The Vertical Distribution of Chthamalus Montagui and Chthamalus Stellatus (Crustacea, Cirripedia) in Two Areas of the NW Mediterranean Sea

Home , Chthamalus, Chthamalus montagui, Chthamalus stellatus, Semibalanus balanoides

The vertical distribution of Chthamalus montagui and Chthamalus stellatus (Crustacea, Cirripedia) in two areas of the NW Mediterranean Sea

F. G. Pannacciulli∗ & G. Relini Laboratori di Biologia Marina ed Ecologia Animale, Dipartimento per lo Studio del Territorio e delle sue Risorse, Universit`a di Genova, Via Balbi 5, Genova, 16126, Italy E-mail: [email protected] (∗author for correspondence)

Key words: barnacle, Chthamalus montagui, Chthamalus stellatus, distribution, rocky shore, Mediterranean Sea

Abstract The Mediterranean Sea is characterised by a small tidal range (0.3–1 m). Despite this, intertidal communities are well established and their upper limits often extend above mean high water level. Organisms living in the intertidal region and in the supralittoral zone rely on both tides and wave action to perform their biological functions. Lack of food, desiccation and predation are common stresses in such a harsh environment. The present study deals with the vertical distribution of two species of intertidal barnacles, Chthamalus montagui Southward and Chthamalus stellatus (Poli), which are the main constituents of the barnacle belt along Mediterranean rocky shores. Previous work, carried out in the Atlantic, showed that where the distribution ranges of the two Chthamalus species overlap, C. montagui is more common in the upper barnacle zone while C. stellatus is dominant lower down. The main aims of our study are: (1) to establish if there is a relationship between position and extension of the barnacle belt on the shore and tidal range and/or wave exposure, (2) to test the hypothesis that in the study areas C. montagui is more abundant than C. stellatus high on the shore, and that the pattern is reversed lower down. Barnacle populations were monitored in summer 1998 in the Gulf of Genoa (Ligurian Sea) and in the Gulf of Trieste (North-Adriatic Sea). The two areas differ in tidal range and hydrodynamism, the former presenting quite strong wave action and a tidal range of 30 cm, the latter having limited wave action and 1 m tidal range. Three shores were randomly selected in each gulf and two transects on each shore. Counts of barnacles in 10 ∗ 10 cm quadrats were done at different shore heights along each transect. The data was subjected to analysis of variance. Results showed that a more pronounced hydrodynamic regime corresponded to a shift of the barnacle belt towards the higher shore (Gulf of Genoa), while in more sheltered areas (Gulf of Trieste), the barnacle distribution was conﬁned to the intertidal region. The relative spatial distribution of C. montagui and C. stellatus within the barnacle belt varied locally, even between transects on the same shore, and this obscured the distribution pattern along the vertical gradient. Nevertheless, it was still possible to conclude that at mid and high shore in Genoa, C. stellatus was more abundant than C. montagui, while in Trieste the pattern was reversed.

Introduction Among different species of intertidal barnacles, those belonging to the genus Chthamalus are very Barnacles are one of the dominant components of lit- common along the littoral zone of the NE Atlantic and toral communities. Because of their abundance and the Mediterranean shores. Until 1976, Chthamalus accessibility on the shore, their ecology has been the stellatus (Poli) was considered to be the only repres- subject of studies for over 100 years. Darwin (1851, entative of this genus in Europe (with the exception 1854) fully realised that many species of cirripedes of Euraphia depressa (Poli) which in the past was er- had a strong intertidal preference. According to Lewis roneously considered to belong to it). Several authors (1964), barnacles are almost ubiquitous and are the (Moore & Kitching, 1939; Southward, 1950, 1963; dominant and most characteristic organisms of the Connell, 1961) described distribution of the C. stel- eulittoral zone throughout the world. latus, along latitudinal and wave exposure gradients, 106 and related its vertical distribution on the shore to the intertidal region and in the supralittoral zone rely several factors including competitive interactions with on tides and wave action to perform their biological other species (e.g. Semibalanus balanoides (L.) in functions. the Atlantic). Other authors (Barnes & Barnes, 1964; The present study was carried out on six shores Kensler et al., 1965; Klepal, 1971; Relini, 1983) con- along the northern Italian coast (Mediterranean Sea) centrated their attention on the horizontal and vertical and deals with the vertical distribution of the main distribution of C. stellatus in the Mediterranean and its constituents of the barnacle belt: C. montagui and C. competition with Euraphia depressa. stellatus. Euraphia depressa, a species endemic to With regard to Chthamalus distribution, the con- this basin, is the third barnacle species found along clusion emerging from these studies is that physical Mediterranean shores. In the areas of study, Euraphia factors limit the distribution at the upper part of the lives in crevices and shadowed areas of the supralit- shore, while the combination of physical and biolo- toral zone and seldom enters in the formation of the gical factors operates at the lower level. In fact, brief barnacle belt on open rocks. For this reason, Euraphia exposure to seawater and consequent problems with has not been included in the investigations. desiccation and poor food supply would be the main This study had two main aims: constraints for individuals living higher on the shore, 1. to establish if there is a relationship between posi- while competition for space, predation and strong tion and extension of the barnacle belt on the shore wave action would be limiting factors at mid and low and tidal range and/or wave exposure; shore. Furthermore, according to Hawkins & Hartnoll (1982), the presence of algal turf would set the lower 2. to test the hypothesis that in the study areas, C. limit of the barnacle distribution. montagui is more abundant than C. stellatus high Southward (1976) separated the species Chthamalus on the shore, and that the pattern is reversed lower montagui Southward from C. stellatus. Following down. this separation, Crisp et al. (1981) and Burrows (1988) investigated the relative distribution of the two Chthamalus species along geographical and vertical Materials and methods gradients. From their work, it appears that the two species can occasionally be separated by habitat, with Study sites C. stellatus being dominant on exposed shores and C. montagui on moderately sheltered ones. Where the The study was carried out in two areas of the NW two species overlap, C. montagui is more common in Mediterranean Sea: the Gulf of Genoa (44◦ 240 N, the upper barnacle zone (MHWS and MHWN), while 8◦ 540 E) in the Ligurian Sea and the Gulf of Trieste C. stellatus is dominant lower down (MTL and below). (45◦ 390 N, 13◦ 460 E) in the north part of the Ad- Occasionally, in wave-washed, wet or shaded places, riatic Sea, Italy (Figure 1). The two areas differ in C. stellatus can occur higher up on the shore. Accord- tidal range and hydrodynamism, the former presenting ing to Burrows (1988), processes of larval dispersal, quite strong wave action and a tidal range of 30 cm, larval development and settlement appear to be the the latter having more limited hydrodynamism and most important factors producing the different adult 1 m tidal range. Wave action is determined by sev- distributions in the two species. Juvenile mortality eral factors including wind direction, local topography could also account for this. In fact, due to morpho- and hydrography. In Genoa, dominant winds blow off- logical differences in the shape of the opercular plates, shore (from north) and inshore (from south-west); the C. stellatus is believed to be more susceptible to de- inshore wind, in conjunction with the open coast and a siccation during early life stages than C. montagui steep continental shelf, generates high hydrodynamic (Foster, 1971). In addition, C. montagui juveniles forces in the area. In contrast, the more embayed seem to require exposure to air in order to be able to situation of the Gulf of Trieste, together with dom- consolidate their shell plates (Burrows, 1988). inant winds blowing offshore (from north-east) and The Mediterranean Sea, in common with most en- very shallow waters (50 m on average) create a more closed seas, is characterised by a small tidal range sheltered condition. (0.3–1 m). Despite this, shore communities are well established in this area and their upper limits are often extended above high water level. Organisms living in 107

Table 1. ANOVA on the effect of shore height on Chthamalus species distribution

Source of variation DF MS F

Species = Sp 1 66.67 Height = He 2 86 443.56 Locality = Lo 1 154 989.80 Shore (Lo) 4 7875.12 Transect (Lo × Shore) 6 5910.06 Sp × He 2 2011.10 Sp × Lo 1 173 853.63 Sp × Shore (Lo) 4 34 751.61 Sp × Transect (Lo × Shore) 6 3138.32 He × Lo 2 18 052.59 He × Shore (Lo) 8 11 330.16 He × Transect (Lo × Shore) 12 3195.66 ∗∗ Sp × He × Lo 2 42 473.14b 51.33 Sp × He × Shore (Lo)b 8 827.47 ∗∗ Sp × He × Transect (Lo × Shore) 12 4164.42a 5.16 Residuala 144 807.76

Cochran’s test C = 0.1091, not signiﬁcant Transformation none

Superscripts are used to identify the appropriate denominator for each test. The term in the model sharing the superscript of any mean square is the term whose mean square is used in the denominator of the F-ratio for the test.

Methods air pressure can sometimes be greater than that due to tides. Sampling, to determine the density of the two The study was carried out in summer 1998. To test Chthamalus spp., was carried out at five levels set at for local spatial variation, three shores (Figure 1) were equal vertical intervals along the transect and within randomly selected in each gulf (S. Chiara, Pontetto the barnacle zone. Due to the very narrow barnacle and P. Chiappa in the Gulf of Genoa and Barcola, S. distribution present at S. Chiara, it was only possible to sample three levels out of five on this shore. In each Croce and Aurisina in the Gulf of Trieste) and two ∗ transects (A and B) on each shore. Shores were selec- transect, three randomly placed 10 10 cm replicate ted from those presenting barnacles but not showing quadrats were used to estimate densities for each spe- peculiarities; they were a few kilometres apart and cies separately at each of the five levels. In fact, for covered the range of exposure typical of the area. With data to be independent (one of ANOVA’s assumptions) regard to this last feature, shores in Trieste were al- values for one species had to come from replicates ways quite sheltered, while those in Genoa had a wide different from the ones used for the other species. range of exposure (in our study S. Chiara was the To avoid bias related to time of sampling, only most sheltered one, while P. Chiappa was the most adult individuals, belonging to class 1+ or above, were exposed). Transects were selected on open rock, were included in the counts. 10–100 m apart and stretched from the lower to the The distribution pattern of C. montagui and C. stel- upper limit of the barnacle belt. Barnacles were con- latus along the vertical gradient was investigated using sidered to have reached their distribution limit where a 5-way Analysis of Variance (ANOVA). The factors densities of less than 1 ind. m−2 were recorded. involved in the analysis were: species (2 levels), shore The heights of the upper and lower Chthamalus height (3 levels, from now onwards referred to as spp. zone were set with reference to Chart Datum height), locality (2 levels), shore (3 levels) and transect (CD), values were adjusted in relation to the air pres- (2 levels). The number of replicates for each treatment sure present at the time of monitoring. In microtidal was three. Species, height and locality were fixed or- environments, variation of the mean sea level due to thogonal factors, while shore was random and nested 108

Homogeneity of variance was assessed by Co- chran’s C test (Underwood, 1997). Student-Newman- Keuls (SNK) test (α = 0.05) was employed for multiple comparisons of the means. Data were analysed with the programme GMAV5 (Underwood & Chap- man, 1998).

Results

The ﬁrst aim of our study was to establish whether there is a relationship between the position of the barnacle belt on the shore and tidal range and/or wave exposure. The extension and position of the barnacle belt along a given transect varied between the shores of the two study areas (Figure 2). In the Gulf of Genoa, the vertical distribution of barnacles stretched from 10 cm (S. Chiara transect A) to 205 cm above CD (P. Chiappa transect A). In this area, nearly all barnacles were found above extreme mean high water level (EMHW) which, due to the very limited tidal range, is situated at only 30 cm above CD. In addition, as the exposure gradient increased, the barnacle distribution shifted further up-shore. Barnacle distribution in the Gulf of Trieste was different, the belt stretching from −3to 105 cm above CD, hence conﬁning Chthamalus spp. to the intertidal region. No trend relative to exposure emerged from the data. The second aim was to test the hypothesis that in the study areas C. montagui is more abundant than C. stellatus high on the shore, and that the pattern is reversed lower down. Figures 3 and 4 show the relative distribution of the two species in Genoa and in Trieste. To allow comparisons across shores and localities, vertical levels were related to their position within the barnacle belt (high, mid high, mid, mid low and low) and not to Chart Datum. In the Gulf of Genoa (Figure 3), C. stellatus was more abundant than C. montagui at most levels. Here, barnacles reached their peak density around mid Figure 1. Maps showing the two study sites (Gulf of Genoa (A) and and mid low shore. In the Gulf of Trieste (Figure 4), Gulf of Trieste (B)) and the six shores (S. Chiara, Pontetto, etc.) individuals of C. montagui were far more abundant where the study was carried out. than those of C. stellatus (several hundreds against a few tens). The highest abundance of C. montagui was found around mid high level on all shores, while the greatest densities of C. stellatus were recorded at in locality and transect random and nested in shore low/mid low levels. and locality. The number of levels of factor height was The levels high, mid and low were employed in the reduced from 5 to 3 due to S. Chiara where only three Analysis of Variance (Table 1). The interaction Sp ∗ levels were monitored. He ∗ Transect (Lo ∗ Shore) was shown to be highly 109

Figure 2. Box plots represent position and extension of the barnacle belt along a given transect (A or B) at one shore (e.g. S. Chiara, Pontetto, etc.). The area between dotted lines represents the intertidal region where: EMHW = Extreme Mean High Water, EMLW = Extreme Mean Low Water. significant, therefore indicating that even between main factor responsible for the vertical distribution of transects of the same shore the interaction Sp ∗ He barnacles. changed. Despite this, the interaction Sp ∗ He ∗ Lo Two areas with different tidal range and expos- was still significant, suggesting that variation between ure were selected for this study: the Gulf of Genoa, localities was greater than variation between transects. which can be considered as representative of the NW Multiple comparisons carried out on the interaction Sp Mediterranean, and the Gulf of Trieste in the north ∗ He ∗ Lo showed that at mid and high shore in Genoa, Adriatic Sea. Genoa is characterised by strong wave C. stellatus was significantly more abundant than C. action and tidal range of 30 cm, Trieste presents shal- montagui, while in Trieste the pattern was reversed. low waters, moderate wave action and 1 m tidal range Thus, C. montagui was not the dominant barnacle spe- (an exceptional value for the Mediterranean Sea). Res- cies higher on the shore in both study areas nor was C. ults showed that barnacles in Trieste were confined to stellatus the most common one on the lower shore. the intertidal region, while in Genoa, their distribution stretched further up-shore as the rate of exposure increased. Discussion The upper limit of the Chthamalus distribution in the Mediterranean is considered to be set by physical The position and extension of barnacle belts on the factors, as Barnes & Barnes (1964) pointed out. Medi- shore are generally related to tidal range and grade terranean barnacles living on the upper shore have to of exposure of the coast. In a microtidal environment, deal with an extreme environment where a scarce wa- such as the Mediterranean Sea with a mean tidal range ter supply, and consequently a lack of food, together of 30 cm, wave exposure can be considered to be the 110

∗ Figure 3. Vertical distribution of C. montagui (left) and C. stellatus (right) on three shores in the Gulf of Genoa. In each transect, three 10 10 cm replicate quadrats were used to estimate densities for each species separately at each of the ﬁve levels within the barnacle belt. Mean values and standard errors are reported. with desiccation and high air temperature limit the sublittoral organisms, such as coralline algae or other distribution. This could explain why Chthamalus was rock-encrusting forms, determined this limit. Barnes absent from the area above the upper tidal level in & Barnes (1964) supported the theory of competi- Trieste, which is seldom reached by water, while it was tion, but suggested that local topography and wave present in Genoa, where wave action is more intense. action could also be involved. Thus, there can be sev- The factors setting the lower limit of Chthamalus eral reasons why the distribution of Chthamalus does distribution have been suggested to be either physical not extend lower on the shore in our study areas and or biological. Moore & Kitching (1939) could not de- various models can be proposed to explain the ob- cide whether excessive immersion or competition with served pattern. Among these, competition with algae, 111

∗ Figure 4. Vertical distribution of C. montagui (left) and C. stellatus (right) on three shores in the Gulf of Trieste. In each transect, three 10 10 cm replicate quadrats were used to estimate densities for each species separately at each of the five levels within the barnacle belt. Mean values and standard errors are reported. supply-side processes, settlement behaviour and pred- (Southward, 1976; Crisp et al., 1981, Burrows, 1988; ation should be considered and investigated in future Pannacciulli, 1995). A brief account on the distribu- studies. tion in the Mediterranean was published by Crisp et al. Little is known as to the relative distribution of C. (1981) and Relini (1983). Our work, therefore, aimed montagui and C. stellatus along the vertical gradient to expand their investigations and verify whether the on Mediterranean rocky shores. Since the separation pattern of Chthamalus distribution described for the of C. montagui from C. stellatus by Southward in Atlantic was also valid in the Mediterranean. 1976, most of the studies related to the distribution Our investigations showed that the spatial vari- of the two species were carried out in the Atlantic ation in the two study areas was high with interac- 112 tions between species and shore height changing even long des côtes méditerranéennes d’Espagne et de France. Bull. from one transect to the other. Nevertheless, some Inst. océanogr. Monaco 62: 1–19. conclusions could still be drawn. Burrows, M. T., 1988. The comparative biology of Chthamalus stellatus (Poli) and Chthamalus montagui Southward. Ph. D. Thesis, In Genoa, where wave action prevails over tides, University of Manchester: 318 pp. the two Chthamalus spp. appeared to be equally dis- Connell, J. H., 1961. The influence of interspecific competition tributed along the vertical gradient, although C. stel- and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42: 710–723. latus was in general more abundant at all levels. This Crisp, D. J., A. J. Southward & E. C. Southward, 1981. On result contrasts with the assumption that C. stellatus is the distribution of the intertidal barnacles Chthamalus stellatus, dominant at MTL and below (Southward, 1976). On Chthamalus montagui and Euraphia depressa.J.mar.biol.Ass. the other hand, the same author also quotes that in U.K. 61: 359–380. Darwin, C., 1851. A Monograph on the sub-class Cirripedia. The wave-beaten places, such as the west coast of Ireland, Lepadidae; or, pedunculated cirripedes. Ray Society, London: C. stellatus can form 30–70% of the total Chthamalus 400 pp. population. This last consideration agrees well with Darwin, C., 1854. A Monograph on the sub-class Cirripedia. The our observations on the wave exposed coast of Genoa. Balanidae; the Verrucidae, etc. Ray Society, London: 684 pp. Foster, B. A., 1971. Desiccation as a factor in the intertidal zonation In contrast, in Trieste, C. montagui was the domin- of barnacles. Mar. Biol. 8: 12–29. ant species at all levels and showed peaks in density Hawkins, S. J. & R. G. Hartnoll, 1982. Settlement patterns of in the upper part of the shore. Conversely, C. stel- Semibalanus balanoides (L.) in the Isle of Man (1977–1981). J. latus appeared to be very scarce above MTL, while exp. mar. Biol. Ecol. 62: 271–283. Kensler, C. B., K. M. Bhatnagar & D. J. Crisp, 1965. Distri- its abundance increased lower down. These results bution and ecological variation of Chthamalus species in the are quite consistent with the suggestion Southward Mediterranean area. Vie Milieu (sér B) 16: 271–294. (1976), i.e. C. montagui is the dominant species in Klepal, W., 1971. Chthamalus stellatus (Poli) und C. depressus sheltered places and where the two Chthamalus spp. (Poli) in der Adria. J. exp. mar. Biol. Ecol. 7: 271–294. Lewis, J. R., 1964. The Ecology of Rocky Shores. The English co-occur, C. montagui is usually more abundant at Universities Press Ltd., London: 323 pp. MHW. Moore, H. B. & J. A. Kitching, 1939. The biology of Chthamalus A more extensive study, on a broader geograph- stellatus (Poli). J. mar. biol. Ass. U. K. 23: 521–541. Pannacciulli, F. G., 1995. Population ecology and genetics of ical scale, is needed to clarify the pattern of vertical European species of intertidal barnacles. Ph. D. Thesis, Univer- distribution of C. montagui and C. stellatus on the sity of Liverpool: 143 pp. shore. Relini, G., 1983. Remarks on the ecology of chthamalids in the Ligurian Sea. Rapp. Proc.Verb. Réun. Comm. Int. Explor. Scient. Mer Méditerranée 28: 273–275. Southward, A. J., 1950. Distribution of Chthamalus stellatus on the Acknowledgements shores of North-East Ireland. Nature 166: 311. Southward, A. J., 1963. On the European species of Chthamalus The authors wish to thank Prof. Mario Specchi (Cirripedia). Crustaceana 6: 241–254. Southward, A. J., 1976. On the taxonomic status and distribution for the logistic support provided in Trieste and of Chthamalus stellatus (Cirripedia) in the North-East Atlantic Maura Maselli, Maria Chiara Casagrande and Paula region: with a key to the common intertidal barnacles of Britain. Moschella for help with the fieldwork. We are also J. mar. biol. Ass. U. K. 56: 1007–1028. grateful to Prof. A. J. Southward and Prof. A. J. Un- Underwood, A. J., 1997. Experiments in Ecology – Their Logical Design and Interpretation using Analysis of Variance. Cambridge derwood for useful comments on the manuscript. This University Press, Cambridge: 504 pp. study was funded by the E.U. (EUROROCK project - Underwood, A. J. & M. G. Chapman, 1998. GMAV5 for Windows – MAS3-CT95-0012). An analysis of variance programme. Institute of Marine Ecology, University of Sydney, Australia.

References

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