J. Mar. Biol. Ass. U.K. (2001), 81, 781^788 Printed in the United Kingdom Ecology of a parasitic barnacle, Koleolepas avis: relationship to the hosts, distribution, left ^ right asymmetry and reproduction Yoichi Yusa*, Shigeyuki Yamato and Masahiro MarumuraO Seto Marine Biological Laboratory, Kyoto University, Shirahama, Wakayama 649-2211, Japan. ONanki High School, 3262 Shinjo, Tanabe, Wakayama 646-0011, Japan. *Present address: Laboratory of Insect Ecology, Kyushu Okinawa National Agricultural Research Center, Nishigoshi, Kumamoto 861-1192, Japan. E-mail: [email protected]¡rc.go.jp The pedunculate barnacle Koleolepas avis is a symbiont of the sea anemone Calliactis japonica, which lives on gastropod shells carried by large hermit crabs, usually Dardanus arrosor. Relationships with the host sea anemone, distribution on the gastropod shell, left ^ right asymmetry and reproduction of the barnacle were investigated. A larger number of barnacles occurred on shells with greater `cylindroid dimensions' of sea anemones. Distribution of barnacles on shells was not random: assuming the in situ position of the shell carried by the hermit crab (458 inclination), there were more barnacles along the lower part of the anemone disk than the upper part. Large barnacles lie on either the left or right sides of their capitula, and those lying on the left side (Type L individuals) tended to occur along the left side of the host, and those on the right side (Type R) along the right side. Barnacles 50.016 g in wet weight had egg masses, and there was a positive relationship between body weight and number of eggs. Koleolepas avis has both hermaphrodites and dwarf (complementary) males attached to them. Large hermaphrodites tended to have larger dwarf males than smaller hermaphrodites. INTRODUCTION Koleolepas avis (Hiro, 1931) is a pedunculate barnacle living underneath or around the pedal disks of sea anemones that live on gastropod shells occupied by hermit crabs (Hiro, 1931, 1933; Yusa & Yamato, 1999). This barnacle, together with two congeners occupying similar microhabitats (Koleolepas willeyi Stebbing, 1900 and Koleolepas tinkeri Edmondson, 1951), have been regarded as rare and rather peculiar barnacles deserving the monotypic family Koleolepadidae (Hiro, 1933) in the suborder Heteralepadomorpha (Newman, 1987). Although information on the ecology of Koleolepas is limited, some interesting features are known. First, K. avis has left ^ right asymmetry in its morphology. Hiro (1933) noted that ``the scutum is . . . well-developed on only one side of the capitulum (in two specimens on the left side and in one on the right)''. Edmondson (1951) made a similar note on K. tinkeri. Second, Koleolepas is one of the few known heteralepadomorph barnacles that occur as hermaphrodites accompanied by dwarf (complementary) males (Pilsbry, 1911; Anderson, 1994; Kolbasov & Zevina, 1999). Stebbing (1900) and Edmondson (1951) noticed a `bulbous process' near the aperture of the barnacle, and Hiro (1931) noted it was a cyprid in form, but none of them referred to its nature nor possible function. Newman et al. (1969) noted the process was in fact a dwarf male in K. tinkeri. Third, a predacious feeding behaviour, cropping of tentacles of the host sea anemones, has been reported in K. avis (Yusa & Yamato, 1999; Figure 1). This paper deals with general aspects of the ecology of K. avis including: (1) relationships to the sea anemones, Journal of the Marine Biological Association of the United Kingdom (2001) hermit crabs and gastropod shells; (2) distribution on the shell and position in relation to the host sea anemone; (3) development and probable function of asymmetry; and (4) mode of reproduction. MATERIALS AND METHODS Collection of gastropod shells Gastropod shells trapped in lobster nets were collected at Minabe Fishery Port, Tanabe Bay, Kii Peninsula, southern Japan (338440 N 1358200 E) from February to April 1996. Most of the shells had sea anemones on them. The lobster nets had been set near rock cli¡s 10^100 m depth for a few days before landing. After collection, the shells were preserved in 5% formalin in seawater until examination. Measurements on gastropod shells, hermit crabs, and sea anemones Each gastropod shell was identi¢ed, and its maximum length and width measured, excluding projections (spines) on the shell. The surface of shells with the sea anemone Calliactis japonica (Carlgren) was divided into nine zones (Figure 2A). Surface area of each zone was measured for one shell per gastropod species, except for zone IVC (inside the aperture), for which measurement was not possible. The measurement was made by covering the zone with small pieces of thin plastic tape of known lengths and widths without overlapping. The relative proportion of surface area of each zone was averaged for 782 Y. Yusa et al. Ecology of a parasitic barnacle the 13 species of gastropods collected, weighed by the number of shells with C. japonica per species. There was a strong positive relationship between the total surface area of a shell measured in this way and the surface area calculated from the maximum length and width, assuming that the shell was a spheroid (r2 0.90, P50.001, N13 shells, all di¡erent species). This indicates that, although shells like Murex troscheli Lischke and Chicoreus asianus Kuroda have many projections, surface areas of shells were highly predictable from their lengths and widths. Hence, surface areas of the remaining shells were estimated from surface areas of spheroids with the same lengths and widths, using the equation: SH 0:623 SP 6:29 Figure 1. Koleolepas avis (near centre), coming out of the gap between the pedal disk of the sea anemone and the gastropod shell, to feed on the host tentacles. (1) where SH is shell surface area and SP is calculated surface area of a spheroid, both in cm2. When there was a hermit crab in a shell, it was removed, identi¢ed, blot-dried and weighed. Each large sea anemone (Calliactis spp.) was identi¢ed and the centre of its zone on the shell noted (Figure 2A). Then the anemone was removed, blot-dried and weighed. Its maximum height, and its longest and shortest diameters perpendicular to each other, were also measured. The `cylindroid dimension' of the anemone was calculated from these diameters, assuming that it was a cylindroid. Measurements of Koleolepas avis When Koleolepas avis was found, the zone on the shell (Figure 2A) and the area around the nearest sea anemone (Figure 2B) were noted. Also, distances to the pedal disk of the nearest sea anemone, and to the attachment disk of the nearest conspeci¢c, were measured over the shell surface. Then the barnacle was removed, blotdried, weighed, and its capitulum width measured. There was a positive relationship between the cube of the capitulum width and body weight among unbroken barnacles (r2 0.90, P50.001, N99). For barnacles with broken parts (N6), body weight was estimated from capitulum width, using the equation: BW 0:00169 CW3 Figure 2. (A) Nine zones on the shell surface; and (B) six areas around the host sea anemone. Journal of the Marine Biological Association of the United Kingdom (2001) 0:00064 (2) where BW is body weight (g) and CW is capitulum width (mm). Barnacles were distinguished into three types of asymmetry: individuals lying on the left side of the capitulum were termed `Type L'; those on the right side `Type R'; and the remaining ones (standing out of the surfaces) `Type M'. When a barnacle was ovigerous, its egg mass was removed from the mantle cavity, carefully dissected with needles, and the number of eggs counted under a binocular microscope. Ten eggs were randomly chosen for each egg mass, their maximum lengths were measured and the presence or absence of eyes were noted. When a hermaphrodite had dwarf males on it, each was removed and its maximum length (front to back of its carapace) was measured. Ecology of a parasitic barnacle Y. Yusa et al. 783 Statistical analysis Several variables measured in this study had left-skewed distributions. Square-root transformation was conducted when appropriate (Sokal & Rohlf, 1981). RESULTS Relationships to sea anemones, hermit crabs and gastropod shells A total of 105 of Koleolepas avis individuals, excluding dwarf males, were found on 38 of the 86 gastropod shells examined in 1996. Two species of large sea anemones, Calliactis japonica and Calliactis polypus (ForskÔl), were found on di¡erent shells occupied by di¡erent species of hermit crabs. In all but one case (37 out of 38; 97%), K. avis occurred on shells with C. japonica (Figure 3). In one case, K. avis occurred on a shell without sea anemones. No K. avis occurred on eight shells with C. polypus, irrespective of the fact that the total weight of C. polypus on a shell was similar (analysis of variance (ANOVA), F0.001, Figure 3. Number of Koleolepas avis on a shell with the sea anemones Calliactis japonica (upper), Calliactis polypus (middle) or no large anemones (bottom). P40.9) and total cylindroid dimension longer (F17.27, P50.001) than those of C. japonica. An additional 21 shells with C. polypus were examined in the winter of 1997, but no K. avis were found on them. Koleolepas avis occurred on 37 out of 59 shells (63%) with the sea anemone C. japonica. The number of barnacles per shell varied considerably, from 0 to 7 (Figure 3). The barnacle number was positively related to the total cylindroid dimension of C. japonica on the shell (r2 0.196, P50.001, N59). On the other hand, total weight or total number of sea anemones had no signi¢cant e¡ects on the number of barnacles on the shell (both P40.4 in a multiple regression including the above three independent variables, whereas P50.05 for the cylindroid dimension). Among the 37 shells with barnacles and sea anemones, the hermit crab Dardanus arrosor (Herbst) occurred in 30 shells (81%) and Dardanus crassimanus (H. Milne Edwards) in one shell (3%). The remaining six shells (16%) were empty (probably because hermit crabs had been lost while the shells were trapped in lobster nets). Among 22 shells without barnacles, D. arrosor occurred in 19 shells (86%), D. crassimanus in two shells (9%), and there were none in one shell (5%). Hermit crab species did not a¡ect the number of barnacles on the shell (ANOVA, F1.73, P40.2). Body weight of D. arrosor had no signi¢cant e¡ect on the number of barnacles on the shell (r2 0.049, P40.1, N49). Barnacles were not found on shells with the hermit crabs Dardanus pedunculatus (Herbst) (N4), Dardanus impressus (De Haan) (N1) or Dardanus lagopodes (ForskÔl) (N1), all of which are symbiotic with the sea anemone C. polypus. Shells with K. avis consisted of 11 species in six families (Table 1). Shells without K. avis consisted of ten species, eight of which were among the former 11 species. Gastropod species did not a¡ect the number of barnacles (ANOVA, F0.73, P40.7, N59, excluding a shell without C. japonica). There was a weak positive relationship between surface area of the shell and the number of barnacles on it (r2 0.068, P50.05). However, this relationship became non-signi¢cant when the total cylindroid dimension of sea anemones on the shell was incorporated Table 1. Gastropod shells with or without Koleolepas avis, among shells with the sea anemone Calliactis japonica (N59). Species Family Chicoreus pliciferoides Kuroda Muricidae Charonia sauliae (Reeve) Cymatiidae Fusinus forceps Fulton Fasciolariidae Psephaea concinna Broderip Voltidae Tonna olearium (L.) Tonnidae Psephaea diviesi (Fulton) Voltidae Murex troscheli Lischke Muricidae Hemifusus tuba (Gmelin) Melongenidae Pleuroploca trapezium (Strebel) Fasciolariidae Monoplex parthenopeum (Kuroda & Habe) Cymatiidae Tonna luteostoma (Ku«ster) Tonnidae Chicoreus asianus Kuroda Muricidae Neptunea kuroshio Oyama Buccinidae *, shell without C. japonica. Journal of the Marine Biological Association of the United Kingdom (2001) Average shell area (cm2) No. with K. avis No. without K. avis Average no. of K. avis/any shell 68 190 107 108 207 99 121 178 111 70 227 115 92 10 7 3 3 3 2 2 1 (1)* 1 1 0 0 10 3 4 2 0 2 1 1 1 0 0 1 1 1.7 2.5 1.3 1.8 3.3 1.3 2.3 1 0.5 3 2 0 0 784 Y. Yusa et al. Ecology of a parasitic barnacle into a multiple regression (P40.4 for area, whereas P50.01 for cylindroid dimension). Distribution on gastropod shell Eighty-six out of 105 individuals (82%) of Koleolepas avis lived in contact with sea anemones (Figure 4A). Only seven individuals (7%) had no hosts within 10 mm (including the one individual with no sea anemones on the same shells). In most of these cases scars of sea anemones were present on the shells near the barnacles, indicating that sea anemones had once lived there. Distance to the nearest conspeci¢c was greater (Figure 4B). Ninety-three out of 102 barnacles (91%; data were not taken for three individuals by mistake) were not in contact with a conspeci¢c. Twenty individuals (20%) had no conspeci¢cs within 50 mm. The number of barnacles on the shell varied between zones, with the highest in zone IB and lowest in zones IVB and IVC (Table 2). Both the relative proportion of surface area of the zone (P50.01) and the total cylindroid dimension of sea anemones in each zone (P50.01) were related to barnacle number (multiple regression, r2 0.96, Figure 4. (A) Distance to the nearest sea anemone; and (B) conspeci¢c. Table 2. Number of Koleolepas avis in relation to the zones on the shell. Zone No. of K. avis Relative shell area (%) Total cylindroid dimension of anemones (cm)* IA IB IIA IIB IIIA IIIB IVA IVB IVC Total 13 33 10 16 8 6 13 3 3 105 11.4 25.2 13.7 16.7 10.3 11.4 8.1 3.2 ^ 100.0 204.5 482.9 107.2 254.0 21.6 37.0 369.5 14.3 33.9 1107.2 *, total of cylindroid dimensions of all the anemones whose centres were in each zone. Journal of the Marine Biological Association of the United Kingdom (2001) N8 zones, except for zone IVC where surface area was not measurable). The distribution of K. avis around the host was not random. For instance, all the barnacles in zones IIA and IIB were in areas 1^3 (Figure 5). When shells were carried by hermit crabs, they were rotated from the living gastropod posture by 458 (our personal observations). Assuming this in situ position, areas 1^3 in zones IIA and IIB were along the lower half of the pedal disk of the host whereas areas 4^6 were along the upper half (Figure 5). When all the barnacles were counted over all the zones (except for zone IVC), more barnacles lived along the lower half of the host than along the upper half (65:16, binomial test, P50.001; areas 2 and 5 in zones I and III were excluded as they could not be regarded as `lower' nor `upper' of the sea anemone; Figure 5). Asymmetry Asymmetry based on the posture of the ¢xed barnacle specimens coincided well with their behavioural and morphological asymmetries: observations on living barnacles showed that the posture was highly constant, with Type L individuals almost always lying on the left side and Type R on the right side. The scutum on the lower side of the capitulum was reduced (see also Hiro, 1933), and when there was a dwarf male, it usually attached to the lower side of the aperture. Type M individuals developed no such asymmetry. All the Type M individuals were 50.05 g in body weight, and most were 50.001g (Figure 6). Such very small individuals did not fully develop attachment disks. Type L and Type R individuals were larger than Type M individuals. Body weights of Type L and Type R individuals were not signi¢cantly di¡erent from each other (ANOVA, F1.11, P40.2). The numbers of Type L and Type R individuals were almost equal (45:42; binomial test, P40.8). Assuming the in situ position of the shell with the hermit crab has a 458 inclination, areas around the sea anemone can be distinguished into `left' or `right' side of the host (Figure 5). For instance, areas 3 and 4 in zone IIA are along the left side of the host, areas 6 and 1 are along the right side, and areas 2 and 5 are neither. Likewise, when Type L and Type R individuals were counted for both left or right sides of the host, Type L individuals tended to live along the left side of the host, and Type R along the right side (Table 3). Reproduction Twenty-one out of 102 hermaphrodites (21%; three individuals were excluded because their capitula were partly broken) had eggs (including embryos). The smallest hermaphrodite with eggs was 0.016 g (2.2 mm in capitulum width). Thirty-six per cent (21 out of 58) of individuals above this size, and 71% (12 out of 17) 40.1g, had eggs. Ovigerous individuals were 0.18 0.166 g (mean SD, N21), or 4.4 1.26 mm in capitulum width and had 3505 3192 eggs. Large individuals tended to have more eggs than smaller ones, both among all the hermaphrodites (r2 0.51, P50.001, N102) and among ovigerous ones (r2 0.77, P50.001, N21; Figure 7A). The egg Ecology of a parasitic barnacle Y. Yusa et al. 785 Figure 5. Distribution of Koleolepas avis in relation to the sea anemone and the gastropod shell. See Figure 2 for areas around the anemone and zones on the shell. Barnacles were categorized into Types L, M or R. Only barnacles with known zones (except for zone IVC) and areas were included (N97). Thin arrows near anemones indicate the direction of the apex of the shell, and thick arrows indicate direction of gravity. Table 3. Relationship between asymmetry types of Koleolepas avis and position around the host sea anemone. Position K. avis types* L R Left Right 20 10 13 21 w2 5.16, P50.05. *, only Type L or Type R individuals with either left or right side of the host were included. capsule was spheroid, the maximum lengths of egg capsules with no eye spots being 224 19 mm (mean SD, N11), capsules with eye spots being slightly larger, 295 15 mm (N10; ANOVA, F93.41, P50.001). Lengths of egg capsules were not related to the body weights of hermaphrodites, either for egg capsules with eye spots (r2 0.09, P40.3, N11) or those without them (r2 0.04, P40.5, N10; Figure 7B). Thirty-one out of 105 hermaphrodites (30%) had dwarf males attached near their apertures (including six cyprids on ¢ve hermaphrodites). Males were sac-like, basically simpli¢ed hermaphrodites without developing long peduncles or attachment disks. The smallest hermaphrodite with a male was 0.007 g (1.9 mm in capitulum width). Forty-six per cent (31 out of 68) of hermaphrodites above Journal of the Marine Biological Association of the United Kingdom (2001) Figure 6. Size distributions of Koleolepas avis of Type L (upper), Type M (middle) or Type R (bottom). this size, and 73% (24 out of 33) above 0.05 g, had dwarf males. Most male-carrying hermaphrodites (81%; 25 out of 31) had only one male, but three hermaphrodites had two males each and three had three males each (hence 40 males in total). In 1999, some additional hermaphrodites were collected, and one of them had ¢ve males on it (Yusa & Yamato, 1999). Among barnacles collected in 1996, there was a positive relationship between body 786 Y. Yusa et al. Ecology of a parasitic barnacle DISCUSSION Relationships to hosts Figure 7. Relationships between: (A) body weight and egg number; and (B) body weight and length of egg capsules (*, eyed embryos; , pre-eyed embryos). Figure 8. Relationships between: (A) body weight of hermaphrodites and number of dwarf males on them; and (B) body weight of hermaphrodites and length of dwarf males (*, dwarf males after metamorphosis; , cyprids). weight of hermaphrodites and number of dwarf males (Figure 8A; r2 0.34, P50.001, N105). But this relationship was non-signi¢cant when hermaphrodites without males were excluded (r2 0.10, P0.09, N31). The maximum length of dwarf males (excluding cyprids) were on average 0.96 0.220 mm (mean SD; N34) shorter than cyprids (1.13 0.056 mm, N6; ANOVA, F4.15, P50.05). Body sizes of hermaphrodites had a positive correlation with lengths of dwarf males on them (Figure 8B; r2 0.43, P50.001, N34), but not with lengths of cyprids (r2 0.0004, P40.9, N6). Out of 31 hermaphrodites with males (including cyprids), 15 (48%) had eggs. None of the four hermaphrodites with only cyprids had eggs. Out of 21 hermaphrodites with eggs, 15 (71%) had males on them. Five of the remaining six ovigerous hermaphrodites without males had another hermaphrodite within 6 mm. Journal of the Marine Biological Association of the United Kingdom (2001) Koleolepas avis depends entirely on the host sea anemone for food and refuge (Yusa & Yamato, 1999). In the present study, such dependence is re£ected in the strict choice of host species and the short distance to the host. The sea anemone Calliactis japonica often left scars on gastropod shells when removed, whereas Calliactis polypus rarely left such scars, suggesting that C. japonica is more sedentary than C. polypus, which changes position in response to the hermit crab's palpation (Ross, 1983). The di¡erence in mobility may be a factor a¡ecting the barnacle's choice of host species. The relationships between K. avis and gastropod shells and hermit crabs seem to be much weaker. The surface area of the shell had a weak relationship to the number of barnacles on it, but this is merely an indirect e¡ect through the cylindroid dimensions of sea anemones on it. Other ecological aspects of K. avis appear to be related to its parasitic nature. First, the number of K. avis on a shell was positively related to the total cylindroid dimension of sea anemones on the shell, but not to their total number or weight. As most barnacles live under or in contact with sea anemones, longer cylindroid dimensions of anemones mean more microhabitats available for the barnacles. They also imply more tentacles, hence food, for the barnacles. Second, most barnacles lived along the lower part of the host with in situ position of the shell. This is apparently related to feeding, as host tentacles are likely to hang down to the lower part, and the barnacle can follow tentacles only after it eventually touches them (Yusa & Yamato, 1999). Living along the lower part of the host should also be e¡ective in avoiding potential predators. This study shows that very small barnacles had no left ^ right asymmetry, but as they grew they became asymmetric. A left ^ right asymmetry in scutal morphology has been reported in Poecilasma (Darwin, 1851; Hiro, 1938). The authors also reported that the £atter scutum lies close to the substratum, but otherwise the function of the asymmetry was unknown. In K. avis, Type L individuals tended to be along the left side of the host sea anemone, and Type R along the right side. We believe that this tendency is also related to feeding. Koleolepas avis crops a host tentacle by holding it with the cirri and the capitulum, and bending its peduncle suddenly in the direction of the aperture (Yusa & Yamato, 1999). Thus Type L individuals along the left side of the host and Type R along the right side can bend their peduncles e¡ectively, with the aid of gravity (see Figure 5). On the other hand, barnacles along the `wrong' side must bend against gravity. The relationship between the position of barnacles and types of asymmetry was not strong, probably because: (1) inclination of the shell by the hermit crab was not always 458; (2) large sea anemones covered more than one zone on the shell; and (3) barnacles might feed on tentacles of anemones other than their nearest host if available. Koleolepas avis was apparently distributed more sparsely than most other pedunculate barnacles, which tend to aggregate (Barnes & Reese, 1960; Williams & Moyse, 1988). The availability of a highly specialized food, host Ecology of a parasitic barnacle Y. Yusa et al. 787 tentacles, may be a factor limiting the density of the barnacle. In turn, the sparse distribution appears to be an important ecological factor for the maintenance of the sexuality of the barnacle (see below). Eggs and larvae Eggs of Koleolepas avis were of moderate size among pedunculate barnacles having planktotrophic larvae (Barnes, 1989). The number of eggs showed a positive relationship with body size in K. avis. Such a relationship is commonly observed among pedunculate barnacles (Zann & Harker, 1978; Barnes, 1989). Direct comparisons of egg number with other pedunculates are of little value owing to the wide range of body sizes across species, but the present data on K. avis, i.e. 3500 eggs in a barnacle of 0.2 g (11mm in overall length), were similar to the corresponding ¢gures in Octolasmis warwickii (Zann & Harker, 1978). No cyprids or later-stage nauplii were found in the mantle cavity of K. avis. This result, together with the moderate egg size of K. avis among planktotrophic pedunculates, indicates that larvae of this barnacle are likely to be released as early-stage nauplii. Cyprids attaching to hermaphrodites were much larger than nauplii. This suggests that the released nauplii were planktotrophic, like a great majority of thoracican barnacles (Barnes, 1989; Anderson, 1994). Sexuality Koleolepas avis has both hermaphrodites and dwarf males. Dwarf males were brie£y noted in Koleolepas tinkeri by Newman et al. (1969). Two other heteralepadomorph barnacles, Paralepas klepalae, and Heteralepas vetula, have been reported to have dwarf males (Pilsbry, 1911; Newman, 1996; Kolbasov & Zevina, 1999). Otherwise this sexuality is unknown in the suborder Heteralepadomorpha. In K. avis, there was a positive relationship between body sizes of hermaphrodites and dwarf males, suggesting that large hermaphrodites obtain more sperm than small ones. Such a relationship between sizes of hermaphrodites and sizes or numbers of their males has been unknown in barnacles with hermaphrodites and dwarf males. In some dioecious (i.e., females with dwarf males) barnacles, large females tended to have larger dwarf males (in Ibla; Klepal, 1987) or more males (in acrothoracican barnacles; Utinomi, 1961; Gotelli & Spivey, 1992). The cirri of K. avis males appear to be too short for suspension feeding, and their body size is too small for cropping the host's tentacles. If dwarf males utilize part of hermaphrodite's food, the positive relationship between their body sizes may simply indicate males on large hermaphrodites are older and hence larger. However, if dwarf males are `absorptive parasites' of hermaphrodites, the relationship may mean an adaptive response of hermaphrodites to give an optimal amount of nutrition to the males for fertilizing their eggs. Sexuality in Cirripedia is complicated; each species has either: (1) females and dwarf males; (2) hermaphrodites and dwarf males; or (3) only hermaphrodites (Darwin, 1851). Since thoracican barnacles are basically hermaphrodites and males and females appeared later in some Journal of the Marine Biological Association of the United Kingdom (2001) lineages (HÖeg, 1995), an important question is what ecological factor is involved in the maintenance of dwarf males and pure females. Using theoretical models, Charnov (1982, 1987) suggests that mating group size is the most important factor likely to a¡ect the sexuality in barnacles. He proposes that simultaneous hermaphroditism evolves when mating group size is limited, as is the case in sedentary animals like barnacles. When there are size classes in a mating group, small individuals should emphasize male function, because sperm are relatively cheaper to produce than eggs. Dwarf males are expected to be more common in small mating groups than large ones, because competition among sperm is less intense in small groups, thus small males with limited resources can be competitive with large hermaphrodites acting as males. Male function in hermaphrodites becomes small in small mating groups, but we suggest that hermaphrodites should retain male function unless mating group size is very small (almost no female partners are available), as they can fertilize eggs of other individuals with a small amount of resources to produce sperm. Thus, small mating group size with incomplete isolation is a probable cause of the maintenance of hermaphrodites with dwarf males in barnacles. Evidence from K. avis supports this hypothesis. Mating group size of K. avis is actually small, but most hermaphrodites were not completely isolated, having at least one conspeci¢c within 50 mm. Direct observations showed that this distance is short enough for a large hermaphrodite to reach another hermaphrodite. In addition, 30% of ovigerous hermaphrodites were without a dwarf male, suggesting that a hermaphrodite has a good chance of fertilizing the eggs of its neighbour. Once dwarf males have evolved, hermaphrodites should house and/or may give nutrition to them, in a condition such as low density where the presence of males is advantageous for them (Newman, 1980). In K. avis, dwarf males are clearly bene¢cial to hermaphrodites isolated from one another. We thank ¢shermen working at Minabe Fishery Port for allowing us access to the materials. Dr William Newman kindly read the manuscript and gave us many valuable comments. Thanks are also due to Dr Toshiyuki Yamaguchi and Dr Tomonari Watanabe for literature. REFERENCES Anderson, D.T., 1994. Barnacles: structure, function, development and evolution. London: Chapman & Hall. Barnes, H. & Reese, E.S., 1960. The behaviour of the stalked intertidal barnacle Pollicipes polymerus J.B. Sowerby, with special reference to its ecology and distribution. Journal of Animal Ecology, 29, 169^185. Barnes, M., 1989. Egg production in cirripedes. Oceanography and Marine Biology. Annual Review, 27, 91^166. 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