The Biology of Rhizocephala

/. mar. biol. Ass. U.K.
(1995), 75, 517-550 517

Printed in Great Britain
REVIEW PAPER
THE BIOLOGY AND LIFE CYCLE OF THE

RHIZOCEPHALA (CIRRIPEDIA)
JENS T. H0EG
Department of Cell Biology and Anatomy, Institute of Zoology, University of Copenhagen,
15 Universitetsparken, DK-2100 Copenhagen, Denmark
This review describes aspects of the life cycle and ecology of the Rhizocephala empha-
sizing (i) comparison with more conventional Cirripedia, and (ii) evolutionary and phylo-
genetic perspectives. Despite numerous extreme specializations to living as parasites in
other Crustacea, most features of the rhizocephalan life cycle resemble those seen in other
Cirripedia, and only the process of host invasion and the ensuing redifferentiation of the
adult parasite represent truly unique features. Larval biology of the Rhizocephala has
developed under selection pressures induced by the difficulty of locating the substratum
for settlement, host defences against parasite invasion, and the special demands imposed
on the sexual system of a parasite. Thus rhizocephalans have (i) lecithotrophy coupled
with very small-sized larvae, (ii) special sensory organs in the cyprid, (iii) a very rapid host
invasion accomplished by minute, female stages, and (iv) dwarf males nourished by the
adult female parasite, such that it emulates a true hermaphrodite. This review also
surveys the nature and underlying causes of the numerous effects that rhizocephalan
parasites can induce on their hosts in terms of morphology, physiology, and behaviour.
The 'host control' induced by rhizocephalans ensures that both male and female hosts
accept the parasite as their own brood and care for it accordingly. This, and other details of
host-parasite co-evolutions are discussed.
INTRODUCTION
Most authorities now recognize that the orders Thoracica, Acrothoracica and
Rhizocephala together form a monophyletic Cirripedia (H0eg, 1992a; Spears et al.,
1994), although Newman (1991) offers a somewhat different opinion. While the cirripede
orders Thoracica and Acrothoracica comprise sessile setose feeders, which we can
describe using ordinary crustacean terminology, the Rhizocephala have become singu-
larly specialized to parasitism within other Crustacea. Not only have rhizocephalan
parasites lost almost all traits normally found in Crustacea, but they also influence the
morphology and biology of their hosts to a remarkable degree. For these reasons the
Rhizocephala have always attracted the attention of biologists, since such extreme
specializations offer unique opportunities for biological and evolutionary insights.
518 J.T. H 0 E G
Our knowledge of rhizocephalan biology has increased significantly in the last

decade, rfoeg (1991) reviewed variations in the sexual system, Hoeg (1992b) empha-
sized ultrastructural details of their morphology, while Hoeg & Rybakov (1992) and
Hoeg & Liitzen (1993) discussed the taxonomy and phylogeny of the order. Finally,
O'Brien & van Wyk (1985) reviewed the effects rhizocephalan parasites have on the
growth of their hosts, but did not cover other aspects of 'host control' or its underlying
causes.
This review takes a novel approach in presenting rhizocephalan biology in an
evolutionary framework and, wherever possible, provides comparisons with more
conventional cirripedes, from which they must ultimately have evolved. The review
covers, (i) the biology of the Rhizocephala themselves; (ii) the very important relation
between these parasites and their hosts; and (iii) hypotheses for the evolution and
phylogeny of these intriguing parasites. Morphological details will receive attention
only where they serve to illustrate functional or evolutionary aspects.
According to H0eg & Rybakov (1992) the order Rhizocephala comprise 258 species in
two suborders, the Kentrogonida with three families and the Akentrogonida with five
families (Table 1). The basis for recognizing a monophyletic Akentrogonida rests on
characters expressed in larval metamorphosis and the sexual system, while the
Kentrogonida may represent a paraphyletic assemblage (Hoeg, 1991; Glenner & Heeg,
1994).
Table 1. The effects induced by rhizocephalan parasites on their crustacean hosts and a
summary of the taxonomy.
Parasite Number of Host Parasitic Parasitic Feminizationn
family (genera) species taxon anecdysis castratio of males
Kentrogonida (24) 226
Peltogastridae (14) 37 Anomura + +
Lernaeodiscidae (4) 16 Anomura + +
Sacculinidae (6) 173<.) Brachyura
Akentrogonida (13) 32<">
Mycetomorphidae (1) 1 Caridea + ?
Clistosaccidae (2) 2 Caridea

Anomura + + (e)
Thompsoniidae (4) 16 Caridea

Anomura
Brachyura
Stomatopoda +(c) + -
Duplorbidae (3) 6 Isopoda
Cumacea ? 7
Chthamalophilidae (3) 4 Balanomorpha - inapplicable
(37) 258
(a)
Some uncertainty exists concerning validity of a few species of Sacculina. (b) Polysaccus (2 species) and
Pirusaccus (1 species) have not yet been assigned to family. (c) While externae present, but host moults in
between externa generations.<d) Only few parasitized animals ever observed.(e) Degree of feminization very
slight.
THE BIOLOGY OF THE RHIZOCEPHALA 519
THE ADULT PARASITE

Parasitologists habitually separate endoparasites from ectoparasites, but this distinc-
tion meets with difficulty when applied to the Rhizocephala. The juvenile parasite
develops entirely within the host, but the adult consists of an external reproductive
body, called the extema, connected by a narrow stalk through the integument to a
ramifying system of nutrient-absorbing roots inside the host. The externa has a singu-
larly reduced morphology (Figure 1) and basically consists of a muscular mantle
enclosing a brood chamber, communicating with the exterior through an orifice, and a
visceral sac with a large ovary (Fteeg, 1992b). Most notably the externa lacks even the
rudiments of a gut, unless we accept that the root system represents the endoderm.
LIFE CYCLE
Figure 2 compares the life cycles of the three cirripede orders, viz. the Acrothoracica
(burrowing barnacles), the Rhizocephala, and the Thoracica (stalked and acorn barna-
cles). In most cirripede species, the larvae emerge from the mantle cavity of the adult as
nauplii that pass through three to six instars before metamorphosing into cyprids while
still pelagic. The cyprid, a larval form unique to cirripedes, locates a substratum suitable
for settlement, attaches permanently by cementation and initiates metamorphosis to
the sessile phase of the life cycle (Walker, 1992; Hoeg, 1992a,b). Only following cypris
metamorphosis do events begin to differ drastically, both between the orders and
between sexes, where these are separate (Glenner & Hoeg, 1994). Metamorphosed
thoracicans and acrothoracicans immediately commence direct development into the
adult. In the Rhizocephala, however, a female cyprid settles on a host animal and passes
through a more or less complex series of events culminating in the eventual injection of
the primordial parasite (Delage, 1884; Heeg, 1990). During the succeeding endoparasitic
phase the female grows its root system and eventually emerges through the host's
integument as the externa. To proceed to sexual maturity, the juvenile externa must
now acquire at least one male cyprid, which following settlement develops into a
morphologically very simplified dwarf male and serves the female parasite for the
lifetime of the externa. (In this review I prefer to use 'dwarf male' for all males that have
a reduced morphology, irrespective of whether they associate with females or her-
maphrodites.)
Figure 2 illustrates that, despite the previously mentioned specializations, most
aspects of the Rhizocephalan life cycle have equivalents in other cirripedes (Glenner &
Heeg, 1994). Although structurally simplified, the externa still possesses some rudi-
ments of ordinary barnacle morphology, especially in the reproductive system. Larval
development presents no remarkable differences. Even the apparently unique kentrogon
stage, which accomplishes host invasion in most Rhizocephala, has probably evolved
by specialization from the juvenile instar resulting from cypris metamorphosis in other
cirripedes (Glenner & H0eg, 1994). Similarly, many cirripedes other than the
Rhizocephala have morphologically reduced males ('dwarf males') associated with
either females (Acrothoracica, Thoracica) or with hermaphrodites (Thoracica), although
X
Q
m
0
Figure 1. An externa of the rhizocephalan Heterosaccus dollfusi (family Sacculinidae) on its host, the brachyuran crab Charybdis longicollis . Attachment under
the abdomen affords the parasite protection against mechanical damage and, since it sterilizes the crab, enables it to take advantage of the host's brood-care
behaviour. Male hosts become both morphologically and behaviourally feminized. Note the very simplified structure of the parasite externa.
Figure 2. Life cycles in the Cirripedia. Diagram emphasizing the basic similarities between the orders
Thoracica (A, B), Rhizocephala (C), and Acrothoracica (D). All species fertilize and brood the embryos
in a sea-water-filled mantle cavity and eventually emit broods of nauplii, or occasionally, cyprids.
The pelagic nauplii moult into cyprids, which settle onto a substratum that differs much between the
species, and also between the sexes where separate. Following attachment, the female or hermaphro-
dite cyprid metamorphoses, and thereafter, except in the Rhizocephala, commences a gradual
development into the adult organism. In the Rhizocephala, the metamorphosed female ('the kentrogon')
corresponds to the very juvenile barnacle in (A, B, & D). However, instead of maturing directly into
an adult, the kentrogon invades the host and thereby initiates the endoparasitic phase that ends when
the parasite emerges on the surface of the host with a reproductive body (= externa, here shown cut
away from host through the stalk). Host invasion and the ensuing redifferentiation of the injected
kentrogon cells into an externa primordium (stippled line in C) represents the only truly unique
feature in the rhizocephalan life cycle. Most Thoracica have pure hermaphroditism, where the
gregarious adults can cross fertilize (A). A separate male sex exists in some Thoracica (B), and in all
Rhizocephala (C) and Acrothoracica (D). Cyprids, which settle onto females or hermaphrodites,
develop into minute dwarf males (encircled). The rhizocephalan male in C, the 'trichogon', corre-
sponds ontogenetically to the female kentrogon. (Vignettes original or redrawn from various sources.)
522 J.T. H 0 E G
pure hermaphrodites prevail in the Balanomorpha (Figure 2). In fact this leaves the
injection and ensuing development of the endoparasitic phase as the only truly unique
characters (autapomorphies) in the rhizocephalan life cycle (Glenrter & Hoeg, 1994).
Even trophic root systems exist in parasitic species of the Thoracica, although they
undoubtedly evolved convergently with those of the Rhizocephala (Anderson, 1994).
When comparing cirripede life cycles, perhaps the most surprising feature concerns
the fact that structurally very similar cyprids can accomplish settlement on a remark-
able variety of substrata, and thereafter accomplish metamorphosis into stages as
morphologically and functionally different as a rhizocephalan kentrogon, a juvenile
setose feeder, or the various forms of dwarf males (Figure 2). This extreme flexibility of
the cyprids within a quite rigid morphological framework undoubtedly contributes to
the well-known success and diversification of the Cirripedia, as discussed by Crisp
(1984), who described the cyprid as the pinnacle of sessile evolution.
While members of the suborder Kentrogonida have largely similar life cycles, signifi-
cant variation exists within the Akentrogonida. The generalized life cycle illustrated in
Figure 3 summarizes both general features and their variations, but does not necessarily
represent the ancestral scheme.
LARVAL DEVELOPMENT
The Rhizocephala have an entirely lecithotrophic development, but except for a
reduced naupliar feeding apparatus, no obvious traits in external morphology distin-
guish rhizocephalan nauplii and cyprids compared with those of other cirripedes
(thaeg, 1992a,b; Moyse et al., in press). The absence of even the rudiments of a gut in the
larvae cannot surprise us, considering that the adults have replaced this organ with the
root system.
Lecithotrophy means that the larvae possess only a finite amount of energy to
complete their development from hatching through metamorphosis. Accordingly,
rhizocephalans have an ontogeny abbreviated in both duration and numbers of larval
instars compared with the mostly planktotrophic thoracican barnacles. In this they
resemble the other cirripede order characterized by lecithotrophy, the Acrothoracica.
Most Acrothoracica and Rhizocephala have only four naupliar instars, while the
Thoracica, whether lecithotrophic or not, generally retain the plesiomorphic cirripede
condition of six instars. Some Rhizocephala, including all Akentrogonida, even omit
naupliar stages altogether and hatch as fully-developed cyprids. Such omission of
nauplii coupled with lecithotrophic development also occurs in the thoracican families
Scalpellidae and Tetraclitidae, and in some Acrothoracica (Anderson, 1994). Cyprids of
the rhizocephalan family Chthamalophilidae represent an extreme case in that they
cannot swim but disperse solely by walking on the substratum with the antennules.
This may represent an adaptation to avoid dispersal, since chthamalophilids parasitize
balanomorph barnacles that live in very dense populations (Bocquet-Vedrine, 1961,
1972). Chthamalophilid cyprids would offer an interesting model for testing Yule &
Walker's (1985) theory of a finite amount of temporary antennular adhesive. An
LARVAE PARASITE
EXTERNA
Emission of nauplii Fertilization of eggs
by implanted c/and
Emission of cyprids brooding of embryos
\ EXTERNA
NAUPLIUS
Implantation of cf
3-5 instars trichogons formed
Lecithotrophic from settled cyprids
Cyprids implant
naked a* cells
\
cCand
CYPRIDS
GSD t
EXTERNA
sexually dimorphic d1 cyprids settle
on virgin externa
ESD?
No sexual dimorphism
CYPRID
t
EXTERNA
9 cyprid settles Emergence on host
on crustacean host as virgin externa
HOST INVASION
By kentrogon formed
from settled 9 cyprid
t
ENDOPARASITIC PHASE
Development of externa
By settled cyprid itself Proliferation of roots
Figure 3. Diagrammatic representation of the rhizocephalan life cycle. In boxes divided by stippled
lines, the top half describes the situation and putative ground pattern found in most Kentrogonida
(K), while the bottom half describes the situation seen in the Akentrogonida and exceptionally in a
few Kentrogonida. The stippled arrow between host invasion and endoparasitic phase signifies that
these processes remain to be described in detail. GSD, Genetic sex determination; ESD, environmen-
tal sex determination.
undoubtedly convergent case of non-swimming cyprids also exist for a few species of
Acrothoracica (Turquier 1985).
Duration of the naupliar phase depends on water temperature and lasts from two
days in the estuarine Loxothylacus (at 25-30C) to more than three weeks in the cold-
water Briarosaccus (5C) (Walker, 1985, 1987, 1988; Walker et al., 1992; Hawkes et al.,
1985). As in other cirripedes, the cypris stage has a very variable duration, ending only
524 J.T. H 0 E G
with settlement, or death, probably from the exhaustion of energy reserves. In the
Thoracica, Lucas et al. (1979) showed that unless a critical amount of energy remains in
the cyprid at the time of settlement, it cannot complete metamorphosis into the feeding
juvenile. We still lack comparable studies of energy metabolism in rhizocephalan
larvae. However, in partial agreement Hoeg & Ritchie (1987) reported how settlement
activity in female cyprids decreased with time.
SITE OF SETTLEMENT
When settling on the host, the female cyprids always attach in places with thin,
unsclerotized cuticle, and this presumably facilitates the ensuing infection process.
However, although each species has a specific site of attachment (e.g. gill filaments or
bases of setae), the site often differs, even between closely related parasites (Veillet,
1964; Ritchie & Hoeg, 1981; H0eg, 1985a,b).
In some akentrogonids, and perhaps also a few kentrogonids, the female cyprid
attaches at the site where the externa will eventually emerge (Reinhard, 1942; Bocquet-
Vedrine, 1961; Heeg, 1982,1990). However, in most cases the cyprid attaches in a quite
different place on the host body, a situation first discovered by Delage (1884) and one
requiring that the juvenile endoparasite migrates through the haemocoel in order to
reach its eventual site of emergence (Smith, 1906). According to Ritchie & Heeg (1981)
the site of settlement is to a large extent governed by the parasite's need to circumvent
grooming defences on the part of the host.
CYPRID METAMORPHOSIS AND HOST INVASION

In the Kentrogonida, the settled cyprid always passes through a metamorphic moult
resulting in a new and highly specialized instar: the kentrogon in females, and the
homologous, but morphologically very different trichogon in males (Figure 2; Delage,
1884; H0eg, 1985a, 1987a). Both stages are much smaller than the cyprid, since the entire
thorax and several other structures remain behind with the spent cypris carapace.
In some species the cyprid can accomplish metamorphosis within as little as ten to
twenty minutes following attachment, apparently because numerous, but subtle, differ-
ences between male and female cyprids at the ultrastructural level foreshadows the
formation of a trichogon or a kentrogon (Hoeg, 1987b).
Despite its minute size the kentrogon has a rather complex morphology (Hoeg,
1985a). Within about two days of settlement, the kentrogon penetrates into the host
using a hollow cuticular stylet, which afterwards serves as a hypodermic needle for
injecting the primordial parasite. Unpublished in vivo observations of many Sacculina
carcini kentrogons have demonstrated that stylet penetration lasts about ten minutes,
while expulsion of the primordial parasite follows after one to three minutes delay and
lasts only ten to twenty seconds. We lack detailed information on the mechanism of
stylet penetration, but it probably proceeds as a purely mechanical process without the
chemical dissolution of host cuticle, as argued by Hoeg (1985b, 1990) for akentrogonids.
In S. carcini, the usually slightly-curved stylet sustains several S-bends from a build-up
of elastic energy just prior to penetration, only to straighten out within seconds when it
finally breaches the host cuticle in a process lasting <30 s (unpublished observations).
Heeg (1985a) argued that kentrogons of Lernaeodiscus porcellanae inject only a single
cell. However, in S. carcini a much more bulky shape with unknown contents emerges
from the stylet tip (Heeg, 1992b, figure 17D). In another sacculinid, Loxothylacus panopaei,
a voluminous and very elongate body emerges from the stylet tip and initiates vigorous
movements (H. Glenner, personal communication). Scrutiny of this new stage may well
help to explain how the endoparasitic phase first became established in rhizocephalan
evolution.
As implied by the taxon name we assume that all species of the suborder
Akentrogonida lack a kentrogon (and a trichogon) (Figure 3, Table 1). Direct observa-
tions have now verified this for the Clistosaccidae and Thompsoniidae, where the
settled cyprid does not moult but employs an antennule to penetrate through the
underlying integument (Heeg, 1985b, 1990; Bower & Boutillier, 1990; Heeg & Liitzen,
1995). In these families, moreover, host invasion and dwarf male implantation differ
only in the substratum on which the cyprid has attached (host or virgin externa).
GROWTH OF THE INTERNAL PARASITE

Most if not all differentiated tissues remain within the spent kentrogon, which serves
only as a vehicle for infection. It is therefore assumed that the early endoparasite must
(embryo-like) differentiate all tissues de novo from embryonic cells inoculated by the
kentrogon (Smith, 1907; Heeg 1985a, Hoeg, 1992b). In this the Rhizocephala stand apart
from most other parasites among non-helminth Metazoa and certainly from all other
parasitic Crustacea, except perhaps the recently discovered Tantulocarida (Boxshall &
Lincoln, 1987; Huys, 1991; Huys et al., 1993). Unfortunately, we know nothing about
this early growth phase, during which 'host control' becomes established. The smallest
endoparasitic stages found (Smith, 1906; Bocquet-Vedrine, 1961; H0eg, 1990) have
already differentiated into an enclosing epithelium and a central 'anlage' of the repro-
ductive organs. In Sacculina carcini, such internae measure about 200 nm across and
occur about four weeks after infection between the alimentary tract and the thoracic
ganglia of the host (Rubiliani et al., 1982). They already carry many short roots and
migrate posteriorly along the gut until they reach the position in the abdomen whence
the externa will eventually emerge. Duration of the internal phase from invasion to
emergence of the externa ranges from three weeks in Loxothylacus panopaei to 1-3 y in S.
carcini (Walker et al., 1992; Liitzen, 1984).
THE ROOT SYSTEM

Distribution within the host
The juvenile and adult parasites obtain nourishment solely by means of a trophic
organ. Except for Chthamalophilus delagei, this organ takes the form of a ramifying
526 J.T. H 0 E G
system of roots growing out from the early endoparasite and extending into the host
from the stalk of the externa (Hoeg, 1992b). Root systems also occur in other parasitic
Crustacea (e.g., nicothoid copepods), but they undoubtedly reach the high point of
specialization in the Rhizocephala.
The degree to which the roots proliferate through the host varies extensively. In
species of some genera (Sacculina, Thompsonia), the roots may reach most parts of the
body including the appendages, while in other species the roots do not extend beyond
the abdomen (Clistosaccus) or may even be limited to the area immediately around the
stalk (Boschmaella). Finally, Chthamalophilus has only a large, slightly lobed bladder
inside the host.
In most Rhizocephala, including all Kentrogonida, the roots infiltrate both the gut
and the hepatopancreas, but apart from this the ventral nerve cord represents the only
other organ frequently reached by roots. This corresponds to the fact that the root
system has two principal functions, (i) absorption of nutrients, and (ii) host control
effected through pertubations to the neuroendocrine system of the host (see below).
Roofs and multiple externae

A special problem concerns the organization of the root system in species with
several externae on the same host. At least in the kentrogonid genus Peltogasterella and
in the akentrogonid family Thompsoniidae, multiple externae all connect to a common
root system and therefore represent a single individual (colonial externae) (Potts, 1906;
Perez, 1931a,b, 1932; Hoeg, 1982; Heeg & Liitzen, 1995).
Root ultrastructure
The dendritic nature of the roots and numerous villus-like projections covering their
delicate cuticle provides the entire system with an enormous surface area for absorp-
tion of nutrients from the host (Hteeg 1992b). Unfortunately the physiological details
remain virtually unknown and the same holds true for the ensuing longitudinal
transport of substances towards the stalk and externa (Hubert et al., 1979; Payen et al.,
1981a, 1983). Already Fischer (1928) noted that the host fails to exhibit any pronounced
defence against the growing roots, such as enveloping them in connective tissue as is
the case with other foreign objects (Rubiliani et al., 1980a). Clearly, the physiology of
rhizocephalan roots needs closer study.
EMERGENCE OF THE EXTERNA

The externa almost invariably emerges in the brood chamber of the host, a position
that affords both support, protection, and adequate ventilation. Parasites of decapods
emerge on the ventral side of the abdomen, those on peracarids emerge in the marsupial
brood pouch, while species of the Chthamalophilidae emerge within the mantle cavity
(= brood chamber) of their barnacle host. Only species of the colonial, and very
specialized family Thompsoniidae deviate in that they occur almost everywhere on the
body (H0eg & Liitzen, 1993). This more exposed position may explain why thompsoniid
parasites lose a substantial number of their externae before they manage to reproduce
(Liitzen, personal communication). Similarly, sacculinid externae may sometimes emerge
on the dorsal side of the abdomen but they invariably die from mechanical damage
before they reach sexual maturity.
Most rhizocephalans emerge when the host moults, but some species (e.g. Peltogaster
paguri and Clistosaccus paguri on pagurids and Sacculina carcini on portunid crabs) can
emerge from hosts at any stage during the moult cycle (H0eg & Liitzen, 1995). Externa
emergence must have represented a critical factor in rhizocephalan evolution, since it
could easily endanger both host and parasite. Prior to emergence, the parasite securely
fuses its own cuticle to that of the host in a ring-shaped zone around the base of the
future stalk. This ensures a firm holdfast for the externa and also avoids producing an
open wound in the host integument.
THE VIRGIN EXTERNA AND ACQUISITION OF MALES

Following emergence, the female parasite must acquire a male, and those that fail to
do so cannot reproduce (Ichikawa & Yanagimachi, 1958; Heeg & Ritchie, 1985). In the
Kentrogonida, the virgin externa acquires an open mantle orifice within a few days of
emergence, and following this event it immediately begins to attract male cyprids from
the plankton (Ritchie & Heeg, 1981). Having settled in or around the mantle aperture,
the male cyprid metamorphoses into a trichogon and becomes implanted into one of the
two preformed receptacles (Heeg, 1987a). This indicates that rhizocephalan males are
reacting to a substance emanating from the receptacles in the mantle cavity and being
released into the water column when the mantle orifice appears (H0eg, 1991; Clare et
al, 1993).
The mode of acquiring males seen in the Kentrogonida represents the plesiomorphic
condition (H0eg, 1991). In the Akentrogonida, the virgin externa lacks both a mantle
aperture to allow entrance of the male and, except for Clistosaccus, also a preformed
organ to receive it (Bocquet-Vedrine, 1961; Liitzen, 1981; Heeg, 1982,1991; H0eg et al.
1990; Heeg & Liitzen, 1993). It follows that male implantation must proceed differently
in this suborder. Where observed, male cyprids use antennular penetration, as in host
invasion, and introduce a large number of naked cells into the mantle tissue of the
virgin parasite. In Clistosaccus, this can, most surprisingly, occur even before emergence
has taken place (Heeg, 1985b). The introduced cells develop into spermatogonia, but
initially they do not differ from those injected into host animals (Heeg, 1985b, Bower &
Boutillier, 1990).
In the Kentrogonida, many male cyprids will often settle on a single externa, but only
two will eventually succeed in reproducing, one in each receptacle (H0eg, 1987a), and
the externa can reproduce normally with only one male. In the Akentrogonida, the
number of implanted males may range from one to more than ten (Heeg, 1985b; Heeg,
1991; Heeg & Liitzen, 1995). The young externa always ceases to attract males within a
few days of the first implantation, so externae containing more than a single male must
have received these within a very limited time span (Heeg & Ritchie, 1985).
528 J.T. H 0 E G
MATURATION TO THE ADULT

The pre-adult phase, from emergence to first brood release, lasts one to four weeks,
provided the externa receives a male without delay (Liitzen, 1981; H0eg, 1982; Heeg &
Ritchie, 1985; Heeg & Liitzen, 1993). Failing this, virgin externa of species with a
receptacle (the Kentrogonida and the akentrogonidan species Clistosaccus paguri) will
remain in stasis, until the arrival of a male stimulates it to resume development into an
adult. Virgin Lernaeodiscus porcellanae can successfully attract males as long as six
months after emergence, but in most species the externa will have perished much
sooner (Liitzen, 1984; Heeg & Ritchie, 1985). With the exception of Clistosaccus, all
Akentrogonida will apparently continue development whether they receive males or
not, and will eventually spawn unfertilized, aborted eggs (Liitzen, 1981; Heeg, 1982;
Heeg et al., 1990; Heeg & Liitzen, 1995). This trait cannot confer any selective advan-
tage, but may reflect that akentrogonids grow so slowly that the externae usually
succeed in getting males in time.
REPRODUCTION
The male organ
Whatever the morphological details, the implanted male becomes an integral part of
the female and effectively substitutes for a true testis, so the male-female association
will emulate a true hermaphrodite (cryptogonochorism sensu Bresciani & Liitzen, 1972).
Unlike thoracican barnacles with dwarf males, rhizocephalan females can acquire male
cyprids only during the earliest part of the external phase. These males, however,
receive nourishment from the female and can therefore remain with the externa until it
dies. In multiparous species (Kentrogonida, Duplorbidae, Chthamalophilidae), the
male or males pass through multiple cycles of spermatogenesis perfectly synchronized
with the female's reproductive cycle.
The kentrogonidan system with cuticle-clad male trichogons and paired receptacles
in the female represents the most plesiomorphic type (Heeg, 1991). The receptacles
undoubtedly originated as simple imaginations of the mantle cavity integument, but in
all extant Kentrogonida they have evolved into very specialized structures (Heeg,
1987a). Very little information exists concerning the ensuing events in the receptacle
and the details of fertilization (Heeg, 1992b; Heeg & Liitzen, 1995).
Males in the Akentrogonida have reached the ultimate reduction, since they consist
only of naked spermatogonia. According to taxon, the akentrogonid male initiates
spermatogenesis either in the mantle, in the ovary at the expense of oocytes, or most
extraordinarily, in bodies invaginated from the mantle and floating freely in the brood
chamber among eggs or embryos (Heeg, 1991; Heeg & Liitzen, 1993; Heeg & Liitzen,
1995). Free-floating male bodies exist in all multiparous akentrogonids. In these species,
a tubular and very constricted mantle aperture assures that the male bodies remain in
the mantle cavity even when they release larvae. Historically, Smith (1906) first de-
scribed the free-floating male bodies in Duplorbis, but misinterpreted them as cuticle-
clad dwarf males that had entered through the mantle aperture. In fact the epithelium
and cuticle enclosing each body originate from the female.
The cryptogonochoristic sexual system of the Rhizocephala has equivalents in some
parasitic Copepoda and Gastropoda and in a bivalve (Bresciani & Liitzen, 1972, 1974;
Liitzen, 1979, and personal communication). In Thoracica, however, dwarf males al-
ways remain independent organisms that can either obtain their own food (some
Scalpellidae) or must remain lecithotrophic throughout, resulting in a limited life span
(Klepal, 1985,1987; Gotelli & Spivey, 1992). In the latter case, the female or hermaphro-
dite must therefore repeatedly recruit new male cyprids from the plankton (Svane,
1986). Interestingly, rhizocephalan species that regularly regenerate lost externae
{Peltogasterella, Sacculina senta, Thompsoniidae) must similarly re-acquire males for
each successive externa generation. Colonial Rhizocephala have a similar problem in
that each externa must receive its own male in order to reproduce. However, in the
Thompsoniidae, where the number of externae per host may reach thousands, Jespersen
& Liitzen (1992) showed how the genus Diplothylacus has circumvented this dilemma.
All externae can receive male cyprids, but only a minority need actually succeed, since
sperm can swim between externae via the root system and ensure fertilization of the
whole colonial generation.
Oviposition and fertilization

Although the rhizocephalan externa has a very simplified structure, details of ovipo-
sition, fertilization, and brooding deviate little from events in the Thoracica. Most
rhizocephalans have specialized the terminal part of the oviduct into a so-called
colleteric gland, which we can relate to the oviducal gland in thoracican barnacles
(Walker, 1992; Hoeg & Liitzen, 1995). Moreover, like all other Cirripedia, rhizocephalans
fertilize and brood the eggs in a sea-water-filled mantle cavity (Walker, 1992) and have
therefore retained the flagellated, motile sperm seen in acrothoracicans and thoracicans
(Healy & Anderson, 1990; H0eg 1992a). This cirripede condition, where spermatozoa
swim through sea-water to reach the eggs, is unique among Crustacea, and must
represent a plesiomorphic trait retained in an otherwise highly specialized taxon.
Peristalsis in the mantle assures ventilation of the brooded embryos and probably also
of the externa tissues. It is noteworthy that some species of the Peltogastridae and
Lernaeodiscidae have haemoglobin, whereas sacculinids have haemocyanin like most
other Crustacea (Block-Raphael, 1948; Fox, 1953; Shirley et al., 1985; Herberts & de
Frescheville, 1981). In comparison, thoracican barnacles seem to lack respiratory pig-
ments altogether (Waite & Walker, 1988) so it cannot be stated with confidence what
type of pigment was present in the ancestral cirripede.
Moulting, reproductive cycle and longevity

Multiparous species (Duplorbidae, Chthamalophilidae, and almost all Kentrogonida)
pass through a moult between emission of larvae and the next oviposition. This cleans
the brood chamber of unhatched embryos and egg parasites and also removes epibionts
530 J.T. H 0 E G
from the exterior surface of the externa. Except for the Sacculinidae, which fail to moult
the exterior surface, such regular moulting results in the accumulation of ecdysial rings
around the stalk (Brinkman, 1936). The number of these rings allows an accurate
estimation of externa age by the formula: Externa age = (ring number) (brood interval
duration) - preadult phase duration.
We can estimate the duration of the preadult phase and brood interval by laboratory
experiments (Ritchie & rteeg, 1981; H0eg & Liitzen, 1995), but some cold water species
exhibit a distinct annual cycle in the ring pattern that enabled Liitzen (1987) to calculate
directly a maximum age of five years in Peltogaster paguri parasitizing hermit crabs and
ten years in Briarosaccus callosus on king crabs.
In general, semelparous externa (e.g. those of Peltogasterella) have shorter life spans
than multiparous ones. However, in the Thompsoniidae, the semelparous externae
grow for a surprising four to five months before they release their first and only brood
(Liitzen & Jespersen, 1992). Within the same time span, the multiparous externa of a
sacculinid could have reached sexual maturity and released more than eight broods.
Size and sex of larvae

Sexual dimorphism
All Rhizocephala have separate sexes. In the Kentrogonida, female and male nauplii
differ in size (Collis & Walker, 1994), while the cyprids differ in both size, structural
details, choice of substratum for settlement, and type of metamorphosis (Heeg, 1984,
1987, 1991; Walker, 1985). Male cyprids are larger than females and have a better
armature of sensory structures. As a further complication some Rhizocephala have a
distinct seasonal variation in mean size of larvae superimposed on the sex-linked size
difference (Heeg, 1984; Walker, 1988; Heeg & Liitzen, 1995). Female cyprids settle
exclusively on potential host animals, while male cyprids never attach directly on the
hosts but only on virgin female parasites. In addition, the cyprid sexes differ in
numerous ultrastructural details, relating to the ensuing dissimilar metamorphosis into
kentrogons and trichogons (Yanagimachi, 1961; Ritchie & tfoeg, 1981; H0eg, 1984,
1987b).
Sex ratio in broods

In the Kentrogonida, any single brood of larvae may consist exclusively of one sex or
of any ratio between the two sexes. The sex ratio may also change through successive
broods released from the same externa. At the population level, the sex ratio in the
larvae changes with season, so males predominate when new externae emerge, ensur-
ing their sexual maturation (Ritchie & Hoeg, 1981; Hoeg, 1984; Walker, 1985,1987,1988;
Haeg & Liitzen, 1995). Walker (1987) investigated which factors may control these
changes in larval sex, and while failing to pinpoint a specific cause, he could at least
eliminate both temperature and day length.
Determination of sex (GSD or ESD)

Species of the Kentrogonida have genetic sex determination (GSD), where sex is fixed
already in the unfertilized egg (Yanagimachi, 1961; Ritchie & Heeg, 1981; Walker, 1985),
but the mechanism responsible for this remains obscure. Yanagimachi (1961) identified
so-called sex chromosomes in a peltogastrid species. However, both Yanagimachi
(1961) and I (unpublished observations) have observed broods with larvae of both sexes
in peltogastrids. This situation, now known to be normal for other Rhizocephala
(Ritchie & Hoeg, 1981; Walker, 1988), causes serious trouble for the mechanism of sex
determination originally suggested by Yanagimachi (1961). Fratello (1968) failed to find
any comparable sex chromosomes in the Sacculinidae.
Almost all Akentrogonida lack morphological traits separating male and female
larvae (Glenner et al., 1989), and this allows for the possibility of environmental sex
determination (ESD), i.e. that sex becomes fixed by the type of substratum only (host or
virgin externa) upon which attachment takes place (Heeg, 1991). Under ESD the
planktonic and sexually indeterminate cyprid could hypothetically search first for a
host animal and by default proceed with female-type host invasion, unless the host
already carries a virgin parasite in which case it would implant itself as a dwarf male. In
thoracican barnacles with a separate male sex it appears that both ESD and GSD may
operate (Gomez, 1975; Crisp, 1983; Svane, 1986).
Reproductive output
Within a species, externa size correlates well with brood size, because the ovary
occupies the majority of the externa tissue. For Lernaeodiscus porcellanae in southern
California, accurate information exists for both parasite prevalence, size and age struc-
ture, correlation between externa size and brood size, and mean brood interval. These
data enable us to calculate the reproductive output for an entire parasite population,
and an individual externa will, according to size, produce a brood of between 1,000 and
20,000 nauplii every two to three weeks for up to two years (Ritchie & Heeg, 1981; Haeg
& Liitzen, 1995). Almost comparable data exist for a few additional species (Liitzen,
1984), but normally there exist only scattered data relating brood size to externa size for
a few individual parasites.
Truly semelparous species exist only in the Akentrogonida, which always release
their larvae as cyprids. This will presumably result in a much-reduced presettlement
mortality due to the short planktonic phase and may compensate for the reduction in
brood number. However, some multiparous species also release their larvae as cyprids
(Bocquet-Vedrine, 1961; Andersen et al., 1990), so no single factor can explain all cases
with abbreviated larval development.
In species with obligatory colonial externae, brood size may fall below 100 (Heeg &
Liitzen, 1995), but the presence of numerous externae (in thompsoniids up to many
thousands) ensures a high reproductive output. Colonial species may gain the advan-
tage that loss of one or a few externae will not lead to total failure of a reproductive
cycle. Moreover, while individual externae release only one to three broods, Peltogasterella
532 J.T. H 0 E G
and the thompsoniids develop through several successive generations of externae

(Perez, 1932; Liitzen & Jespersen, 1992; H0eg & Liitzen, 1995).
LARVAL ECOLOGY
Lecithotrophy and size of larvae
Lecithotrophy occurs in all Acrothoracica and in many Thoracica, but the fact that
rhizocephalan larvae uniquely lack limb gnathobases and have very reduced append-
age setation and a minute labrum testifies to a profound specialization to this type of
ontogeny (Walker, 1988). The crustacean ground pattern undoubtedly included
planktotrophic nauplii (Walossek, 1993). Some of the parasitic Ascothoracida and most
Cirripedia have retained this ontogeny, where initially small-sized nauplii can grow
large and accumulate energy during an extended planktonic phase (Strathmann, 1993).
Lecithotrophic Cirripedia normally ensure the same end by producing large, energy-
rich eggs, resulting in a decreased mortality due to a short planktonic phase at the
expense of a small brood size. Interestingly, however, the lecithotrophic Rhizocephala
have some of the smallest eggs and larvae within the Cirripedia, with cyprids in the 70-
400 fim range compared with >600 urn in lecithotrophic Scalpellidae (Barnes, 1953;
Glenner et al., 1989; Anderson, 1994). Several factors would favour such small size in
rhizocephalan larvae: (i) while small size at settlement undoubtedly correlates with
high mortality in ordinary barnacles, the Rhizocephala develop inside a host, protected
from the external environment and with lavish energy reserves at their immediate
disposal; (ii) the large reproductive output implicit in small-sized larvae counteracts the
expectedly very high failure rate in locating and successfully infesting a host (see
below); and (iii) small larvae may stand a better chance of circumventing host grooming
defences (see below).
Substratum location and larval success

The substratum for female settlement (host animals) occurs with a much greater
frequency than the substratum for male settlement (hosts carrying virgin parasites).
Perhaps to assist in locating their rare substratum, male cyprids carry larger and more
numerous thin-walled sacs on the antennules than female cyprids. In external morphol-
ogy, these sacs resemble the olfactory aesthetascs known from groups such as the
Copepoda (Walker, 1985; Glenner et al., 1989). But no experiments have verified
whether or not male cyprids can, at a distance, detect water-borne pheromones released
from the virgin (Hoeg, 1991; Clare et al., 1993) as has been demonstrated by Anderson &
Dale (1989) for larvae of the parasitic isopod Probopyrus pandalicola. The generally larger
size and consequently larger energy reserves of male cyprids may also allow them to
search longer for virgin externae. However, while male cyprids may have more diffi-
culty in locating a substratum than females, they stand a much better chance of
metamorphosing successfully once they have settled. In a lernaeodiscid, Ritchie &
Hoeg (1981) and Fleischer et al. (1991) showed how settled female cyprids must cope
with the extremely effective grooming defence of the porcellanid host, which normally
can remove all parasite larvae before they manage to invade. Male cyprids do not risk
such removal, and their empty carapaces can remain for several days around the mantle
aperture following expulsion of the trichogon (unpublished observations).
Acquisition of males and invasion of the host represent two very critical phases in the
rhizocephalan life cycle. In both sexes, the cyprids metamorphose with surprising
speed (<10 min). In females, Hoeg (1985a) saw this as a defence against host grooming,
since the crab can more easily remove the cyprid than the small and scale-shaped
kentrogon. In males, H0eg (1987a, 1991) explained the rapid formation of the trichogon
as a result of competition between several males trying to reach into one of the two
available receptacles. Alternatively, the rapid metamorphosis in both sexes may merely
reflect the effect of small size and limited energy resources. For the externa, successful
implantation of males rarely represents a critical factor. H0eg & Ritchie (1985) found
that virgin externae of Lernaeodiscus porcellanae acquired males within a few days, while
in English Channel populations of Sacculina carcini the frequency of male cyprids
settled per virgin averages two, i.e. sufficient to 'fill' both receptacles (unpublished
observations).
EVOLUTION OF THE RHIZOCEPHALAN SEXUAL SYSTEM

Separate sexes or hermaphrodite ancestor
Pure hermaphroditism is the most widespread sexual system in the Cirripedia, but
this does not necessarily mean that it is also ancestral. As illustrated in Figure 2, the
Rhizocephala do not stand alone among cirripedes in having separate sexes (Klepal,
1985,1987). Figure 4 shows the sexual systems plotted onto a phylogeny of the Cirripedia
Cirripedia
Tantulocarida Ascothoracida Acrothoracica Rhizocephala Thoracica
9c/ 9d'($f) 9c/ 9b' 9/ c/y 9c/
Figure 4. The occurrence of males in the Cirripedia and closest relatives mapped onto a putative
phylogeny. The Thoracica have all possible combinations, while the remaining Cirripedia and
immediate relatives all have separate sexes. This could indicate that both the rhizocephalan and the
cirripede stem species had separate sexes. Hermaphroditism exists in a few Ascothoracida, but
probably not in the ground pattern (Grygier, 1987). Where present, cirriped males are dwarf males
permanently associated with the larger females (dioecy) or hermaphrodites (androdioecy).
534 J.T. H 0 E G
and their closest relatives, based on both traditional characters, larval ultrastructure
and molecular data (Heeg, 1992a; Huys et al., 1993; Spears et al., 1994). This illustrates
that, except for the Thoracica, all relevant outgroups to the Rhizocephala have separate
sexes and suggests that this was also the case both in the rhizocephalan and in the
cirripede stem species. This claim also receives indirect support from comparison with
other highly specialized parasites among copepods and gastropods, none of which
developed their cryptogonochoristic systems from an ancestral hermaphroditic state
(Bresciani & Liitzen, 1972,1974; Liitzen, 1979). Moreover, the thoracican genera Rhizolepas,
parasitic on annelids, and Anelasma, parasitic on sharks, are hermaphrodites and so
testify that parasitism in the Cirripedia does not necessarily entail the existence of
dwarf males. On the other hand, the thoracican family Scalpellidae exemplifies the case
where males have evolved from normal hermaphrodites, and where species that
combine dwarf males with pure females (androdioecy), probably represent the most
advanced condition (Newman, 1980; Klepal, 1987).
The advantage of cryptogonochorism

Whatever the evolutionary starting point (pure hermaphroditism or presence of
males) the cryptogonochoristic situation in the Rhizocephala confers obvious advan-
tages. For sessile organisms living at very low population densities, such as parasites,
there is only a remote chance that any two individuals will succeed in infesting the same
host and interbreeding (Crisp, 1983). Nevertheless, this is exactly what must happen in
Anelasma and Rhizolepas. Compared with these parasites, both rhizocephalan sexes gain
advantage from having cryptogonochoristic dwarf males. A larva settling as a male,
benefits from circumventing the very chancy process of invading the host and from
reaching sexual maturity within days rather than months of settlement. The female
parasite also benefits enormously from acquiring a lifetime's source of external sperm
at the small cost of offering protection and nourishment to the male. Finally, many
Rhizocephala exercise profound control over their hosts and could hardly do so unless
they occurred singly, a condition enabled by having dwarf males.
HOST SPECIFICITY
Most rhizocephalan species occur on more than one host species. Some, such as
Briarosaccus callosus and Clistosaccus paguri, parasitize a surprising number of species
and in Sacculina carcini the eleven known hosts belong to three different brachyuran
families (Boschma, 1962; rfeeg, 1982; Heeg & Liitzen, 1985; Hoggarth, 1990). However,
rhizocephalan taxonomy relies heavily on very crude morphological characters. There-
fore some of these cases may well represent sibling species, which can be separated only
by chromosome numbers (Fratello, 1966,1967,1968), larval ultrastructure (Andersen et
al., 1990), or perhaps isoenzymes. It seems that host specificity does not rest with the
cyprid, since they settle and metamorphose on crab species that do not normally carry
externae in the field (Ritchie & Heeg, 1981; Rubiliani, 1984; Hoeg & Liitzen, 1995). Such
normally 'fatal errors' could perhaps lead to successful establishment on a new host
species. The Thompsoniidae may exemplify this, since they parasitize not only a wide
range of Decapoda but also the Stomatopoda (H0eg & Liitzen, 1993). Likewise, species
of the Chthamalophilidae occur on both Chthamalidae and the distantly related Balanidae
(Heeg et al., 1990). Sometimes the parasite seems to have followed the host through an
evolutionary specialization. Thus most peltogastrids occur on true hermit crabs, while
Briarosaccus occurs on lithodids, which represent highly specialized paguroids
(Cunningham et al., 1992). Sesarmaxenos, which parasitizes true freshwater crabs, must
obviously have followed the host throughout specialization to this environment. How-
ever, a comprehensive understanding of the evolution of host specificity will require a
detailed phylogenetic analysis of both hosts and parasites (Brooks, 1988; Brooks &
McLellan, 1991,1993).
EFFECTS ON THE HOST

Most Rhizocephala exercise what Ritchie & H0eg (1981) labelled 'host control' in that
they profoundly influence the host at levels of both morphology, physiology, and
behaviour (Baudoin, 1975; O'Brien & van Wyk, 1985; Sparks, 1985; Hubert et al., 1989).
Most of these effects are highly interrelated, but it nevertheless seems practical to
separate them into changes of sexual characters (parasitic castration, feminization of
males, 'egg mimicry') and changes in moult cycle and growth.
The classical review by Reinhard (1956), and also Hartnoll (1967) and O'Brien & van
Wyk (1985), rightly emphasize variation and evolutionary aspects. Most other accounts
erroneously generalize that all Rhizocephala (i) sterilize both host sexes, (ii) feminize
infested males, and (iii) arrest the moult cycle of all infested animals. However, many
rhizocephalans do not exhibit these full-scale effects, nor were they all present in the
stem species (Ritchie & Hoeg, 1981). In fact the extent of modifications to the host varies
extensively both between different host species infested with the same parasite and
between different parasite species (see, e.g., Rubiliani et al., 1980a,b; O'Brien & van
Wyk, 1985; Sparks, 1985). At higher taxonomic levels the variation ranges from little or
no effect in hosts of the Chthamalophilidae to the very extensive host control exercised
by the Sacculinidae. The Kentrogonida generally induce more profound effects than the
Akentrogonida (Bocquet-Vedrine, 1961; Ritchie & H0eg, 1981; Hubert et al., 1989).
Parasitic host control in Crustacea has long interested biologists, since the intimate
interplay between host and parasite in terms of controlling moulting and reproductive
systems provides valuable biological insights. Here I will review the morphological
effects induced in hosts, their underlying causes, and the possible evolutionary benefits
to the parasite species. We have a fair understanding of the first and last theme, but the
molecular level details of 'host control' remain largely unexplored, leaving this area
wide open for future research.
Morphological effects
In the Sacculinidae, and probably in most other kentrogonids, endocrine organs,

gonads, and central nervous system (CNS) sustain more or less extensive disturbances
536 J.T. H 0 E G
in morphology whether contacted by roots or not. Moreover, the extent of damage

correlates little if at all with the degree of root infiltration in the particular organ.
Organs infiltrated by roots

In sacculinids, the ventral ganglionic mass (VGM) represents an obligatory and very
early target for the roots (Matsumoto, 1952; Payen et al., 1979, 1981b). In contrast,
infiltration of the brain, the gonads, and the androgen gland is facultative and variable
in extent. Only rarely will roots reach the eye stalks containing the sinus glands and
roots never reach the Y-organs (Iwakura, 1951; Rubiliani & Payen, 1979; Rubiliani et al.,
1980b; Rubiliani-Durozoi et al., 1980).
Most probably other kentrogonids have a pattern of root distribution similar to
sacculinids, but the condition in the Akentrogonida seems more variable. In most
akentrogonids, the roots reach the ventral nerve cord, but it often remains unknown
whether they actually penetrate the neurolemma or whether the roots just follow the
nerves to reach various parts of the body. (Potts 1912,1915; Perrin, 1964; Liitzen, 1981;
H0eg, 1982; Lutzen, 1992; Liitzen & Jespersen, 1992). In chthamalophilids, the roots
never infiltrate the gonads or the nervous system but remain localized around the stalk
and cause only mechanical damage to the host organs (Bocquet-Vedrine, 1961). Other-
wise, we generally lack information on morphological effects induced by akentrogonid
rhizocephalans, except with regard to the gonads.
Endocrine organs and nervous system

Chassard-Bouchaud & Hubert (1975,1976) showed how the Y-organ in sacculinized
Carcinus maenas always regress to a variable degree, sometimes resulting in complete
autolysis of this multi-functional organ (Vernet et al., 1978). The androgen gland first
hypertrophies and then degenerates, and normal function of the sinus gland has
consistently ceased (Veillet & Graf, 1958; Rubiliani & Payen, 1979; Rubiliani et al.,
1980b; Rubiliani-Durozoi et al., 1980). The CNS always sustains extensive lysis of
secretory pericarya, also in areas not penetrated by roots, and in the VGM this occurred
as early as during the first month of controlled, laboratory infestations of C. maenas
(Payen et al., 1981b). Roots penetrating the CNS seem adapted for secretion rather than
absorption and they preferentially infiltrate and damage areas containing neurosecre-
tory cells.
'Parasitic sterilization'
In most Rhizocephala, infestation results in complete sterilization in so far as female
hosts never carry eggs and the gonopores of both sexes can degenerate or disappear
completely (Table 1). 'Parasitic sterilization', rather than the commonly used term
'castration', more accurately describes the state, since the gonads need not necessarily
degenerate completely. Most hosts have smaller gonads than healthy crabs and often
they are also at a rather advanced stage of degeneration, but the morphological effects
vary considerably, sometimes even within the same parasite species (e.g. Shiino, 1931;
George, 1959; Hartnoll, 1967; Rubiliani et al., 1980b; Rubiliani-Durozoi et alv 1980;
Rubiliani, 1983; Sparks, 1985). In sacculinized C. maenas, the gonads, whether pen-
etrated by roots or not, always exhibit inhibitory effects on spermatogenesis and
vitellogenesis (Rubiliani et al., 1980b). In some pagurids infested by rhizocephalans,
histological observations have revealed degeneration of the ovaries, while the testes
look next to normal (Nielsen, 1970). In other pagurids, the rhizocephalan merely arrests
gonad activity (spermatogenesis, vitellogenesis) at the stage reached when infection
took place, in which case some hosts may have gonads with almost mature sperm or
eggs (Shiino, 1931). As an extreme, female hosts of Thompsonia littoralis may ovulate
with a small brood while carrying externae, but they are still effectively sterile since
they loose the eggs within a few days (Lutzen & Jespersen, 1992).
Smith (1906) states that following loss of the externa, the host will normally revert to
a fertile state unless its has sustained considerable morphological modification. This,
however, has relevance only in cases where the parasite is relatively short-lived, such as
in many sacculinids. In the Akentrogonida, the hermaphrodite barnacle hosts of the
Chthamalophilidae can continue to reproduce while parasitized, although probably
with a lower reproductive output due to the considerable space the parasite occupies in
the brood chamber (Bocquet-Vedrine, 1961; Hoeg et al., 1990; Ogawa & Matsuzaki,
1991).
Feminization
Many rhizocephalans not only sterilize, but also feminize male hosts to a variable
degree in terms of morphology, growth pattern and behaviour. Giard (1886,1887) first
observed this interesting phenomenon, which also occurs in bopyrids (Reinhard, 1956;
Baudoin, 1975; O'Brien & van Wyk, 1985). Internally, the testes may sometimes actually
be converted into ovaries (Okada & Miyashita, 1935a,b). Feminization of the external
morphology results from the moults occurring while the rhizocephalan remains inter-
nal (Veillet, 1945). Feminization may affect overall size, relative size of chelae, number
and morphology of pleopods, presence of gonopores, and shape of the abdomen (e.g.,
Brinkmann, 1936; Okada & Okasaka, 1939; Hartnoll, 1967; Nielsen, 1970; Attrill, 1989).
In brachyuran, galatheid, and porcellanid hosts the narrow abdomen of males ap-
proaches the much broader shape seen in females. The pleopods can to various degrees
approach the shape of the biramous ones used in females for egg-bearing, and male-
specific pleopods may disappear entirely while female-specific ones appear.
As with the gonads, the effect on external morphology varies extensively, and the
sensitivity of a host species to a particular parasite plays an important part (Nielsen,
1970; Attrill, 1989). Attrill (1989) also found that the feminizing effect of lernaeodiscids
breaks down when their munidan hosts live at extreme depths. In the Akentrogonida,
only Lutzen (1981) reported a slight feminization (in pleopods of Sylon). Thompsoniids
seem not to feminize and the Chthamalophilidae obviously cannot do so, since they
infest hermaphroditic barnacles.
Degeneration of the androgen gland probably explains the feminization seen in
parasitized males (Veillet & Graf, 1958). However, the damage to the testes may result
538 J.T. H 0 E G
directly from factors released by the roots, since no close correlation exists between
regression of the androgen gland and inhibition of spermatogenesis (Rubiliani et alv
1980a, Rubiliani-Durozoi et al., 1980). Similarly, Nielsen (1970) detected no correlation
between feminization of pleopods and changes in the testes. The occasional presence of
so-called hyperfeminization, where parasitized females have an abnormally broad
abdomen, may indicate that complex factors operate in feminization (Hartnoll, 1967;
Hochberg et al., 1992).
As a logical effect of irreversible androgen gland degeneration, hosts that lose the
externa and commence moulting, generally remain morphological females (Veillet,
1945), although Smith (1906) did note the development of an ovo-testis in a host after
loss of the externa.
Effects on moulting cycle

O'Brien & van Wyk (1985) gave an authoritative review on how many Rhizocephala
influence the moulting cycle of their hosts with diverse effects on both morphology and
size. In sacculinids, the parasite emerges following the moult at which the now steri-
lized brachyuran host would otherwise have attained puberty (allometric moult) after
which event all moulting ceases (parasitic anecdysis). The crab remains at intermoult
stage C4 as long as it carries an externa (Andrieux, 1968) and, unlike healthy crabs, the
natural or experimental loss of appendages will not induce ecdysis (O'Brien & Skinner,
1990). However, some sacculinized hosts may resume moulting after natural or acci-
dental loss of the externa (Veillet, 1945), but not majid crabs, which always enter natural
anecdysis after the moult at puberty (O'Brien, 1984; O'Brien & van Wyk, 1985).
Hosts of non-sacculinid Rhizocephala continue to moult after parasite emergence
(Table 1). The externa avoids falling away at such moults because in the stalk region it
repeatedly interlocks its own cuticle with the newly-forming host cuticle. (Potts, 1906;
Perez, 1931c; Brinkman, 1936; Veillet, 1945; Bocquet-Vedrine, 1961; Heeg, 1982). Porce-
lain crabs hosting externae of Lernaeodiscus porcellanae continue to moult with almost the
same frequency and size increments as in healthy crabs of the same size and sex, and
can readily regenerate lost appendages (unpublished observations). Otherwise we lack
accurate information on moult frequencies in parasitized hosts (O'Brien & van Wyk,
1985).
Colonial species of Peltogasterella and the Thompsoniidae exercise moult control by
preventing ecdysis while the host carries externae. However, the host moults soon after
the loss of one externa generation, heralding the emergence of a new generation (P6rez,
1932; Liitzen & Jespersen, 1992).
A simple scheme would explain the arrested moult cycle seen in sacculinids by a
progressive degeneration of the moult-stimulating Y-organs and an accompanying
decrease in circulating ecdysteroid levels. In agreement, injection of synthetic
ecdysteroids into sacculinized crabs causes them to progress from late intermoult (C4)
to early premoult (DO), although they never pass through ecdysis (Andrieux, 1974), and
the experiment also demonstrates that the integumental receptors remain operative.
Furthermore, Andrieux et al. (1976a,b) maintained that the injection of ecdysteroids
caused the much-disturbed protein-composition in the haemolymph of sacculinized

crabs to change into that seen in healthy ones, but the experimental details do not seem
well controlled. In disagreement with the explanation outlined above, Andrieux et al.
(1981b) found no significant differences when comparing ecdysteroid levels in the Y-
organ, haemolymph or integument between healthy and sacculinized crabs. They
concluded that sacculinized crabs possess the apparatus for both synthesis of ecdysone
and its hydroxylation, and that a deficit in hormonal levels alone cannot adequately
explain the effect seen on the moult cycle. Since that time research along these lines has
ceased.
Effect on host size

Many Rhizocephala affect the size of their host, but the extent and the underlying
causes seem complex and difficult to analyse, especially in the absence of well-control-
led laboratory observations (O'Brien & van Wyk, 1985). Most investigators have relied
on simple field samples to estimate effects (e.g. Bourdon, 1963; Baffoni, 1947, 1949;
Altes, 1965; Samuelson, 1970a,b; Hawkes et al., 1986,1987). O'Brien & van Wyk (1985),
however, emphasized that deviations between size-prevalence curves for parasitized
and healthy crabs can have multiple causes, not all related to effects on the moult cycle,
but also depending on preferential larval settlement, size- or sex-dependent survival,
and synchronization of parasite and host life cycles. Veillet (1945) found, for example,
that sacculinid externae survive better on female crabs than on males due to the latter's
narrower abdomen even when feminized. Moreover, the fact that male crabs become
more or less feminized, also in their growth pattern, means that the size-prevalence
curve for parasitized crabs should appropriately be compared with that for the healthy
female population rather than the whole unparasitized population as is unfortunately
customary (O'Brien & van Wyk, 1985).
An inverse size-prevalence pattern (= parasitized hosts smaller) seems to character-
ize the Sacculinidae (O'Brien & van Wyk, 1985). However, Takahashi & Matsuura
(1994) found that Sacculina senta parasitizing the grapsid Hemigrapsus sanguineus exem-
plifies an exception. The host moults within 40 to 120 days of loss of the externa, but a
new, apparently regenerated externa appears within a few days. So while the host
remains parasitized for an extended period, it can nevertheless grow in size between
each successive externa generation.
In other Rhizocephala, the pattern seems more diverse, and peltogastrids and
lernaeodiscids can either accelerate or decelerate host growth (Brinkman, 1936; Bourdon,
1963; O'Brien & van Wyk, 1985).
The mechanism of host control
As summarized in Figure 5, several lines of evidence demonstrate that rhizocephalan

roots have a double action upon target organs: (i) a direct effect by invasion of the
tissues with roots, such as always occurs in the ventral ganglionic mass and often also in
the gonads; (ii) an indirect effect on the CNS, endocrine organs and gonads by diffusible
540 J.T. H0EG
Androgen Sinus
CNS
gland ^."' '*" gland
t
ROOTS Y-organ
Feminization I
of male hosts
Effect on
Behaviour Gonad host size cycle
Pleopods
Gonopores Parasitic Parasitic
Abdomen sterilization anecdysis
Figure 5. Diagram illustrating the effects induced by rhizocephalan parasites on the physiology,
morphology, and behaviour of their hosts. Thick unbroken arrow, obligatory infiltration by parasite
roots. Thick broken arrow, facultative infiltration by roots. Stippled arrow, effects mediated by
diffusible factors. Thin unbroken arrow, unspecified cause-effect relation. In some cases (gonad,
androgen gland) effects by diffusible factors may apparently operate either directly between parasite
roots and target organ, indirectly via the central nervous system (CNS), or both. See text.
factors (hormones or toxins) without any penetration by the roots (Payen et al, 1979;
Rubiliani & Payen, 1979; Rubiliani et al., 1980a,b; Payen et al., 1981; Rubiliani, 1983).
Since damage to the CNS appears early and usually before contact with roots, the
manipulations of some organs may operate through the neuroendocrine system. In
agreement, the radiotracer studies of Rubiliani & Godette (1981) found that sacculinized
crabs had much reduced levels of both protein synthesis in the CNS and transport of
compounds to the eye stalks compared with healthy animals. However, the testes may
sustain considerable damage before any effect appears in the CNS, so diffusible root
factors may apparently also affect target organs directly (Rubiliani, 1983).
The existence of diffusible substances accords with data on the protein composition
of the haemolymph, for which several studies have demonstrated both qualitative and
quantitative differences between sacculinized and healthy crabs (Andrieux et al., 1976a,b,
1980; Rubiliani & Godette, 1981; Sanviti et al., 1981; Herberts, 1982; Shirley et al., 1985,
1986). Additional important evidence comes from experiments simulating parasitism
by subjecting healthy crabs to implantation of live parasite roots, to injection of extracts
from parasite roots, or to injection of haemocoelic fluid from sacculinized crabs (Rubiliani,
1983, 1985; Rubiliani & Godette, 1981; Rubiliani et al., 1980a). All these treatments
produced functional and structural changes to internal organs, mirroring those found
in naturally infested crabs, and corroborate the existence of diffusible factors emanating
from the roots. Finally Andrieux et al. (1981a) injected haemocoelic extracts from
sacculinized crabs into healthy ones and thereby duplicated both the changed protein
composition in the haemolymph and the arrested moult cycle characterizing the former.
Effects on host metabolism
Most studies on metabolism in hosts parasitized by Rhizocephala are fairly old and
tried either to confirm or to oppose the view that nutritional drain inflicted by the
rhizocephalan causes the parasitic sterilization (e.g. Potts, 1906; Smith, 1911, 1913;
Reinhard & von Brandt, 1944; Lenel, 1954; Rudloff & Veillet, 1954). We therefore need
modern, quantitative studies which compare the nutritional load sustained by parasitized
crabs with the energy normally expended in the crab's own growth and reproduction.
'Egg mimicry' and effects on host behaviour
The rhizocephalan parasite can also profoundly influence the behaviour of the host.
Rasmussen (1959) observed how sacculinized crabs assume the migrational pattern of
ovigerous females, while Hartnoll (1967) and Ritchie & Fteeg (1981) observed how the
externa, in occupying the very same place as the embryos in an ovigerous female,
effectively mimics a brood of eggs. Thus a parasitized host will not damage the externa,
which it could easily do, but instead tends to it with its normal brood-caring behaviour.
Such host care is vital to the parasite, and Ritchie & Ffoeg (1981) witnessed progressive
fouling and eventual death of externae, whose hosts were prevented from grooming
them. At parasite spawning, the host performs its natural spawning behaviour of
flapping the abdomen, which assists the dispersal of parasite larvae. Moreover,
parasitized crabs have a lower threshold to the peptide hormones triggering this
response than healthy, ovigerous females (DeVries et al., 1989).
As an important effect of feminizarion, these behavioral patterns also extend to
parasitized males, which otherwise never exhibit brood-caring behaviour (Ritchie &
Hoeg, 1981). Unfortunately all accounts of behaviour in hosts carrying Rhizocephala
remain more or less anecdotal, since no study employed controlled, ethological experi-
ments.
HOST-PARASITE CO-EVOLUTION
This review has demonstrated a considerable variation in rhizocephalan life cycles
and the extent of effects these parasites induce in their hosts. Therefore it is difficult to
propose generalizations concerning host-parasite co-evolution, especially considering
that we have only just begun to understand the phylogeny of the Rhizocephala (Hoeg &
Liitzen, 1993).
Most rhizocephalans sterilize their host, and some species can reach very high levels
of prevalence, e.g. >95% in populations of commercially important king crabs infested
by Briarosaccus callosus in Japanese waters (Watabe, 1995). We should therefore expect
that there exist strong selection pressures for the evolution of mechanisms to avoid
being infested. No gene selection can exist in sterilized hosts (Baudoin, 1975), and the
study of Ritchie & Hoeg (1981) shows that the host's primary line of defence lies in
preventing the parasite larvae from invading and becoming internal. Indeed Fleischer
et al. (1992) predicted that many hosts other than the porcelain crab studied by Ritchie
542 J.T. H 0 E G
& H0eg (1981) have developed grooming behaviours for this very purpose.
Sterilization of the host enables 'egg mimicry' and frees the energy, which females
otherwise spend in reproduction. Feminization ensures that parasites on males can also
profit from the protection and mechanical support of a broad abdomen and from
'brood-care behaviour'. Where present, these effects are not only advantageous, but
very critical to parasite survival (Ritchie & Hoeg, 1981). The observation that the testes
can remain little affected in some host species shows that sterilization of males follows
from feminization rather than serving an end in itself.
The advantages of manipulating the host's moulting cycle seem more complex.
Parasitic anecdysis undoubtedly represents an apomorphy for the Sacculinidae and
confers an immediate advantage to the parasite: (i) in making energy otherwise spent in
moulting and growth available to the host and thence to the parasite; (ii) in avoiding the
risk of falling off the host during ecdysis, or that the host dies itself during that process,
when it is most vulnerable (O'Brien & van Wyk, 1985). I suggest that the Sacculinidae
have such a short life span (less than one year) that possible adverse effects from
inducing parasitic anecdysis have insufficient time to materialize before the externa
dies naturally. The longer-lived (two to ten years) species of the Lernaeodiscidae and
Peltogastridae allow the host to continue moulting. This ensures that the host will not
suffer from fouling or loss of appendages, so these parasites exemplify a strategy where
a present investment (allowing the host to continue moulting) offers a future advantage
to the individual's survival and reproduction (Baudoin, 1975).
Hartnoll (1967) argued that parasitic castration in the Rhizocephala evolved origi-
nally and only to obtain brood care from the host. However, this can hardly serve as a
general explanation, since parasitic castration also prevails in bopyrid Crustacea and in
many other parasites, not located in brood chambers. In decapods, there exist only two
well-ventilated and well-protected locations for a parasite with external body parts, viz
the gill chambers and beneath the abdomen. Most Rhizocephala occupy the abdominal
position, where they will benefit from brood-care behaviour on the part of the host. The
study of DeVries et al. (1989) indicates that rhizocephalan 'egg mimicry' involves not
just parasitic castration and the mechanical presence of an object under the abdomen,
but also an active biochemical-level participation by the parasite to 'mislead' the host
into believing itself permanently ovigerous. I therefore suggest that parasitic castration
evolved prior to, but also pre-adapted for, the evolution of egg mimicry and feminization
during rhizocephalan phylogeny.
I owe so much to discussions with colleagues on rhizocephalan and cirripede biology that I am
often at pains to trace where and when an idea first surfaced. I am particularly grateful to Prof. J.
Liitzen for many enjoyable hours working together on rhizocephalan biology; to Prof. W.A.
Newman who incessantly requests that ideas be constructed within an evolutionary framework;
to Dr Graham Walker and Dr I. Svane for sound biological insights; and to Dr G.A. Boxshall and
Dr D. Walossek for exercising my ideas on homology and phylogeny. I also thank Dr H. Glenner
and Dr P.G. Jensen for long time co-operation and numerous discussions on evolutionary theory
and practice. Dr N. Bruce, Prof. F.R. Schram and two anonymous referees improved on the final
text with many critical comments. Last but not least, I thank my wife and daughter for support in
all possible and impossible ways.
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The Biology of Rhizocephala

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/. mar. biol. Ass. U.K.

(1995), 75, 517-550 517

THE BIOLOGY AND LIFE CYCLE OF THE

Our knowledge of rhizocephalan biology has increased significantly in the last

Clistosaccidae (2) 2 Caridea

Thompsoniidae (4) 16 Caridea

THE ADULT PARASITE

CYPRID METAMORPHOSIS AND HOST INVASION

GROWTH OF THE INTERNAL PARASITE

THE ROOT SYSTEM

Roofs and multiple externae

EMERGENCE OF THE EXTERNA

THE VIRGIN EXTERNA AND ACQUISITION OF MALES

MATURATION TO THE ADULT

Oviposition and fertilization

Moulting, reproductive cycle and longevity

Size and sex of larvae

Sex ratio in broods

Determination of sex (GSD or ESD)

and the thompsoniids develop through several successive generations of externae

Substratum location and larval success

EVOLUTION OF THE RHIZOCEPHALAN SEXUAL SYSTEM

The advantage of cryptogonochorism

EFFECTS ON THE HOST

In the Sacculinidae, and probably in most other kentrogonids, endocrine organs,

in morphology whether contacted by roots or not. Moreover, the extent of damage

Organs infiltrated by roots

Endocrine organs and nervous system

Effects on moulting cycle

caused the much-disturbed protein-composition in the haemolymph of sacculinized

Effect on host size

The mechanism of host control

As summarized in Figure 5, several lines of evidence demonstrate that rhizocephalan

Effects on host metabolism

'Egg mimicry' and effects on host behaviour

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