J. Mar. Biol. Ass. U.K. (2001), 81, 651^654 Printed in the United Kingdom
Salinity dependence in the marine mud snails Hydrobia ulvae and Hydrobia ventrosa Johan Grudemo* and Carl Andre¨O *Department of Zoology, Go«teborg University, Box 463, SE-405 30 Go«teborg, Sweden. Tja«rno« Marine Biological Laboratory, SE-452 96 Stro«mstad, Sweden. *E-mail:
[email protected]
O
The e¡ect of di¡erent salinities on the marine snails Hydrobia ulvae and Hydrobia ventrosa (Mollusca: Prosobranchia) was studied in laboratory experiments. For juvenile snails, neither shell growth nor the strength of interspeci¢c competition were a¡ected by salinity within the range of 15^30 psu. In contrast, we found that larvae of H. ulvae were sensitive to salinity: survival was higher and the larvae were more active in higher salinity. The negative in£uence of low salinity on H. ulvae larvae may not be the only explanation of the complementary ¢eld distribution of the two species, since habitat separation is present in areas without spatial salinity variation.
INTRODUCTION Fenchel (1975a) suggested that two marine intertidal snail species, the larviparous Hydrobia ulvae (Pennant), and the direct developer, Hydrobia ventrosa (Montagu), show character displacement (Brown & Wilson, 1956), since their shell sizes di¡er more in sympatry than in allopatry; the species are expected to show exploitative competition since both mainly eat diatoms. Both species are nonrandomly distributed in relation to di¡erent environmental factors such as salinity (Fenchel, 1975a), shelter (Saloniemi, 1993; Barnes, 1999), and sediment quality (Grudemo & Johannesson, 1999). When distribution is correlated to an environmental factor, a necessary part of the evidence for character displacement is to show that the di¡erence in the environment between allopatric and sympatric localities does not a¡ect body size (Grant, 1972; Arthur, 1982). In Denmark, H. ulvae often dominates at localities with high salinity and H. ventrosa at localities with low salinity (Muus, 1967; Fenchel, 1975b). Fenchel proposed that the species have di¡erent salinity optima, that may explain their distribution. In a laboratory experiment, Hylleberg (1975) investigated the performance of H. ulvae and H. ventrosa in di¡erent salinities (10^30 psu) and temperatures (5^358C), and concluded that H. ventrosa could be expected to be competitively superior at low salinity and H. ulvae at high, and that salinity is important for the distribution of the two species. Other studies indicate, however, that di¡erences in salinity are of less importance for the distribution and coexistence of the two species: Hylleberg (1986) reported that H. ulvae lives in salinities down to 5 psu in the Baltic Sea; Gorbushin (1996) showed that H. ulvae was competitively superior to H. ventrosa at low salinity (3^15 psu); and in England H. ulvae dominates tidal areas and H. ventrosa enclosed coastal lagoons, which Barnes (1999) suggested was not due to di¡erences in salinity, but probably to the di¡erent recruitment strategies of the species. On the Swedish Skagerrak coast, H. ulvae dominates in wave exposed localities with coarse-grained sediments and H. ventrosa in sheltered localities, where the sediment Journal of the Marine Biological Association of the United Kingdom (2001)
is more ¢ne-grained (Grudemo & Johannesson, 1999). This habitat separation occurs despite little spatial variation in salinity. The role of salinity for the distribution of the Hydrobia species thus require further investigation. Here we investigate the e¡ect of di¡erent salinities on juveniles and larvae, and test the hypothesis that H. ulvae is better adapted to high salinity, whereas H. ventrosa is better adapted to low.
MATERIALS AND METHODS Growth and competition in juvenile snails of Hydrobia ulvae and Hydrobia ventrosa
During two months in autumn 1998, growth and competition in juvenile Hydrobia ulvae and Hydrobia ventrosa were studied at di¡erent salinities at 108C with a light regime of 16:8 h light/darkness. Snails were placed in plastic cups (area 11cm2) with sieved ¢ne sandy sediment. Growth, measured as the di¡erence in shell length before and after the experiment, was quanti¢ed for one marked target snail only in each cup. In both species, the length of target snails was 1.6^2.0 mm at the start of the experiment. The snails were subjected to three competition treatments: (1) no competition (1 target snail of H. ulvae or H. ventrosa: population density 930 m72); (2) competition from H. ulvae (1 target snail 6 H. ulvae competitor snails: total population density 6500 m72); and (3) competition from H. ventrosa (1 target snail 6 H. ventrosa competitor snails). The number of competitors was chosen to represent medium ¢eld competition. The competitor snails were larger than the target snails, with a shell length of 3 mm at the start. The sizes of snails were chosen to resemble the natural situation when juvenile snails grow up together with larger adults. The experiment was conducted at three salinities, 15, 22.5 and 30 psu, representing low, medium and high salinity at the Swedish Skagerrak coast. The salinity was held constant during the two-month period through daily addition of distilled water.
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Salinity dependence in Hydrobia
Growth of the target snails was analysed with a threefactor ANOVA. The factors were: species (SP) with two levels (H. ulvae and H. ventrosa); competition (C) with three levels; and salinity (SA) with three levels. The linear model was:
factor and the average proportion of swimming larvae for each discp across the six time intervals, transformed to arcsine ( x), as the dependent variable.
xijkl m SPi SAj Ck SPi SAj SPi Ck SAj Ck SPi SAj Ck eijkl
Survival of H. ulvae larvae was recorded after ¢ve, ten and 20 d from hatching. At the start of the experiment 30 larvae were transferred to 500-ml beakers. We used six replicate beakers for each combination of salinity and duration time, so each beaker was only read once. Water and food was changed every third day. In each beaker the proportion of live larvae p was quanti¢ed. Survival was transformed to arcsine ( x) and analysed using two-way ANOVA with salinity and time as factors.
where xijkl is the growth of the target individual, m the average growth of all snails, and eijkl the residual. All factors were considered ¢xed, and all tests were thus performed with the residual as error-term. For each combination of treatments, 15 replicates were used. To obtain appropriate interactions (Hurlbert & White, 1993), and to reduce variance heterogeneity, the logarithm of growth (ln(growth 0.1)) was used in the analysis. Student ^ Newman ^ Keuls (SNK) test was used for post-hoc analyses. Fecundity, larval behaviour and survival of H. ulvae were studied in the laboratory at three di¡erent salinities, 12, 18 and 28 psu. The larvae were reared in 50-l tanks and fed the £agellate Isochrysis galbana at 100 cells ml71 (cf. Renaud & Parry, 1994); a system in which we have previously reared H. ulvae to metamorphosis. Fecundity of Hydrobia ulvae and water column distribution of larvae at di¡erent salinities
In nine 5-l buckets, a 2-cm thick layer of sieved, ¢ne sandy sediment and a water column of 16 cm was assembled. Four hundred adult snails were placed in each bucket corresponding to a density of 14,000 m72. There were three replicate buckets for each salinity. Since sex ratio was unbiased at the sampling locality (w2-test, N50, P0.78), each bucket would be expected to contain 200 females and 200 males. The snails had been acclimatized to the di¡erent salinities during seven days. The buckets were placed outdoors and the snails thus exposed to a natural day length cycle and ambient temperature (208C). The production of larvae was recorded after ¢ve, nine, and 12 days. At sampling, the water column was divided into one upper fraction of 8 cm and a lower one of 8 cm. Water was collected with a membrane pump and sieved through 60-mm mesh size, whereupon the larvae were stored in ethanol until counted. After both fractions were sampled, new water was added. The e¡ect of salinity on fecundity and distribution of larvae was analysed with linear regression, with either the total number of larvae produced (three occasions and two fractions) in each bucket, or the proportion of larvae in the upper fraction in each bucket p (averaged over occasions and transformed to arcsine ( x)) as dependent variables. Swimming behaviour of Hydrobia ulvae larvae
Ten newly hatched larvae were placed in triplicate discs containing 5 ml water. After 45, 105, 165, 375, 765 and 1380 minutes the proportion of larvae swimming were noted. Between the readings, the larvae were held in constant light and temperature (208C). The experiment was analysed with a one-factor ANOVA, with salinity as Journal of the Marine Biological Association of the United Kingdom (2001)
Survival of Hydrobia ulvae larvae
RESULTS Growth and competition in juvenile snails of Hydrobia ulvae and Hydrobia ventrosa
During the experiment, mortality was low and only one dead target snail was found. However, 21 target snails (8%) had either lost the paint or escaped from the cup. In the ANOVA the lost snails were replaced with the average growth of the surviving individuals from the same treatment. The residual degrees of freedom were corrected accordingly. The di¡erent salinities did not a¡ect growth, either on their own, or in interaction with competition or species (Table 1). Hydrobia ulvae grew faster than Hydrobia ventrosa, and competition generally reduced growth rate. However, competition from H. ulvae reduced growth of both species more than competition from H. ventrosa. We found an interaction between species and competition caused by H. ulvae su¡ering slightly less from competition from H. ventrosa, than H. ventrosa (Figure 1). When the competitors were H. ulvae, growth of both species was reduced by the same amount. Fecundity and water column distribution of larvae in Hydrobia ulvae
No relation between salinity and fecundity was found (Figure 2A, N9, r2 0.21, P0.22). Hydrobia ulvae larvae were, however, more active in higher salinities as the proportion of larvae in the upper Table 1. ANOVA-table for the test of the e¡ect from salinity on growth and competition of juvenile Hydrobia ulvae and H. ventrosa. Factor
SS
Species, SP 32.82 Competition, C 72.14 Salinity, SA 0.21 SPC 1.24 SPSA 0.26 CSA 0.91 SPCSA 1.47 Residual 43.07 Total 152.12
df
MS
1 2 2 2 2 4 4 231 249
32.82 36.07 0.11 0.62 0.13 0.23 0.37 0.19
F
P
176.04 50.0001 193.45 50.0001 0.56 0.54 3.32 0.04 0.69 0.47 1.22 0.26 1.97 0.08
Salinity dependence in Hydrobia J. Grudemo and C. Andre¨
653
Figure 1. Growth of Hydrobia ulvae and Hydrobia ventrosa in di¡erent combinations of salinity and competition (mean SE). A
Table 2. ANOVA-table for survival of Hydrobia ulvae larvae in di¡erent salinities after di¡erent times. Factor Salinity Time SalinityTime Residual Total
SS
df
MS
F
P
0.95 14.50 1.11 1.20 17.76
2 2 4 45 53
0.47 7.25 0.28 0.03
17.7 272.3 10.4
50.0001 50.0001 50.0001
part of the water column increased with salinity (Figure 2B, N9, r2 0.77, P0.0019). Swimming behaviour of Hydrobia ulvae larvae B
The proportion of swimming individuals were higher at 28 psu, 0.572 0.063 (mean SD) than at 18 psu, 0.011 0.019 or 12 psu, 0 0, (P50.0001; SNK post-hoc test: P50.05) This result indicates thus that H. ulvae larvae were more active in high salinity than in low. Survival of Hydrobia ulvae larvae
Both salinity, duration, and their interaction were statistically signi¢cant (Table 2). Student ^ Newman ^ Keuls-test showed that survival after 5 d was high and similar in all salinities, and that no larvae survived for 20 d in any of the salinities. On average, larvae lived longer at higher salinity, and after ten days survival was signi¢cantly higher in 28 psu than in 18 psu, and lowest in 12 psu salinity. Also from this experiment, it seems that larvae of Hydrobia ulvae were favoured by high salinity. Figure 2. (A) Fecundity in di¡erent salinities, measured as the number of larvae produced by 400 Hydrobia ulvae snails during 12 days. (B) The relationship between salinity and the proportion of larvae located in the upper half of the water column in 5-l buckets. Each symbol is the average value for one bucket. Journal of the Marine Biological Association of the United Kingdom (2001)
DISCUSSION There was no indication of salinity dependent growth in juvenile snails of Hydrobia ulvae and Hydrobia ventrosa, either with or without competition. This contradicts the
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J. Grudemo and C. Andre¨
Salinity dependence in Hydrobia
view that di¡erences in salinity are of vital importance to juvenile snails (Hylleberg, 1975). However, we did ¢nd that the performance of H. ulvae larvae was salinity dependent. The activity and viability of the larvae were higher at 28 psu than at 18 and 12 psu. Thus, if ¢eld distributions of the species are a¡ected by salinity (Muus, 1967; Fenchel, 1975a) this may well be due to its in£uence on H. ulvae larvae. Hydrobia ulvae grew faster than H. ventrosa both with and without competitors, and H. ulvae was a stronger competitor to individuals of both species. Similar results shown at 30 psu by Grudemo & Bohlin (2000) were thus supported, and appear to be general in salinities down to at least 15 psu. Since no in£uence from di¡erences in salinity on growth and competition in juvenile Hydrobia was found, the present results disagree with a previous experiment by Hylleberg (1975), who measured egestion of organic matter in faecal pellets in Hydrobia species at di¡erent salinities and temperatures. He concluded that H. ulvae was more e¤cient at high salinity and H. ventrosa at low. When establishing a relationship between di¡erent environmental factors and ¢tness, it is important to measure a response variable that is at least partly correlated with ¢tness. Although egestion of total faecal pellets (including both organic and inorganic material) has been used as a measure of food intake in other studies (e.g. Cammen, 1989), we question that egestion of organic matter in faecal pellets is an appropriate measure of ¢tness. Hylleberg (1975) did not show explicitly that egestion of organic material was correlated to food intake. However, even if this correlation exists, one cannot conclude that individuals are doing better when food intake is higher. If the food demand is higher, the snails may well have lower ¢tness. In fact, there are in Hylleberg's study indications that ¢tness is low when egestion is high: in H. ulvae egestion increased when temperature rose and was highest at 308C, which was close to lethal temperature. This is further supported by the fact that egestion in the other species, H. ventrosa, did not increase with temperature in the same way as in H. ulvae, and that H. ventrosa survived at 358C. Shell growth is a better measure of ¢tness than egestion, and thus conclude that a ¢eld correlation between salinity and population densities of the species is not likely to be caused by the impact from di¡erent salinities on juvenile snails. In contrast, our experiments showed that larvae of H. ulvae were more viable at high salinity. This supports the idea that spatial variation in salinity may lead to di¡erences in population densities (Fenchel, 1975b), although studies from several other areas without spatial salinity variation also show habitat separation between the two species (Hylleberg, 1986; Saloniemi, 1993; Barnes, 1999; Grudemo & Johannesson, 1999). The only known ¢eld distribution that shows a correlation between salinity and distribution of H. ulvae and H. ventrosa is from Denmark (Muus, 1967; Fenchel, 1975b). Our results suggest that this may be caused by impact from salinity on H. ulvae larvae. However, besides the correlation to salinity, Fenchel (1975b) also found a correlation between water movements and distribution in the same area. In summary, we found no evidence that moderate di¡erences in salinity are important for growth and Journal of the Marine Biological Association of the United Kingdom (2001)
competition ability of juvenile Hydrobia snails. It seems, however, that low salinity is unfavourable for H. ulvae larvae. Although this may explain its ¢eld distribution in Denmark, more evidence is needed to generalize this conclusion. This study was ¢nanced by the foundations of Helge Ax:son Johnson (C.A., J.G.) and Colliander (J.G.), and the EU through Tja«rno« Centre of Excellence (C.A.). We thank Torgny Bohlin and Kerstin Johannesson for valuable discussions and comments on the manuscript.
REFERENCES Arthur, W., 1982. The evolutionary consequences of interspeci¢c competition. Advances in Ecological Research, 12, 127^187. Barnes, R.S.K., 1999. What determines the distribution of coastal Hydrobiid mudsnails within north-western Europe ? Publicazioni della Stazioni Zoologica di Napoli: Marine Ecology, 20, 97^110. Brown, W.L. & Wilson, E.O., 1956. Character displacement. Systematic Zoology, 5, 49^64. Cammen, L.M., 1989. The relationship between ingestion rate of deposit feeders and sediment nutritional value. In Ecology of marine deposit feeders (ed. G. Lopes et al.), pp. 201^222. Berlin: Springer-Verlag. Fenchel, T., 1975a. Character displacement and coexistence in mud snails (Hydrobiidae). Oecologia, 20, 19^32. Fenchel, T., 1975b. Factors determining the distribution patterns of mud snails (Hydrobiidae). Oecologia, 20, 1^17. Gorbushin, A.M., 1996. The enigma of mud snail shell growth: asymmetrical competition of character displacement ? Oikos, 77, 85^92. Grant, P.R., 1972. Convergent and divergent character displacement. Biological Journal of the Linnean Society, 4, 39^68. Grudemo, J. & Bohlin, T., 2000. E¡ects of sediment type and intra- and interspeci¢c competition on growth rate of the marine snails Hydrobia ulvae and Hydrobia ventrosa. Journal of Experimental Marine Biology and Ecology, 253, 115^127. Grudemo, J. & Johannesson, K., 1999. Size of mudsnails, Hydrobia ulvae and H. ventrosa, in allopatry and sympatry; conclusions from ¢eld distributions and laboratory growth experiments. Journal of Experimental Marine Biology and Ecology, 239, 167^181. Hurlbert, S.H. & White, M.D., 1993. Experiments with freshwater invertebrate zooplanctivores: quality of statistical analyses. Bulletin of Marine Science, 53, 128^153. Hylleberg, J., 1975. The e¡ect of salinity and temperature on egestion in mud snails (Gastropoda: Hydrobiidae). Oecologia, 21, 279^289. Hylleberg, J., 1986. Distribution of hydrobiid snails in relation to salinity, with emphasis on shell size and co-existence of the species. Ophelia, 4, 85^100. Muus, B.J., 1967. The fauna of Danish estuaries and lagoons. Distribution and ecology of dominating species in the shallow reaches of the mesohaline zone. Meddelelser fra Danmarks Fiskeri- og HavundersÖgelser (Ny Serie), 5, 1^316. Renaud, S.M. & Parry, D.L. 1994. Microalgae for use in tropical aquaculture. II. E¡ect of salinity on growth, gross chemical composition and fatty acid composition of three species of marine microalgae. Journal of Applied Phycology, 6, 347^356. Saloniemi, I., 1993. An environmental explanation for the character displacement pattern in Hydrobia snails. Oikos, 67, 75^80. Submitted 16 January 2001. Accepted 5 June 2001.
