Ecology of a parasitic barnacle, Koleolepas avis- relationship to the hosts, distribution, left–right asymmetry and reproduction-yusa2001

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]¡
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.
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.
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
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
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 ˆ0.90,
P50.001, Nˆ13 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 ˆ 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.
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
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 ˆ0.90, P50.001, Nˆ99). For barnacles with broken
parts (Nˆ6), body weight was estimated from capitulum
width, using the equation:
BW ˆ 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)
where BW is body weight (g) and CW is capitulum width
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).
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), Fˆ0.001,
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 (Fˆ17.27,
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 ˆ0.196,
P50.001, Nˆ59). 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, Fˆ1.73, P40.2). Body weight of D. arrosor had
no signi¢cant e¡ect on the number of barnacles on the
shell (r2 ˆ0.049, P40.1, Nˆ49). Barnacles were not found
on shells with the hermit crabs Dardanus pedunculatus
(Herbst) (Nˆ4), Dardanus impressus (De Haan) (Nˆ1) or
Dardanus lagopodes (ForskÔl) (Nˆ1), 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, Fˆ0.73, P40.7, Nˆ59, 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 ˆ0.068, 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 (Nˆ59).
Chicoreus pliciferoides Kuroda
Charonia sauliae (Reeve)
Fusinus forceps Fulton
Psephaea concinna Broderip
Tonna olearium (L.)
Psephaea diviesi (Fulton)
Murex troscheli Lischke
Hemifusus tuba (Gmelin)
Pleuroploca trapezium (Strebel)
Monoplex parthenopeum (Kuroda & Habe) Cymatiidae
Tonna luteostoma (Ku«ster)
Chicoreus asianus Kuroda
Neptunea kuroshio Oyama
*, 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
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 ˆ0.96,
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.
No. of
K. avis
Relative shell
area (%)
Total cylindroid dimension
of anemones (cm)*
*, 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)
Nˆ8 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 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, Fˆ1.11, 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).
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,
Nˆ21), 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 ˆ0.51, P50.001, Nˆ102) and among ovigerous
ones (r2 ˆ0.77, P50.001, Nˆ21; 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 (Nˆ97). 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.
K. avis types*
w2 ˆ5.16, 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,
Nˆ11), capsules with eye spots being slightly larger,
295 15 mm (Nˆ10; ANOVA, Fˆ93.41, P50.001).
Lengths of egg capsules were not related to the body
weights of hermaphrodites, either for egg capsules with
eye spots (r2 ˆ0.09, P40.3, Nˆ11) or those without them
(r2 ˆ0.04, P40.5, Nˆ10; 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
Y. Yusa et al.
Ecology of a parasitic barnacle
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 ˆ0.34, P50.001, Nˆ105). But this relationship was non-signi¢cant when hermaphrodites without
males were excluded (r2 ˆ0.10, Pˆ0.09, Nˆ31).
The maximum length of dwarf males (excluding
cyprids) were on average 0.96 0.220 mm (mean SD;
Nˆ34) shorter than cyprids (1.13 0.056 mm, Nˆ6;
ANOVA, Fˆ4.15, P50.05). Body sizes of hermaphrodites
had a positive correlation with lengths of dwarf males on
them (Figure 8B; r2 ˆ0.43, P50.001, Nˆ34), but not with
lengths of cyprids (r2 ˆ0.0004, P40.9, Nˆ6).
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).
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.
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Submitted 8 January 2001. Accepted 17 July 2001.
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