J. Mar. Biol. Ass. U.K. (2005), 85, 375^382 Printed in the United Kingdom

Life cycle, population dynamics and productivity of Ventrosia maritima in the Evros Delta (northern Aegean Sea)

Theodoros Kevrekidis*P and Thomas WilkeO *Democritus University of Thrace, Laboratory of Environmental Research and Education, GR-68100, Alexandroupolis, Greece. OAnimal Ecology & Systematics, Justus Liebig University Giessen, Heinrich-Bu¡-Ring 26^32 (IFZ), D^35392, Giessen, Germany. PCorresponding author, e-mail: [email protected]

Life cycle, population dynamics and productivity of the larviparous mudsnail species Ventrosia maritima were investigated at low salinities (0.3^6 psu) in di¡erentiated parts of a Mediterranean lagoon (Monolimni Lagoon). Monthly samples were collected during the period from February 1998 to February 1999 in both parts of the lagoon.Ventrosia maritima displayed an annual life cycle. Recruitment occurred in summer and autumn at the outer part of the lagoon and additionally in late winter at the innermost part. A positive correlation was found between the percentages of small individuals and salinity or sediment organic matter at the outer part. Growth practically ceased in winter. The mudsnail displayed remarkable densities and an increase in growth in spring at 51psu indicating that it is highly tolerant to extremely low salinities. Population density showed a signi¢cant seasonal variation; it increased from early summer to autumn (30,000^40,000 individuals m72) following the summer and autumn recruitment. No signi¢cant correlation between the density of V.maritima and several examined physicochemical variables was found; a negative correlation was observed between the density of the mudsnail and that of the co-occurring poly- chaete Streblospio shrubsolii. Secondary production calculated by the size^frequency method gave a mean annual density (N) of 9740 ind m72, a mean biomass (B) of 1.66 g ash-free dry weight (AFDW) m72 y71, a production (P) of 4.51g m72 y71 and a P:B ratio of 2.72 at the outer part of the lagoon and a N of 14,570 ind m72, a B of 3.2 g AFDW m72 y71, a P of 9.9 g m72 y71 and a P:B ratio of 3.09 at the innermost part. At the innermost part of the lagoon, where the seawater renewal rate and hydro-dynamism were lower and the sediment ¢ner and organically richer, V. maritima displayed more recruitment pulses, a larger body size and a denser and more productive population than the one at the outer part. Our ¢ndings are compared to published data for the direct-developing congeners V.ventrosa and V.truncata.

INTRODUCTION body size and population density of mudsnail species (Forbes & Lopez, 1990; Grudemo & Johannesson, 1999), The amphi-Atlantic mudsnail species of the subfamily the study of life cycle, population dynamics and produc- Hydrobiinae (Rissooidea: Hydrobiidae) are frequently tivity of hydrobiinids, in relation to the degree of contact important elements of coastal habitats and a major source of the lagoonal habitat with the open sea, emerges as one of food for birds, ¢sh and other predators. Because of their of the research priorities in this highly £uctuating environ- signi¢cant role in brackish-water ecosystems, they have ment. become one of the most intensely studied molluscan The mudsnail species Ventrosia maritima (Milaschewich, genera in the world. Research topics involve parasitism, 1916) was, until very recently, only known from the Black energetics, deposit feeding and nutrition, reproductive Sea region. However, by applying mitochondrial DNA e¡ort and food chain resources, migration patterns and sequencing and phylogenetic tools, the occurrence of this dispersal, as well as population genetics and speciation. species was ascertained in the Evros Delta, northern However, some aspects of their biology and ecology, such Aegean. Additionally, the ¢rst detailed data concerning as life history, population dynamics and productivity, its ecology and distribution in a lagoon system were given have been studied only in few selected species. The direct- (Kevrekidis et al., 2005). Ventrosia maritima proved to be a developing Ventrosia ventrosa (Montagu, 1803), a typical ‘typical’ lagoonal species displaying its highest abundances lagoonal species and the larviparous Peringia ulvae in the innermost and isolated lagoonal parts. However, to (Pennant, 1777), a species of marine origin, are our knowledge, life cycle, population dynamics and examples (Siegismund, 1982; Bachelet & Yacine-Kassab, productivity of this species have not been described 1987; Barnes, 1994; Drake & Arias, 1995; Probst et al., yet. Although some information is available from the 2000). Most of these studies deal with mudsnail local Russian, Ukrainian, Romanian and Bulgarian populations from north-western Europe and north- literature (Chukhchin, 1976), it is not possible to assign eastern America. However, little is known about the these data to certain mudsnail species. Part of the biology and ecology of the mudsnail species at low problem is that numerous, often indistinguishable muds- salinities (55 psu). As the habitat type may well a¡ect nail species, have been reported from the Black Sea

Journal of the Marine Biological Association of the United Kingdom (2005) 376 T. Kevrekidis and T.Wilke Biology and ecology of Ventrosia maritima

Table 1. The range of several abiotic variables of water and sediment (after Kevrekidis, 2004) and Spearman’s rank correlation coe⁄cient values between these variables and the percentage of Ventrosia maritima individuals having a shell length 41.1 mm (r1) or density of V. maritima (r2)atStationsI1 and B2.

Station I1 Station B2

Variable Range r1 r2 N Range r1 r2 N

Water Depth (cm) 50^85 0.023 n.s. 70.234 n.s. 13 30^55 0.599 n.s. 0.209 n.s. 11 Salinity (psu) 0.3^5.6 0.824 ** 0.413 n.s. 13 0.3^5.7 70.407 n.s. 0.459 n.s. 13 71 Dissolved O2 (mg l ) 6.05^14.7 70.276 n.s. 0.465 n.s. 11 9.78^18.0 0.045 n.s. 70.036 n.s. 11 O2 saturation (%) 74^122 70.284 n.s. 0.364 n.s. 11 101^220 0.100 n.s. 0.018 n.s. 11 pH 7.4^9.1 70.279 n.s. 0.041 n.s. 13 7.45^9.32 0.501 n.s. 0.113 n.s. 13 Temperature (8C) 1.8^26.7 0.259 n.s. 70.511 n.s. 13 4.2^28.5 70.077 n.s. 70.203 n.s. 13 Sediment Temperature at 1 cm (8C) 2.1^26.6 0.283 n.s. 70.470 n.s. 13 3.7^27.0 70.025 n.s. 70.160 n.s. 13 Temperature at 5 cm (8C) 1.9^26.5 0.283 n.s. 70.470 n.s. 13 3.5^28.6 70.033 n.s. 70.198 n.s. 13 Median diameter (Md) (mm) 143^176 0.156 n.s. 0.161 n.s. 13 94^129 70.244 n.s. 0.050 n.s. 13 Organic matter (%) 0.15^1.73 0.868 *** 0.498 n.s. 13 0.48^2.20 0.220 n.s. 0.330 n.s. 13 n.s., not signi¢cant; **, P50.01; ***, P50.001.

region. Moreover, di¡erent names are used in di¡erent MATERIALS AND METHODS littoral states. Study area Preliminary genetic data (Thomas Wilke, unpublished data; Kevrekidis et al., 2005) indicate that the actual The Evros Delta is located at the north-eastern part of number of mudsnail taxa in the Black Sea region might the Aegean Sea. Fresh water £ows into the delta area both be low. In fact, all populations studied so far from the through the eastern and western branches of Evros River Black, Asov and Aegean Seas appear to be conspeci¢c as well as through the streams Mikri Maritsa and and belong to V. maritima (based on comparative genetic Loutron. Three islets and some lagoons have been formed studies of topotypes from Sevastopol, Ukraine). It should in the delta area. Monolimni (or Paloukia) Lagoon occu- be noted that V. maritima is a larviparous taxon character- pying an area of about 1.12 km2 communicates with the sea ized by a small initial whorl, *175 mm in diameter mainly through a 15m wide opening at its north-west end. and a planktotrophic protoconch 2 comprising about In July 1997, water salinity near the bottom varied 1.5 whorls (Anders Ware¤ n & Thomas Wilke, between 30.0 and 31.5 psu overall in Monolimni Lagoon. unpublished data). All other known Ventrosia species are An increased freshwater in£ow during winter and spring direct-developing. Wilke & Davis (2000) suggested that of 1998 following a period of intense rainfall on the river di¡erent life styles (i.e. direct developing species versus catchment area resulted in a sharp decline in salinity species with pelagic larvae) may have signi¢cant e¡ects values during February 1998 to February 1999. The on population structures of those species. With this in monthly variation in the values of water and sediment mind, one would expect that V. maritima may di¡er in physicochemical parameters during February 1998 to important ecological features from its direct-developing February 1999 at Station I1 (located at the outer southern congeners. part of the lagoon) and at Station B2 (located at the inner- The main goals of this study are: (1) to describe the most northern part of the lagoon and where seawater biological and ecological characteristics of the mudsnail renewal rate and the hydrodynamism are lower) has been taxon V. maritima in the Evros Delta (Aegean Sea) such as given by Kevrekidis (2004). Salinity and temperature life cycle, growth, population dynamics and productivity; showed similar values at both stations throughout the (2) to investigate the variability of those characteristics in annual cycle. Salinity was lower than 1psu during winter relation to the degree of contact with the sea; and (3) to and spring, while it varied between 1.2 psu and 5.7 psu compare the present data with available data for direct- during summer and autumn; water temperature was developing Ventrosia species in order to ¢nd possible di¡er- lower than 108C during February^March 1998 and ences between taxa with di¡erent life styles. November 1998^February 1999, being lowest in December The present study could help to deduce ¢ne-scale ecolo- 1998 (1.88C at Station I1and 4.28C at Station B2) and higher gical di¡erences among cryptic mudsnail species, which, than 208C in summer and early autumn; sediments were in turn, might aid in the identi¢cation of those taxa in the ¢ner at Station B2 (very ¢ne sand) than at Station I1 (¢ne absence of molecular markers. Moreover, it will also sand), while sediment organic matter content was higher at contribute to a better understanding of processes and Station B2 (mean 1.1%) than at Station I1 (mean 0.73%), patterns in the macrozoobenthic community in the Evros where it was lowest during February^June 1998 (0.15^ Delta, which is a wetland of international value according 0.45%) and December 1998^February 1999 (0.27^0.88%) to the RAMSAR convention, and of the Mediterranean (Kevrekidis, 2004). Table 1 shows the £uctuations of all coastal brackish water habitats in general. these environmental parameters over that period.

Journal of the Marine Biological Association of the United Kingdom (2005) Biology and ecology of Ventrosia maritima T. Kevrekidis and T.Wilke 377

Figure 2. Population structure of Ventrosia maritima at Station B2 in Monolimni Lagoon.

(500 kg), was recorded in Monolimni Lagoon in 1998, according to the local ¢shery service.

Data collection and analyses Monthly samples of macrobenthic fauna were collected during February 1998^February 1999 at the sampling Stations I1 and B2. At each station, four random sampling units were taken each time with a vanVeen special sampler with handles; the sampler covered a surface of 400 cm2 (20 20 cm) and penetrated to a depth of 20 cm. The  Figure 1. Population structure of Ventrosia maritima at Station samples were sieved on a 500-mm mesh sieve and the I1 in Monolimni Lagoon. animals were kept in a 5% formalin solution. Further details on sampling are given by Kevrekidis (2004). At Station I1, two of the sampling units were sieved on the The structure of the macrozoobenthic assemblages in 500-mm mesh sieve under which a 250-mm mesh sieve both parts (Stations I1 and B2) of Monolimni Lagoon had been placed. throughout February 1998^February 1999 has been In the laboratory, mudsnail individuals were separated described by Kevrekidis (2004). A Ruppia maritima L. from the remaining macrobenthos. A number of mud- meadow occurred in the innermost part of the lagoon, snails collected in March, May, July, September, while macroalgae were occasionally observed in both November 1998 and January 1999 at Station B2 and in parts of the lagoon. An annual ¢shing production of August, October, December 1998 and February 1999 at 11,100 kg, primarily consisting of Mugilidae (10,500 kg) Station I1 (20 mudsnails per month) were used to study and particularly of Mugil cephalus Linnaeus, 1758, Liza the penis type of male individuals, ensuring that all indi- aurata Risso, 1810 and L. saliens Risso, 1810, and the cata- viduals belonged to the same radiation. The characteristics dromous migrant Anguilla anguilla (Linnaeus, 1758) of all individuals studied (Kevrekidis et al., 2005) are

Journal of the Marine Biological Association of the United Kingdom (2005) 378 T. Kevrekidis and T.Wilke Biology and ecology of Ventrosia maritima indicative of the genus Ventrosia. DNA sequencing and RESULTS phylogenetic analyses of mudsnails collected at Stations I 1 Population structure and growth and B2 on 17 July 1999 indicated that the hydrobiid taxon from Monolimni Lagoon belongs to the species Ventrosia The population structure of Ventrosia maritima at Stations maritima (Milaschewich, 1916) (Kevrekidis et al., 2005). I1 and B2 for each sampling date is provided in Figures 1 The individuals of V. maritima retained on the 500-mm and 2 respectively, by length^frequency histograms. The mesh sieve were measured, decalci¢ed in a 10% HCl solu- smallest V. maritima individual found had a shell length of tion and counted. Shell length (L, from apex to anterior 0.63 mm at Station I1 and of 0.55 mm at Station B2. The margin of the aperture) was measured with the aid of an largest length values varied between 2.6 and 3.25 mm at eye-piece micrometer under a stereomicroscope to the Station I1 and between 3.18 and 4.78 mm at Station B2 nearest 0.025 mm. The presence of small individuals of throughout the sampling period. It should be mentioned V. maritima on the 250-mm mesh sieve was examined only that no individuals of V. maritima were found in the in order to obtain supplementary information concerning 250-mm mesh sieve during the study period at Station the recruitment period. I1. Development in time of the size groups of V. maritima On the basis of shell length, individuals were aggregated delimited by means of the graphical analysis of the into size-classes; a size-class interval of 0.2 mm was frequency distributions is given in Figures 3 and 4. selected. The populations were analysed by the graphical Ventrosia maritima individuals of the smaller size-classes analysis of polymodal frequency distributions (Harding, (41.1mm) were mainly found from July to November at 1949). The signi¢cance of the seasonal variation in popu- Station I1 (Figure 1). A positive correlation was found lation density was tested by Kruskal^Wallis one-way between their percentages and salinity or sediment analysis of variance (ANOVA). Spearman’s rank correla- organic matter content (Table 1). The 1998 year-class was tion coe⁄cient (r) was applied to identify signi¢cant recruited in three groups (Figure 3). The ¢rst group was correlations between the percentages of individuals having a shell length 41.1mm and abiotic variables as well as between population density and environmental variables. The individuals collected in a given sampling unit (1126 ind, length range: 0.825^4.425 mm) were grouped into length-classes (29 classes, 0.125 mm each one). The indivi- duals of each length-class were decalci¢ed, their ash-free dry weight (weight loss after 2 h of incineration at 5508C of individuals previously dried at 1008C for 24 h) was determined and the average AFDW in each length- class was calculated. For the study of the relation shell length (L), ash-free dry weight (AFDW), the centre and the calculated average AFDW in each length class were used. Searching for the best description of that relation, we chose the equation AFDW bLa ¼ (where a, b are constants), which showed the highest posi- Figure 3. Development in time of the size groups of Ventrosia tive coe⁄cient of correlation. So, the simple allometry maritima at Station I1; dots, mean shell length; bar lines, standard deviation; numbers, percentages of size groups in the formula was transformed as follows: Log10 AFDW a Log L + Log b. ¼ total population. Size groups having a participation 10 10 percentage lower than 0.8% were not illustrated. Annual production was calculated by the size^ frequency Hynes’s method, since it was not possible to discriminate accurately the di¡erent overlapping cohorts at least in Station B2. The largest size-classes, which had a very low number of individuals, were grouped, since a possible overestimate by Hynes’s method might be caused by the very low numbers of individuals in the largest size groups. The formula used was Hynes’s formula as given by Menzies (1980).The formula is as follows:

i P i (nj nj 1) (WjWj 1)1=2 365=CPI (1) ¼ " j 1 À þ Á þ # Á X¼ where i the number of size-classes or ‘times loss’ factor; nj the¼ mean number of individuals in size-class j; ¼ Figure 4. Development in time of the size groups of Ventrosia Wj the mean weight of an individual in the jth size- maritima at Station B ; dots, mean shell length; bar lines, ¼ 1/2 2 class; (Wj Wj + 1) the geometric mean weight standard deviation; numbers, percentages of size groups in the ¼ between two size-classes and CPI the cohort production total population. Size groups having a participation interval in days. ¼ percentage lower than 0.8% were not illustrated.

Journal of the Marine Biological Association of the United Kingdom (2005) Biology and ecology of Ventrosia maritima T. Kevrekidis and T.Wilke 379 observed in July having a relatively large mean length (1.14 mm), suggesting that its recruitment had occurred several days earlier; this group grew rapidly during summer and attained a mean length of 1.7 mm in September (growth rate 0.28 mm month71) (Figure 3). The second and third recruitment groups were observed in September and October respectively; they grew rapidly and were incorporated into the existing groups contributing to the non-increase in mean size of the 1998 year-class during autumn (Figure 3).The mean size of the 1998 year-class also did not increase during winter (Figure 3). The 1997 year-class was present in the ¢rst sampling having a mean length of 2.05 mm; it started to grow from March onwards and attained a mean length of Figure 5. Monthly variation in population density (mean 2.42 mm in May (Figure 3). The mean size of the 1997 standard error) of Ventrosia maritima at Stations I1 and B2 in Æ year-class decreased after May (Figure 3) suggesting Monolimni Lagoon. mortality. The major part of the 1997 year-class vanished after July, while a small part survived up to November H 9.359, P50.01 in Station B ;n n n n 3) ¼ 2 1¼ 2¼ 3¼ 4¼ reaching a mean length of 2.6 mm. Therefore, V. maritima having the lowest values in spring and the highest ones in displayed an average life span of about one year and a autumn. At Station I1, population density gradually possible maximum of less than 1.5 years. increased from June (mean density 256 ind m72) onwards, Individuals smaller than 1.1mm were mainly found in especially in early and mid autumn (Figure 5). The June, November and January^February 1999 at Station highest value was recorded in October (mean density: 72 B2 (Figure 2) indicating that annual recruitment mainly 30,250 ind m ) (Figure 5); afterwards, density gradually occurred in early summer and in autumn, but in mid or decreased until the last sampling (mean density: late winter as well. No signi¢cant correlation between 15,137 ind m72) (Figure 5). Population density at Station 72 their percentages and the examined abiotic variables was B2 increased from May (mean density: 4368 ind m )to found (Table 1). The 1998 year-class was recruited in four November (mean density: 38,675 ind m72) (Figure 5); groups (Figure 4). The ¢rst group was observed in this increase, which was intense in September and February^March 1998; its mean size increased during November, was temporarily interrupted in July and spring. This group overlapped with the 1997 year-class in October (Figure 5). From November onwards, density May and with the second recruited group from July decreased until February 1999 (mean density: onwards (Figure 4). The second group was observed in 15,837 ind m72). At both stations, population density was June (mean length 0.98 mm), grew rapidly and attained a much higher in February 1999 than in February 1998. mean length of 2.5 mm in September (growth rate No signi¢cant correlation between density of V. maritima 0.51mm mo71) (Figure 4); this group appeared about one and the examined physicochemical parameters was month earlier and reached a larger size in September found at both stations (Table 1). Nevertheless, it showing a faster growth rate than the ¢rst recruited should be mentioned that the decrease in population group at Station I1. The third and fourth recruited groups density of V. maritima during winter (Figure 5) were observed in September and November respectively; coincided with a decline in both temperature and salinity they grew rapidly and were incorporated into the existing values. groups contributing to the non-increase in the mean size of The density of V. maritima throughout the study period the 1998 year-class during autumn (Figure 4). The mean was signi¢cantly correlated with the density of only a few size of the 1998 year-class did not increase during winter species (Table 2).There was a positive correlation with the either (Figure 4). Some large individuals separated from density of the bivalve Abra ovata at Station I1 and that of the main body of this year-class in January^February Chironomidae larvae at Station B2 (Table 2) induced by 1999 suggests mortality among the adults. Individuals coincident £uctuations. A signi¢cant negative correlation born in 1997 were present in February 1998 (mean length was found between V. maritima and the small (52 cm) 2.47 mm); their mean size decreased in March and May polychaete Streblospio shrubsolii at Station I1 (Table 2); the (Figure 4) indicating mortality. Most of the 1997 year highest abundances of V. maritima in mid and late autumn class disappeared after May; a small part persisted until coincided with a gradual decline in population density of winter, attaining a mean length of about 4 mm. Therefore, S. shrubsolii at Station I1 (Kevrekidis, 2005), possibly the average life span of V.maritima at Station B2 was about suggesting a signi¢cant competitive interference. Streblospio one year. The ¢rst recruitment group of the 1999 year- live in the upper 2^3 cm of the sediments and are suspen- class was observed in January 1999 (Figure 4). sion and surface-deposit feeders.

Population density Length/weight relationship

The mean annual density of Ventrosia maritima was There exists a positive correlation between Log10 higher at Station B (14,571.7 individuals m72) than at AFDW and Log L(r 0.982; N 29). The regression 2 10 ¼ ¼ Station I (9743.8 individuals m72). Density showed a equation was: Log AFDW 2.088 Log L71.362. 1 10 ¼ Â 10 signi¢cant seasonal variation at both stations (Kruskal^ There also exists a positive allometry for the relation Wallis one-way ANOVA: H 8.436, P50.05 in Station I ; Log AFDW, Log L since a41(a 2.088), which means ¼ 1 10 10 ¼ Journal of the Marine Biological Association of the United Kingdom (2005) 380 T. Kevrekidis and T.Wilke Biology and ecology of Ventrosia maritima

Table 2. The range of the density (individuals m72)oftheconstantandabundantmacrozoobenthicspeciesthroughoutthesampling period at Stations I1 and B2 (after Kevrekidis, 2004) and Spearman’s rank correlation coe⁄cient (r)valuesbetweendensityof Ventrosia maritima and that of each one of these species (N 13). ¼

Station I1 Station B2

Taxa Density range r Density range r

Corophium orientale Schellenberg, 1928 69^21156 0.231 n.s. 94^8081 0.555 n.s. Abra ovata (Philippi, 1836) 0^825 0.714 * 1225^5262 0.549 n.s. Streblospioshrubsolii(Buchanan, 1890) 281^3831 70.791 ** 81^6763 70.423 n.s. Hediste diversicolor (O.F. Muller, 1776) 106^1625 0.346 n.s. 312^1250 70.311 n.s. Gammarus aequicauda (Martynov, 1931) 50^1112 70.126 n.s. 44^2050 0.429 n.s. Chironomidae larvae 0^7437 0.632 * Cumacea 0^1494 0.448 n.s.

*, P50.05; **, P50.01; n.s., not signi¢cant.

Table 3. Production estimates of Ventrosia species at di¡erent localities; B, mean annual biomass; P, annual production.

B P Species Habitat (g AFDW m72)(g AFDW m72) P:B Authors

V. truncata Parker River, Massachusetts, USA Salt marsh pool 11.2 67.7 or 78.1a 6.0 or 7.0 Mandracchia & Ruber (1990) V. ventrosa Kysing Fjord, Denmark Fjord estuary 4.6d 5.5 or 8.4b 1.2 or 1.8d Siegismund (1982)c Bay of Cadiz, Spain Lagoon 0.5 1.0a 2.0 Drake & Arias (1995) V. maritima Monolimni Lagoon, Greece a Station I1 Lagoon 1.7 4.5 2.7 Present study a Station B2 Lagoon 3.2 9.9 3.1 Present study

Notes: a, values estimated by the size^frequency method; b, values estimated by the Crisp’s method or a modi¢cation of Crisp’s method; c, values estimated over a ten month period; d, values calculated by Bachelet & Yacine-Kassab (1987) according to author’s data.

that Log10 AFDW increases faster than Log10 L. The ably contributed to the autumn recruitment. Evidence of AFDW can be converted to dry weight (DW) using the late summer or autumn breeding of the young-of-the- equation: DW 1.334 AFDW, where the value 1.334 was year of its congener V. ventrosa was observed both in the obtained from¼ the data on mean percentage of ashes for laboratory and in the ¢eld (Barnes, 1994; Probst et al., V.maritima. 2000). Lassen & Clark (1979) reported that Atlantic V. ventrosa takes about three months to reach sexual maturity at lower temperatures and higher salinities (158C and Secondary production 20 psu, respectively) than those occurring in Monolimni The 365/CPI ratio was assumed to be unity since the lagoon during summer and early autumn. Recruitment production interval was about one year. The calculations was not observed in winter and spring. Very low tempera- of the size^frequency method showed that the values of n tures (5108C) during winter and early spring and extre- (mean annual density), B (mean annual crop), P (annual mely low salinities (51psu) throughout winter and spring production) and P:B (annual turnover ratio) are equal to possibly deterred breeding of V. maritima. Field data from 9743.8 ind m72, 1.66 g AFDW m72 (or 2.21g DW m72 northerly habitats indicated that 108C is the temperature using the equation DW 1.334 AFDW), 4.51g AFDW threshold for breeding of V. ventrosa and laboratory experi- m72 (or 6.02 g DW m72)¼ and 2.72 respectively at Station ments revealed a sharp decrease or a cessation of its egg 72 72 I1 and 14,571.7 ind m , 3.20 g AFDW m (or 4.27 g DW production in salinities down to 5 psu (Lassen & Clark, m72), 9.90 g AFDW m72 (or 13.21g DW m72) and 3.09 1979). The low sediment organic matter content during respectively, at Station B2. winter and spring, which is a crude index of food avail- ability, probably resulting in slow growth rates, might have contributed to the absence of breeding. DISCUSSION At the innermost part of Monolimni Lagoon, recruit- Ventrosia maritima displayed an annual life cycle in ment of V.maritima also occurred in winter. Winter recruits Monolimni Lagoon. Recruitment occurred in summer were possibly derived from eggs laid in late autumn/early and autumn at the outer part of the lagoon. Summer winter, the development of which was possibly prolonged recruits were produced by over-wintering snails and prob- due to low temperatures and salinities (Lassen & Clark,

Journal of the Marine Biological Association of the United Kingdom (2005) Biology and ecology of Ventrosia maritima T. Kevrekidis and T.Wilke 381

1979; Fish & Fish, 1981). Autumn recruits, which grew Ventrosia maritima possibly is more tolerant to very low sali- faster than the respective ones at Station I1,possibly nities than its congeners V. ventrosa and V. truncata, since, matured during late autumn and contributed to that under laboratory conditions, V. ventrosa individuals winter recruitment. collected from the White Sea died after 60 days of staying Ventrosia ventrosa, the congener of V. maritima, is a short- in fresh water (Berger & Gorbushin, 2001) and individuals lived semelparous mud snail; its maximum life span varies of V. truncata (as H. totteni) maintained in salinities of 0 to between one and two years (Siegismund, 1982; Barnes, 5 psu were largely inactive (Wells, 1978). 1994; Drake & Arias, 1995; Probst et al., 2000). In north- Ventrosia maritima displayed more recruitment pulses and western European coastal habitats, V. ventrosa usually a higher density at Station B2 than at Station I1, although displays a single annual period peaking in summer it possibly su¡ered predation pressure and low oxygen (Lassen & Clark, 1979; Barnes, 1994; Probst et al., 2000), concentrations at night during summer (Kevrekidis, while in the south of its distribution range, at a shallow 2004). Moreover, the species also showed a faster growth coastal lagoon in the Bay of Cadiz, south-west Spain, and a larger body size at Station B2, despite the fact that where water temperature seasonally varies between 8 and increasing density depresses growth in mudsnails (Forbes 24.58C and salinity between 18 and 65 psu, it reproduced & Lopez, 1990). As a consequence, biomass, production throughout the year (Drake & Arias, 1995). Another and production/biomass ratio (P:B ratio) of V. maritima congener of V. maritima, the direct-developing V. truncata were also higher at Station B2. As water temperature and (Vanetta, 1924), which is found along the Atlantic coast of salinity showed similar values at both parts of the lagoon northern North America, also displayed an annual life throughout the annual cycle, the lower seawater renewal cycle in Massachusetts salt marsh pools; an annual rate, the lower hydrodynamism or/and the ¢ner and orga- recruitment occurred in summer (Mandracchia & Ruber, nically richer sediments at the innermost part probably 1990). enable V. maritima to establish a denser and more produc- Growth of both V. maritima populations at Monolimni tive population. Similarly, V. ventrosa and V. truncata gener- Lagoon practically ceased in winter, indicating low meta- ally attain a larger average body size and in some cases a bolic rates probably caused by the low water temperatures. higher density as well at protected habitats with ¢ne- A possible greater intraspeci¢c competition for food in late grained sediments (Forbes & Lopez, 1990; Grudemo & autumn and early winter, when densities peaked, might Johannesson, 1999). A low seawater renewal rate possibly have contributed to that cessation of growth. The impor- favours the survival, reproduction and growth of a typical tance of temperature in a¡ecting growth rates and the lagoonal species such as V. maritima. Guelorget & density-dependence of growth of Ventrosia species and, of Perthuisot (1992) hypothesized that ‘con¢nement’, which other hydrobiinid snails as well, were also previously represents the time of renewal with elements of marine reported (Forbes & Lopez, 1990; Drake & Arias, 1995). origin (e.g. trace elements, vitamins etc.), primarily deter- Extremely low salinities (51psu) during winter and mines the distribution and features of populations in spring might have negatively a¡ected growth rates of V. lagoonal ecosystems. Forbes & Lopez (1990) suggested maritima, but did not deter their increase during spring, that sediment transport events, the frequency of which while there is no evidence from earlier studies of the in£u- increases with increasing hydrodynamism, negatively ence of low salinities (55 psu) on the growth of mudsnails. a¡ect survival and time available for feeding in mudsnails. Population density of V. maritima increased from late Fine sediments have been considered to represent a richer spring or early summer to autumn following the summer food source for deposit-feeders like mudsnails than coarse and autumn recruitment. Winter recruitment at the inner- ones (Forbes & Lopez, 1990). most part of the lagoon did not result in an increase in The maximal shell lengths achieved by V. maritima in density. Predation pressure by the crab Carcinus aestuarii Monolimni Lagoon (3.3 mm at Station I1, 4.9 mm at and the goby Knipowitschia caucasica was possibly respon- Station B2) are in the range of those attained by various sible for the temporary decline of V. maritima density in populations of V. ventrosa (3.5^5.5 mm) (Barnes, 1994; July at Station B2 (Kevrekidis, 2004). An intense intraspe- Drake & Arias, 1995; Probst et al., 2000) and V. truncata ci¢c competition resulting from the peak abundances was (2^6 mm) (Forbes & Lopez, 1990; Mandracchia & possibly the prominent cause of the decline in population Ruber, 1990). The shell length/ash-free dry weight rela- density of V. maritima in late autumn. Probst et al. (2000) tionship has been described exponentially in several suggested that young snails of V. ventrosa emigrated from hydrobiinid populations. The exponent a showed a value densely populated areas by £oating at the water surface. of 2.1 in V. maritima, while it varied between 2.05 and 2.28 In addition, a high mortality due to low temperatures in some V.ventrosa populations (Siegismund, 1982; Drake & (54.58C) and salinities (51psu) possibly contributed to Arias, 1995). the decline in V. maritima density during winter. Field data Annual production and annual turnover ratio values of and laboratory experiments indicated that V. ventrosa from V. maritima are among those previously reported for other northern Europe is very tolerant even to subzero tempera- Ventrosia populations despite the extremely low salinities tures (Hyllenberg & Siegismund, 1987; Berger & occurring in Monolimni Lagoon (Table 3). Regarding Gorbushin, 2001), while under laboratory conditions the P:B, the values for V. maritima are higher than those of survivorship of V. truncata [as Hydrobia totteni (Totten)] V. ventrosa in the south of its distribution range (Bay of sharply decreased below 48C (Wells, 1978). However, the Cadiz, south-west Spain); Ventrosia ventrosa showed even occurrence of V. maritima in late winter and spring in lower P:B values in the north of its distribution range remarkable densities at salinities 51psu, and the increase (Kysing Fjord, Denmark) (Siegismund, 1982; Drake & in its growth rates in spring as well, indicate that this Arias, 1995) (Table 3). Accelerated maturity, protracted mudsnail is highly tolerant to extremely low salinities. breeding season and high P:B values probably typify

Journal of the Marine Biological Association of the United Kingdom (2005) 382 T. Kevrekidis and T.Wilke Biology and ecology of Ventrosia maritima low-latitude/warm-water Ventrosia populations. However, Grudemo, J. & Johannesson, K., 1999. Size of mudsnails Hydrobia the di¡erences in P:B ratio between the two populations ulvae (Pennant) and H. ventrosa (Montagu), in allopatry and of V. maritima in Monolimni Lagoon imply that local sympatry: conclusions from ¢eld distributions and laboratory factors, such as seawater renewal rate, hydrodynamism, growth experiments. Journal of Experimental Marine Biology and sediment type, etc., are also important in a¡ecting P:B Ecology, 239,167^181. Guelorget, O. & Perthuisot, J.P., 1992. Paralic ecosystems. ratio. Biological organization and functioning. Vie et Milieu, 42, Acknowledging that little comparative data are avail- 215^251. able for oligohaline mudsnail populations from southern Harding, J.P., 1949. The use of probability paper for the parts of their distribution areas (particularly the graphical analysis of polymodal frequency distributions. Mediterranean Sea), we have found signi¢cant ecological Journal of the Marine Biological Association of the United Kingdom, di¡erences between the larviparous Ventrosia maritima and 28,141^153. their direct-developing congeners V.ventrosa and V.truncata. Hylleberg, J. & Siegismund, H.R., 1987. Niche overlap in mud Future comparative studies and controlled experiments snails (Hydrobiidae): freezing tolerance. Marine Biology, 94, have to show whether these di¡erences are, at least in 403^407. part, due to the di¡erent life styles or whether climatic, Kevrekidis, T., 2004. Seasonal variation of the macrozoobenthic hydrological and eco-physiological features are responsible community structure at low salinities in a Mediterranean lagoon (Monolimni Lagoon, Northern Aegean). International for the observed characters. Review of Hydrobiology, 89,407^425. Kevrekidis, T., 2005 Population dynamics, reproductive biology This study was carried out in the Laboratory of Environ- and productivity of Streblospio shrubsolii (Polychaeta: Spionidae) mental Research and Education of Democritus University of in di¡erent sediments at low salinities in a Mediterranean Thrace (DUTH). Many thanks go to Ms V. Kalpia, Mr A. lagoon (Monolimni lagoon, Northern Aegean. International Mogias and Ms T. Boubonari for sampling and laboratory assis- Review of Hydrobiology, 90,100^121. tance. We would also like to thank three anonymous referees for Kevrekidis, T., Wilke, T. & Mogias, A., 2005. When DNA puts their valuable comments on a previous version of the paper. ecological works back on the right track: genetic assessment and distribution patterns of mudsnail populations in the REFERENCES Evros Delta lagoons. Archiv fu« r Hydrobiologie, 162, 19^35. Lassen H.H. & Clark, M.E., 1979. Comparative fecundity in Bachelet, G. & Yacine-Kassab, M., 1987. Inte¤ gration de la phase three Danish mudsnails (Hydrobiidae). Ophelia, 18,171^178. post-recrute¤ e dans la dynamique des populations du gaste¤ ro- Mandracchia, M.A. & Ruber, E., 1990. Production and life cycle pode intertidal Hydrobia ulvae (Pennant). Journal of of the gastropod Hydrobia truncata, with notes on Spurwinkia Experimental Marine Biology and Ecology, 111,37^60. salsa in Massachusetts salt marsh pools. Estuaries, 13,479^485. Barnes, R.S.K., 1994. Investment in eggs in lagoonal Hydrobia Menzies, C.A., 1980. A note on the Hynes’s method of estimating ventrosa and life-history strategies in north-west European secondary production. Limnology and Oceanography, 25,770^773. Hydrobia species. Journal of the Marine Biological Association of the Probst, S., Kube, J. & Bick, A., 2000. E¡ects of winter severity United Kingdom, 74,637^650. on life history patterns and population dynamics of Hydrobia Berger, V.Ya & Gorbushin, A.M., 2001. Tolerance and resistance ventrosa (Gastropoda: Prosobranchia). Archiv fu« r Hydrobiologie, in gastropod mollusks Hydrobia ulvae and H. ventrosa from the 148, 383^396. White Sea to abiotic environmental factors. Russian Journal of Siegismund, H.R., 1982. Life cycle and production of Hydrobia Marine Biology, 27,314^319. ventrosa and H. neglecta (Mollusca: Prosobranchia). Marine Chukhchin, V.D., 1976. Life cycle and growth of Hydrobia acuta Ecology Progress Series, 7,75^82. (Drap.) and H. ventrosa (Mont.) in the Black Sea. Biologiya Wells, F.E., 1978. The relationship between environmental vari- Morya, 37, 85^90. [In Russian.] ables and the density of the mud snail Hydrobia totteni in a Nova Drake, P. & Arias, A.M., 1995. Distribution and production of Scotia salt marsh. Journal of Molluscan Studies, 44,120^129. three Hydrobia species (Gastropoda: Hydrobiidae) in a Wilke, T. & Davis, G.M., 2000. Infraspeci¢c mitochondrial shallow coastal lagoon in the Bay of Ca¤ diz, Spain. Journal of sequence diversity in Hydrobia ulvae and Hydrobia ventrosa Molluscan Studies, 6, 185^196. (Hydrobiidae: Rissooidea: Gastropoda): do their di¡erent life Fish, J.D. & Fish, S., 1981. The early life-cycle stages of Hydrobia histories a¡ect biogeographic patterns and gene £ow? ventrosa and Hydrobia neglecta with observations on Potamopyrgus BiologicalJournal of the Linnean Society, 70,89^105. jenkinsi. Journal of Molluscan Studies, 47,89^98. Forbes, V.E. & Lopez, G.A., 1990. The role of sediment type in growth and fecundity of mud snails (Hydrobiidae). Oecologia, 83,53^61. Submitted 22 June 2004. Accepted 28 February 2005.

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