 individuals/cm2) than on the flat surface (median 0.18 individuals/cm2). The orientation of the blocks in the water column (horizontal vs. vertical) did not significantly affect the density of recruits (ANOVA, F = 1.458 p = 0.23). The random factor (concrete blocks) expressing the uncontrolled differences between the blocks or their locations in the lake explained a significant part of the recruitment variation (ANOVA, F = 5.125 p < 0.001).

Discussion The location of settlement influences the lifetime mortality and production rates of sessile organisms, the major components of selection pressure (Czarno€Îeski et al. 2003). Therefore the initial life stages should evolve the ability to choose the settlement site that ensures the highest expected reproductive

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value of the later sessile stages. Recruitment of zebra mussels results from passive settlement of larvae and preferences for certain physicochemical and biological characteristics of the substrate. Mussels tend to avoid sunny, bright and exposed substrates, and they preferentially attach to rough surfaces covered with biofilm (Wainman et al. 1996, Marsden & Lansky 2000, Kobak 2001). The choice of substrate may occur in two phases (Ackerman et al. 1994). For several days, actively swimming and crawling pediveligers ( < 300 mm high larvae with foot) can regulate the timing of byssal thread secretion according to information they receive on the type of substrate they are colonising. Metamorphosed stages including adults may translocate by crawling; postveligers and small juveniles are also able to return to the water column by cutting the byssus and producing suspension threads with the siphon or foot. In our experiment, young D. polymorpha attained significantly higher densities on V-grooved than on flat substrates (median 0.32 vs. 0.18 individuals/cm2, Table 1). Earlier studies reported higher rates of recruitment of dreissenid larvae on microheterogenous surfaces (Marsden & Lansky 2000). In barnacle larvae, Hills et al. (1999) demonstrated that on a microscale such a phenomenon results from the increased number of potential settling sites provided by rough materials. Settling sites also become more numerous on substrates with large-scale heterogeneity. In our experiment we controlled for this dependence by calculating mussel densities versus the actual surface area on both types of substrate. Earlier works demonstrating higher recruitment of zebra mussels on stones or adults’ shells did not differentiate between a preference for complex substrates and the effect of an increased number of settling sites on heterogeneous surfaces (e.g., Lewandowski 1982 b, Chase & Bailey 1996, Kobak 2001). Our results suggest that large-scale substrate heterogeneity may indeed stimulate recruitment of zebra mussels. Our findings accord with descriptive observations of the preference of zebra mussels for concavities (Marsden & Lansky 2000) and with tendencies detected in marine sessile invertebrates (Lemire & Bourget 1996, Hills et al. 1999). Unfortunately, we were unable to identify the life stages responsive to substrate topography, nor to assess the extent to which the detected recruitment pattern was linked to probable variation of water turbulence over different types of surface. Larvae settlement should be higher on upper horizontal surfaces than on their undersides or vertical surfaces (Marsden & Lansky 2000). Recruitment in our experiment did not differ between horizontally suspended and vertically suspended blocks (Table 1), in contrast to Yankovich & Haffner’s (1993) finding that zebra mussels more heavily colonised the sides than the tops of cement blocks. The discrepancy can be explained by the relation between substrate orientation and light conditions (Marsden & Lansky 2000). If horizon-

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Marcin Czarno€¸eski, ukasz Michalczyk and Agnieszka Pajdak-Stós

tal surfaces are more exposed to sunlight than vertical ones, as in Yankovich & Haffner’s experiment, zebra mussels tend to move from horizontal to vertical substrates. In our experiment, primary settlement might have been higher on horizontal than on vertical blocks, but the equal recruitment found on the two types of blocks indicates that mussels relocated from the illuminated upper sides of the horizontal blocks to the shaded undersides, as also shown by Walz (1975) and Lewandowski (1982 b). Indeed, we observed incomparably more mussels attached to undersides than to the tops of the horizontal blocks (not tested statistically). The initial life stages of sessile organisms are suggested to prefer conspecifics as settling sites (Rodriquez et al. 1993, Chase & Bailey 1996, Wainman et al. 1996, Reimer & Tedengren 1997, Côté & Jelnikar 1999, Clare & Matsumura 2000, Kobak 2001). Chemical cues are believed to mediate such a tendency (e.g., Chase & Bailey 1996, Clare & Matsumura 2000). Wainman et al. (1996) found equal recruitment of dreissenid veligers on substrates with adult mussels and with empty shells, both higher than on a stony substrate without mussels, indicating that the chemicals may originate from shell material rather than the soft tissue. In our experiment, zebra mussels preferred a complex substrate over a flat one, implying that the irregularities of the surface in mussel aggregates itself may elicit the settling decision. Côté & Jelnikar (1999) report that the rate of clumping in Mytilus edulis is generally linked to the chance of encountering conspecifics during random walks. However, mussels initially set far apart increased their crawling speed compared to individuals placed closer to each other, and both groups aggregated at the same rate. This indicates that the immediate decision about attachment indeed relies on physical stimulation but that the proximity of conspecifics is perceived through chemical cues. The operation of mechanisms of chemical or physical detection of conspecifics suggests that gregariousness in D. polymorpha is an evolved strategy rather than a consequence of hyperproduction of larvae that settle on scarce substrates. The strategy entails the costs of increased intraspecific competition, such as reduction of the growth and reproduction rates, or acceleration of mortality at late ages (Bertness & Grosholz 1985, Okamura 1986, Czarno€Îeski et al. 2003). The benefits that might outweigh such costs are poorly documented in zebra mussels. Clumping reduces external mortality from predation in other bivalves (Bertness & Grosholz 1985, Okamura 1986). Interestingly, Mytilus edulis even adjusts the rate of clumping to the risk of predation by lobsters (Côté & Jelnikar 1999). Gregariousness has also been suggested to increase fertilisation or filter-feeding efficiencies (Barnes & Powell 1950, Pawlik 1986). Further studies should identify the benefits from gregariousness that play the most important role in zebra mussels.

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Acknow ledgements The work was supported by the Polish State Committee for Scientific Research, grant ´ no. 6P04C05015. A. Stanczykowska and K. Lewandowski helped design the ex´ A. Ganczarek, P. Kubajak, U. Poperiment. We thank A. Bulek, A. Chyli nska, korska, Z. Prokop and è . Sobczyk for assistance in the work, P. Stós for underwater work, and the Strza€owo Forestry Authority for its hospitality. J. Koz€owski and K. Wi Îackowski and three anonymous referees made helpful comments on drafts of the manuscript. M. Jacobs helped edit it.

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