Large-Scale Patterns of Shell Variation in Littorina Striata, a Planktonic Developing Periwinkle from Macaronesia (Mollusca: Prosobranchia)

Marine Biology (1998) 131: 309±317 Ó Springer-Verlag 1998

H. De Wolf á T. Backeljau á S. Van Dongen R. Verhagen Large-scale patterns of shell variation in Littorina striata, a planktonic developing periwinkle from Macaronesia (Mollusca: Prosobranchia)

Received: 10 September 1997 / Accepted: 15 January 1998

Abstract Littorina striata King and Broderip, 1832 is a less, it seems that generalisations about macrogeo- strictly Macaronesian, intertidal periwinkle with plank- graphic shell morphology patterns, based on interspe- tonic development. The species displays a high degree of ci®c comparisons, are not directly applicable to intra- shell variation involving size and sculpture (nodulose vs speci®c patterns, and may strongly depend on local smooth shells). The present work provides a preliminary conditions which make adequate sampling and data account of some aspects of this shell variation on wave- treatment very dicult. exposed shores over the entire geographical range of the species. Based on morphological patterns observed among other prosobranchs it was predicted that south- Introduction ern specimens of L. littorina should on the average be larger, heavier, more nodulose, and should show more Intertidal rocky shore gastropods display a considerable shell repair marks, than northern specimens. These ex- amount of intraspeci®c shell variation (e.g. Gaillard pectations were con®rmed for shell size and weight. In 1965; Struhsaker 1967; Vermeij 1978 and references contrast, there was no consistent pattern in nodulosity therein; Crothers 1985; Chapman 1995; Johannesson between archipelagos, even though there were dier- 1995; Reid 1996 and references therein), of which the ences at much smaller scales. Shell repair marks were distribution and biological signi®cance have hitherto more prevalent in northern populations, but this trend mainly been investigated at microgeographical scales was only due to a signi®cant N±S dierence among (i.e. over distances of meters) (e.g. Johannesson 1986, nodulose shells. This is surprising as nodulose shells 1995; McMahon 1990; Frid and Fordham 1994; Chap- displayed signi®cantly fewer shell repair marks than man 1995; Preston et al. 1996). These studies revealed smooth shells. These observations were tentatively in- that wave action and predation have a strong in¯uence terpreted as a function of presumed dierential N±S on the horizontal intertidal distribution of shell mor- patterns of wave action and ambient temperatures. In photypes on rocky shores. Small, light and relatively this context, wave action in Macaronesia seems to in- smooth specimens with a large aperture tend to occupy crease in the south (contrary to what current theories wave-exposed habitats, whereas elongated, heavy and predict). This atypical situation may confound the in- strongly sculptured specimens with a small aperture tend terpretation of morphological patterns in L. striata so to occupy wave-sheltered shores where predation is in- that ®rm conclusions cannot be drawn without further tense (e.g. Vermeij 1978; Reimchen 1981; Crothers 1985; experimental work at dierent spatial scales. Neverthe- Sundberg 1988; Boulding and Van Alstyne 1993; Frid and Fordham 1994; Chapman 1995; Preston et al. 1996). On the other hand, vertical intertidal patterns of inter- Communicated by O. Kinne, Oldendorf/Luhe and intraspeci®c shell variation on rocky shores have been explained by desiccation and heat stress (e.g. Ve- H. De Wolf (&) á R. Verhagen rmeij 1978; McMahon 1990; Britton 1995 and references Evolutionary Biology Group, University of Antwerp (RUCA), Groenenborgerlaan 171, B-2020 Antwerp, Belgium therein), such that splash zone specimens tend to be more sculptured, more highly spired and have smaller T. Backeljau Royal Belgian Institute of Natural Sciences (KBIN), apertures compared to specimens from lower intertidal Vautierstraat 29, B-1000 Brussels, Belgium levels (e.g. Rao and Bhavanarayana 1976; Vermeij 1978; S. Van Dongen Crothers 1985; Thivakaran and Kasinathan 1990). University of Antwerp (UIA), Universiteitsplein 1, These adaptations have been suggested to regulate B-2610 Wilrijk, Belgium thermal regimes and maximize heat loss (Vermeij 1978). 310

In contrast to these microgeographical patterns, oping gastropods (e.g. Crothers 1985; Grahame and Mill macrogeographical trends of shell variation in intertidal 1986; Johannesson 1986; Reid 1996). gastropods are less well understood. Vermeij (1978) Given the apparent concordance between the micro- suggested in this respect that macrogeographic variation geographic shell patterning in Littorina striata and cur- is at least in part a function of a latitudinal trend of rent theories, we investigate in this study whether shell decreasing wave action, combined with increasing heat variation in L. striata also ®ts Vermeij's (1978) macro- stress and predation intensity towards the tropics geographic model based on interspeci®c comparisons. (Branch 1976; Vermeij 1973, 1978). Hence, rocky shore On the basis of latitudinal trends in predation intensity, gastropods from lower latitudes tend to be more sculp- wave action and thermal stress, this model predicts that tured, more globose and have smaller apertures than (1) shells of L. striata from southern populations should species from higher latitudes (e.g. Dautzenberg and be larger, heavier (i.e. thicker), more sculptured and Fischer 1912; Vermeij 1978, 1980 and references therein; have smaller apertures than specimens from the north; Ortega 1986). Anti-predatory devices, like apertural and (2) shell repair marks resulting from predation teeth and thicker shells, should therefore be more prev- should be more frequent in specimens from the south. alent towards lower latitudes (e.g. Palmer 1979 and references therein; Dudley 1980; Seeley 1986; Vermeij 1992; Boulding et al. 1993; Reid 1996 and references Materials and methods therein), as well as the frequency of shell repair marks (e.g. Vermeij 1978; Ackroyd et al. 1980). A total of 1640 mature (Shell height >5 mm; fully developed genitalia) specimens, involving 1130 smooth and 510 nodulose Vermeij's (1978) observations were, however, almost shells, from 41 populations of Littorina striata were collected at 13 entirely based on interspeci®c comparisons of shell traits islands of the four Macaronesian archipelagos (Fig. 1; Table 1) among limpets, periwinkles and neritids. Thus, except covering the entire geographical range of the species (between for a few studies (e.g. Philips et al. 1973; Dudley 1980; 39°41¢N and 14°20¢N and 31°13¢W and 13°38¢W). In order to en- Vermeij 1980, 1992; Seeley 1986), little is known about sure that morphological dierences re¯ected macrogeographic variation, rather than microgeographic habitat dierences, we intraspeci®c macrogeographical shell variation. More- collected all periwinkles at comparable wave-exposed sites, where over, most studies on this issue have involved non- planktonic developing molluscs, which are expected to display a higher degree of shell variation than species with a planktonic dispersing stage (e.g. Scheltema 1971; Crisp 1978; McMahon 1992; Chapman 1995), even S ã o Jorge though Boulding (1990) suggested that the correlation N=2 between variation in shell morphology and develop- 40° Azores S ã o Miguel N=12 mental mode may be weak. N Santa Maria In the present contribution we describe and attempt Faial Pico N=3 N=1 to interpret aspects of intraspeci®c macrogeographic N=2 Porto Santo patterning of shell variation in the Macaronesian (i.e. N=1 Azores, Madeira, Canary Islands and Cape Verde Is- Madeira Deserta Grande N=1 lands), planktonic developing periwinkle Littorina Madeira striata King and Broderip, 1832. Like many other lit- 30° N=2 torinids, L. striata shows a remarkable variation in shell Canary Is size, shape and sculpture (i.e. nodulose to smooth) (Reid Tenerife 1996) and, despite the planktonic development of the N=2 species and thus a predisposition for intense gene ¯ow, Gran Canaria reveals a considerable degree of microgeographic vari- N=3 ation (Britton 1995; De Wolf et al. 1997). Indeed, shells 20° S ã o Nicolau from wave-exposed sites tend to be more globose, are N=2 Sal longer, have larger apertures, and usually lack signi®- S ã o Vicente N=5 cant external sculpturing, whereas shells from sheltered N=5 sites tend to be less globose, are smaller, have smaller apertures, and are more often nodulose (De Wolf et al. Cape Verde Is 1997). In addition, specimens from higher shore levels 10° and from dark basaltic rocks with strong solar heating tend to be more nodulose (Britton 1995; De Wolf et al. Atlantic Ocean 1997). These patterns have been correlated with wave action and heat stress, but not with predation (Britton 1995; De Wolf et al. 1997). Yet, on the whole they 30° W 20° 10° 0 correspond well with the pattern and interpretation of Fig. 1 Macaronesia, locations of sampled Littorina striata popula- similar shell polymorphisms in non-planktonic devel- tions 311

Table 1 Littorina striata. Ori- gin of sampled material, col- Archipelago Island Locality N Smooth Nodulose lected at the Azores, Madeira, Canary and Cape Verde Is- Azores SaÄ o Miguel Mosteiros 2 lands, and absolute numbers of Capellas 1 smooth and nodulose shells Santana 1 collected at each of the 13 is- Vila de Nordeste 1 lands (N number of populations Faial da Terra 1 sampled, each of sample PovocËaÄ o1 size = 40) Caloura 1 Lagoa 1 Santa Clara 1 Feteiras 1 Ferereia 1 324 156 Santa Maria Anjos 1 33 7 SaÄ o Jorge F. da St. Cristo 1 Urzelina 1 54 26 Pico Lajes 1 Calhau 1 75 5 Faial P. da Almoxarie 1 Capelinhos 1 P. da Espalama 1 73 47 Madeira Madeira CanicËio de Baixo 1 P. de St. Caterina 1 58 22 Porto Santo Porto Santo 1 21 19 Deserta Grande Doca 1 8 32 Canary Is. Gran Canaria Agoustin 3 99 21 Tenerife Playa da America 2 31 49 Cape Verde Is. SaÄ o Vicente Baia das Gatas 2 Mindelo 2 Calhau 1 141 59 Sal Santa Maria 2 Jose Fonseca 1 Pedro de Lumen 2 158 42 SaÄ o Nicolau Harbour 2 55 25

each time a few square meters were sampled for 15 min. Sampling level 1000). When necessary, data were tested for normality was done between July 1994 and March 1996. with the Kolmogorov±Smirnov statistic. The following individual shell traits were measured to the All analyses were performed with the software packages Sta- nearest 0.05 mm using callipers: shell height (HS), shell width tistica v. 5.0 (Statsoft 1995) and NTSYS v. 1.80 (Rohlf 1993). (WS), aperture height (HA), aperture width (WA) and height of the spire (HT). Total (shell plus soft body) weight (TW) and soft body weight (BW) were determined to the nearest milligram. Finally, Results individuals were sexed, assigned to nodulose versus smooth morphotypes (Fig. 2) and scored for the presence/absence of repair The distribution of smooth versus nodulose shells did injuries, which were recorded for the whole shell surface (Fig. 2). The archipelago distribution of nodulosity and shell repair not dier signi®cantly between the four archipelagos marks was investigated by means of a logistic regression model, (F 0.63; df 3, 9; p 0.600). However, a signi®- using the GLIMMIX procedure of the SAS (Littel et al. 1996) cant residual variation (v2 114.6; df 9; software package, whereby the factor ``island'' was nested into p < 0.0001) indicated strong distributional dierences ``archipelago''. The interaction between islands and archipelagos for both shell morphs between islands. Shell breakage was considered as a random eect (variance 0.629) and was put as such into the logistic model. diered signi®cantly between nodulose and smooth Morphometric patterns were evaluated with a three-way mul- shells ( p 0.0001; Table 2; Fig. 3), with nodulose tivariate analysis of variance (MANOVA), contrasting three main shells displaying fewer shell repair marks (parameter factors: archipelago (Azores, Madeira, Canary Islands, Cape Verde estimate: smooth 0.1128; nodulose )1.5239) Islands), morphotype (nodulose, smooth) and sex (male, female). Nodulose and smooth shells were compared in function of the (Fig. 3). The signi®cant interaction with archipelago archipelago with post-hoc SheeÂ tests. Morphological shell varia- ( p 0.0101; Table 2) indicated, however, that the ef- tion was further analyzed by canonical discriminant analysis fect of archipelago diered per morphotype. Separate (CDA) of the 13 islands. Squared Mahalanobis distances were analyses indeed showed that nodulose specimens in the calculated between the four archipelagos and were used to con- struct a UPGMA (unweighted pair-group mean analysis) tree. The Cape Verde Islands displayed signi®cantly fewer shell correlation between geographical and squared Mahalanobis dis- repair marks than elsewhere (Fig. 3; p 0.0029), tances was investigated with a Mantel test (permutation whereas there was no signi®cant archipelago eect on 312

Fig. 2 Littorina striata. Exam- ples of smooth (A, F ) and A nodulose (B, C, D, G) morphotypes, of shell breakage (F, G ) B and erosion (E ). Eroded specimens such as E were not in- C cluded in our analysis because they could not be scored consistently as either smooth or nodulose

D E 2 mm A B C D E

2 mm F G

F G

Table 2 Littorina striata. Results of the logistic regression, con- interaction involving morphotype and archipelago was trasting the factors morphotype (i.e. smooth, nodulose shells) and highly signi®cant (Table 3: 1 ´ 3, p < 0.0001), indicat- archipelago, for the eect of shell repair (i.e. damaged, undamaged) (NDF numerator degrees of freedom; DDF denominator degrees of ing that morphometric dierences between the smooth freedom) and the nodulose shells varied between the four archipelagos (Fig. 4). Indeed, nodulose specimens were on Source NDF DDF TypeIII-Fp average smaller and lighter than smooth specimens, ex- Morphotype 1 9 87.27 0.0001 cept at the Cape Verde and Canary Islands, where both Archipelago 3 9 3.05 0.0845 morphs did not dier signi®cantly in size or weight Morphotype ´ 3 9 6.96 0.0101 (Fig. 4; Table 4). Regardless of morphotype, Cape Archipelago Verde shells were on average larger and heavier than shells from the Azores, Madeira and the Canary Islands (Fig. 4; Table 4). The smallest and lightest shells were shell breakage in smooth Littorina striata (Fig. 3; found in the Canary Islands (Fig. 4; Table 4). Irrespec- p 0.3034). tive of morphotype (Table 3: 2 ´ 3, p 0.154) and The MANOVA of morphometric patterns showed archipelago (Table 3: 1 ´ 2, p 0.555), females were that the three main factors contributed signi®cantly to on average larger and heavier than males. Although the the observed shell variation (Table 3). Also the two-way three-way interaction also contributed signi®cantly to 313

3 involved (Morrison 1969). Hence, this interaction will Nodulose damaged not be considered further. shells (p=0.0029) The ®rst two canonical variables (CVs) of the CDA 2 Smooth damaged accounted for 81.80% of the total variation (Table 5) shells (p=0.3034) and were used to plot the 13 Macaronesian islands on a two-dimensional graph (Fig. 5). CV1 was mainly an 1 expression of aperture width (WA) and shell weight [i.e. contrasting between total (TW) and body weight (BW)], with positive values indicating specimens with wider apertures and heavier shells. This CV axis indicated 0 that Cape Verdian shells tended to have wider apertures and heavier shells than Canarian, Madeiran and Azorean specimens (Fig. 5). This shell weight pattern -1 also followed from Fig. 4, which shows that the dif- ference between the means of total weight and body weight in the Azores, Madeira and the Canary Islands

Mean value, estimated proportion Mean value, of shell breakage -2 was much smaller than in the Cape Verde Islands AZ MA CA CV (Fig. 4). Fig. 3 Littorina striata. Mean values of the estimated proportions of CV2, on the other hand, mainly expressed the aper- shell breakage in smooth and nodulose specimens in the Azores (AZ ), ture height (HA) (Table 5). It revealed no clear pattern Madeira (MA), Canary Islands (CA) and Cape Verde Islands (CV ) for the populations of the Azores, Madeira and the Canary Islands, but discriminated strongly between the Table 3 Littorina striata. Results of a three-way multivariate three Cape Verde Islands, suggesting a conspicuous analysis of variance, testing for dierences between archipelago variation in aperture height among the Cape Verdian (Factor 1), sex (Factor 2), morphotype (Factor 3) and their inter- actions populations. Similar results were obtained when the CDA was Source Wilks' k Rao's Rdf1, 2 p-level performed on each shell morphotype separately, indicating that the two-way interaction between morphotype 1 0.4353 75.2204 21,4701 <0.0001 2 0.9845 3.6740 7,1637 <0.0006 and archipelago observed in the MANOVA (Table 3) 3 0.9239 19.2498 7,1637 <0.0001 did not obscure the overall pattern that within each 1 ´ 2 0.9882 0.9273 21,4701 0.5549 morphotype Cape Verdian specimens had the widest 1 ´ 3 0.9352 5.2830 21,4701 <0.0001 apertures and heaviest shells. 2 ´ 3 0.9935 1.5271 7,1637 0.1536 1 ´ 2 ´ 3 0.9793 1.6405 21,4701 0.0329 Finally, the UPGMA dendrogram (Fig. 6) of the squared Mahalanobis distances between the four archipelagos, separated the Cape Verde Islands from the the total variance, its contribution was only very limited others, even though there was no statistically signi®cant (smallest Rao's R of all signi®cant eectors; Table 3) relationship with geographic distance between archipel- and was probably a result of the large total sample size agos (Mantel's test: r 0.416, p 0.294).

Fig. 4 Littorina striata. Graph- 1300 ical representation of the two- 1200 way interaction between archipelago and morphotype, where 1100 smooth and nodulose shells are 1000 compared at each archipelago for each of the seven measured 900 shell characteristics (abbrevia- 800 tions see Fig. 3) 700 600 500

Dependent variables 400 Shell height 300 Shell width Aperture height 200 Aperture width 100 Shell top height Total weight 0 AZ MA CA CV AZ MA CA CV Body weight Smooth morphotype Nodulose morphotype 314

Table 4 Littorina striata. Results of SheeÂ post-hoc tests, for dif- (N) and smooth (S) shells in the Azores (AZ), Madeira (MA), the ferences in shell width, shell height, aperture width, aperture height, Canary Islands (CA) and the Cape Verde Islands (CV ) shell top height, total weight and body weight, between nodulose

AZ S AZ N MA S MA N CA S CA N CV S CV N

Shell width (above diagonal), shell height (below diagonal) AZ S 0.0001 0.9999 0.0001 0.0001 0.0001 0.0001 0.0001 AZ N 0.0001 0.0001 0.9999 0.8028 0.0366 0.0001 0.0001 MA S 0.9978 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 MA N 0.0001 1.0000 0.0001 0.9919 0.3314 0.0001 0.0001 CA S 0.0001 0.9510 0.0001 0.9861 0.6776 0.0001 0.0001 CA N 0.0001 0.1719 0.0001 0.4065 0.8076 0.0001 0.0001 CV S 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0813 CV N 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.9860 Aperture width (above diagonal), aperture height (below diagonal) AZ S 0.0001 1.0000 0.0001 0.0001 0.0001 0.0001 0.0001 AZ N 0.0001 0.0001 1.0000 0.9992 0.6656 0.0001 0.0001 MA S 1.0000 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 MA N 0.0001 1.0000 0.0001 0.9998 0.8759 0.0001 0.0001 CA S 0.0001 0.0839 0.0001 0.4753 0.4446 0.0001 0.0001 CA N 0.0001 0.0013 0.0001 0.0325 0.7911 0.0001 0.0001 CV S 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0387 CV N 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.5708 Shell top height (above diagonal), total weight (below diagonal) AZ S 0.0001 0.4517 0.0008 0.0001 0.0001 0.0001 0.0001 AZ N 0.0001 0.0001 0.8662 1.0000 0.8034 0.0001 0.0001 MA S 1.0000 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 MA N 0.0001 1.0000 0.0037 0.9144 0.2482 0.0001 0.0001 CA S 0.0001 0.9987 0.0001 0.9997 0.8399 0.0001 0.0001 CA N 0.0001 0.9034 0.0001 0.9608 0.9954 0.0001 0.0001 CV S 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.9856 CV N 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.1962 Body weight AZ S AZ N 0.0001 MA S 0.8975 0.0019 MA N 0.0001 0.9999 0.0218 CA S 0.0001 1.0000 0.0049 1.0000 CA N 0.0001 0.7674 0.0001 0.9671 0.8592 CV S 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 CV N 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.7034

Table 5 Littorina striata. Standardized coecients of the canonical variables in a CDA, contrasting all 13 Macaronesian Islands (HS Discussion shell height; WS shell width; HA aperture height; WA aperture width; HT shell top height; TW total weight; BW body weight; Our results tentatively indicate that: (1) there is no clear Cum.% cummulative percentage explained variation; Can R canonical correlation coecient) patterning of nodulose versus smooth shells between archipelagos; (2) nodulose shells display signi®cantly Root 1 Root 2 Root 3 Root 4 fewer shell repair marks than smooth shells; (3) nodulose specimens from the Cape Verde Islands show signi®- HS 0.0181 )0.5161 1.6829 2.7218 WS )0.4814 )1.1481 )2.5600 2.5427 cantly fewer shell repair marks than elsewhere, while HA 0.1629 2.8512 )1.3016 )2.6654 shell breakage in smooth specimens does not show a WA 1.0560 )0.9075 2.1094 )0.2349 dierential pattern between archipelagos; (4) regardless HT 0.3022 )0.8827 )1.5936 )2.2448 of morphotype, specimens from the Cape Verde archi- TW 1.2245 )0.2288 0.9114 )0.3464 BW )1.4934 1.2358 0.7157 0.3465 pelago are on average larger, have heavier shells and Eigen value 1.5716 0.5314 0.2475 0.0953 have wider apertures; and (5) nodulose specimens are on Cum.% 0.6113 0.8180 0.9142 0.9513 average smaller and lighter than smooth specimens, ex- Can R 0.7818 0.5891 0.4454 0.2950 cept in the Cape Verde archipelago, where both mor- p <0.0001 <0.0001 <0.0001 <0.0001 photypes do not dier signi®cantly in size or weight. Hence, only shell size and weight in Littorina striata vary according to Vermeij's (1978) model of macrogeographic trends, since northern specimens (i.e. from the 315

2 to Welsh coasts. However, using wind speed ®gures one can estimate relative wave heights in open sea (see Jen- São Nicolau kins 1973), and these ®gures can serve as indirect mea- sures of wave action, even if waves become lower and 1 steeper in coastal regions (Jenkins 1973). Based on Macaronesian wind speed ®gures for the period 1868 to São Miguel 1963 (Crunning 1967), we calculated that wave heights Sal around the Cape Verde Islands are on average two to Pico 0 Faial three times higher than elsewhere in Macaronesia.

CV 2 Madeira Hence, in contrast to the general expectation, wave ac- São Jorge Doca Grande Porto Santo tion in Macaronesia does not seem to decrease in the south. Santa Maria Patterns of predation intensity are even more dicult -1 Gran C. Tenerife to assess. However, during this study, the only crab that São Vicente was observed in signi®cant numbers was Plagusia depressa (Fabricius, 1775), a species that is particularly common on the wave-exposed shores at the Cape Verde -2 Islands. Yet, P. depressa is not expected to prey upon -2 -1 0 1 2 3 CV 1 Littorina striata as it is a herbivorous crab. Therefore, we have no reason to assume that the high crab density Fig. 5 Littorina striata. Graphical representation of the ®rst two in the Cape Verde Islands, as compared to the Azores, is canonical variables (CV1, CV2), representing all 13 Macaronesian associated with an increased littorinid predation pres- islands (s, Azores; j,Madeira;h, Canary Islands; d,CapeVerde Islands) sure. The partially unexpected N±S dierentiation of environmental conditions in Macaronesia may provide a Azores, Madeira and Canary Islands) are on average basis for a tentative interpretation of some aspects of smaller and lighter than southern specimens (i.e. Cape macrogeographical patterns of shell variability in Lit- Verde Islands). In contrast, nodulosity does not vary torina striata. consistently between northern and southern archipela- Aperture size has been shown to vary as a function of gos, while aperture size and shell repair in L. striata even wave exposure (e.g. Heller 1976; Raaelli 1982; Crothers show a geographical relationship that is diametrically 1985; Grahame and Mill 1986; Gibbs 1993). A larger opposed to the predictions of Vermeij's (1978) model. aperture allows for a larger foot and better holdfast, However, microgeographical dierences may possibly thus decreasing the risk of dislodgement on wave-ex- have in¯uenced the current macrogeographical shell posed shores. Yet, a larger aperture may be disadvan- patterns, although we attempted to sample at compa- tageous at sites with high thermal loads as it would rable shores. increase heat conduction. Smaller apertures should Nevertheless, in order to interpret the contradictory prevail in such case because they reduce heat conduction N±S trends of shell variability in Littorina striata,itis (Vermeij 1978). Since Littorina striata with the largest necessary to assess whether environmental conditions in aperture was found in the Cape Verde Islands where Macaronesia follow the latitudinal trends expected by wave-exposure and air/water temperature appear higher Vermeij (1978), Branch (1976), Palmer (1979), Dudley than elsewhere in Macaronesia, it seems that on wave- (1980) and Bertness and Cunningham (1981). At least exposed shores wave action is more important in de- for the daily air temperature and surface water temper- termining aperture size, than thermal stress. This is ature this seems to be the case, since both increase to- consistent with the idea that thermal stress on wave- wards the Cape Verde Islands (Crunning 1967). exposed shores can be accommodated by conductive Wave action is dicult to quantify since there are no cooling via wave-splash (McMahon 1990). appropriate wave-exposure scales for Macaronesia. The fact that we collected more smooth than nodu- Ballantine's (1961) scale, for example, is only applicable lose specimens was probably due to our attempt to sample comparable wave-exposed shores, where nodulose shells should be less common (De Wolf et al. 1997) 7.2 6.0 4.8 3.6 2.4 1.2 0 because of their increased risk at drag (Denny 1988). Azores However, nodulosity in Littorina striata has also been Madeira related to heat stress, for it has been suggested that on Canary Islands wave-sheltered shores nodulose shells might have a more Cape Verde ecient thermoregulation than smooth specimens (Britton 1995; De Wolf et al. 1997). Yet, whether ther- 7.2 6.0 4.8 3.6 2.4 1.2 0 mal stress would also aect nodulosity on wave-exposed Fig. 6 Littorina striata. UPGMA tree of squared Mahalanobis shores remains questionable as in these conditions the distances between the four archipelagos inhabited by L. striata risk of drag may outweigh the advantage of thermo- 316 regulation, as on wave-exposed shores shells can be tions about macrogeographic patterns of shell mor- cooled by wave-splash (see previous paragraph). phologies based on interspeci®c comparisons are not The present data do not provide a basis to decide on necessarily applicable to intraspeci®c patterns. the mechanisms and forces that are at the basis of the observed shell morphology patterns (natural selection vs Acknowledgements This research was supported by the MAST 3 ecophenotypic plasticity). Yet, at microgeographic programme of the European Commission under Contract Number scales, dierential shell morphology patterns are main- MAS3-CT95-0042 (AMBIOS). Travel expenses were partly cov- ered by STRIDE, Portugal. The authors would like to thank tained in the presence of intense gene ¯ow (De Wolf et al. D. Reid (Natural History Museum, London) for critical comments unpublished data), while at least aperture size shows a on an earlier draft of the manuscript, and D. Verbergt (Hogere phenotypic response (i.e. increases) when specimens are Zeevaartschool, Antwerpen), P.G.B. Jones (Hydrographic Oce of transplanted from a wave-sheltered to a wave-exposed the UK) and K. Wouters (KBIN) for various types of help. H. Van shore (De Wolf et al. 1997). Such a response may be Paeschen (KBIN) prepared the illustrations. H. De Wolf holds an IWT scholarship. related to an increased food availability (and/or quality) in wave-exposed conditions, resulting in an increased growth rate. Conversely, slower growth rates at wave- sheltered shores have been invoked as a trigger to de- References velop nodulose shells (e.g. Reid 1996). Yet, the present Ackroyd S, Behrendt K, Bito J, Brown L, Denckla M, Dudley C, results cast doubts on this latter suggestion, since on the Josephson S, Kibel A, Laster S, Maddox J, Montroll C, wave-exposed shores of the Cape Verde Islands, nodu- Przybylski M, Segal J, Speck S, Stracher A, Wheeler D (1980) lose shells reach the same shell size and weight as smooth Comparative rates of predation on northern and southern specimens, indicating that nodulosity may be not di- periwinkles. J Wash Acad Sci 78: 35±36 rectly related to growth rate dierences. On the other Ballantine JW (1961) A biologically-de®ned exposure scale for the comparative description of rocky shores. Field Stud 1: 1±19 hand, the fact that Littorina striata can produce larger Bertness MD, Cunningham C (1981) Crab shell crushing predation and heavier shells in the Cape Verde Islands may be due and gastropod architectural defense. J exp mar Biol Ecol 50: to the lower energy cost of calci®cation at lower latitudes 213±230 (Graus 1974), since calcium carbonate dissolves less well Boulding EG (1990) Are the opposing selection pressures on exposed and protected shores sucient to maintain genetic dif- at higher temperatures (Graus 1974; Clarke 1983). ferentiation between gastropod populations with high Obviously, our results and interpretations are very intermigration rates. Hydrobiologia 193: 41±52 tentative and speculative. For example, we have no ad- Boulding EG, Buckland-Nicks J, Van Alstyne KL (1993) Mor- equate information with regard to potential predators, phological and allozyme variation in Littorina sitkana and related Littorina species from the northeastern Paci®c. Veliger 36: such as carnivorous crabs, birds or ®sh. 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