38 R
.E. Thresher et al. J. Exp. Mar. Biol. Ecol. 254 2000 37 –51
1. Introduction
Non-indigenous marine species threaten both marine industries and biodiversity. Information on the numbers, diversity and impacts of exotic marine species is still sparse
Ruiz et al., 1999, but for a number of high profile ‘pests’ the impacts are so obvious that efforts are underway to reduce both the frequency of new introductions Committee
on Ships’ Ballast Water, 1996 and the impacts of existing pest populations. Examples of these high profile species include the Atlantic ctenophore, Mnemiopsis leideyi, intro-
duced into the Black Sea and implicated in the decline in regional fisheries Shiganova, 1998, the European seagrass, Spartina anglica, which is overgrowing mud flat
communities along the coasts of North America, New Zealand and Australia, and the European shore crab, Carcinus maenas. C
. maenas is an exceptionally successful emigrant, with established invasive populations in Australia, Japan, South Africa and
North America Cohen et al., 1995; Grosholz and Ruiz, 1995. The collapse of shellfish fisheries on the American east coast has been attributed to predation by C
. maenas Smith et al., 1955. Ecological studies of C
. maenas in North America and Australia Grosholz and Ruiz, 1996; papers in Thresher, 1997 indicate that it is a highly
competitive generalist predator capable of radically altering the composition and dynamics of invaded assemblages Grosholz et al., 2000.
Options for dealing with introduced marine pests parallel those for dealing with terrestrial pests. These range from physical removal Walton, 1997 through to a variety
of possible biological treatments and to environmental rehabilitation the last based on the assumption that invasive species primarily affect degraded habitats. Environmental
rehabilitation as a control strategy is an unlikely option for C . maenas, which has
established dense populations in largely unaltered habitats though see Janzen, 1998. The large numbers of the crabs and their high fecundity suggest that physical removal
will also have only a minor effect on their impacts. These and other options available to deal with C
. maenas were reviewed at an international workshop on managing the species Thresher, 1997, which suggested two options that were likely to be effective.
The first is a large-scale program of physical removal, possibly in the form of a subsidised fishery, which might reduce impacts temporarily or in small areas. The
second was biological control.
Classical biological control involves the introduction of a predator, parasite or pathogen to reduce the impacts of the invasive species. The approach has a long history
and mixed success rate for terrestrial pests Van Driesche and Bellows, 1996. Success depends largely on the effectiveness of the control agent and its safety. The latter largely
equates to issues of specificity: a ‘safe’ biological control agent is one that attacks only the target species. Detailed protocols for assessing the specificity of biological control
agents against terrestrial pests have been developed see Kaufman and Nechol, 1992. These protocols could be applied with minor modification to marine biological control
agents Kuris, 1997.
The participants in the workshop on managing C . maenas identified several potential
biological control agents, ranging from heteroflagellate diseases Goggin, 1997 to metazoan parasitic castrators Lafferty and Kuris, 1996. Of these, the most probable
appeared to be the rhizocephalan barnacle, S . carcini.
R .E. Thresher et al. J. Exp. Mar. Biol. Ecol. 254 2000 37 –51
39
S . carcini is a common and well-studied parasite of C. maenas in the crab’s native
¨ range Høeg and Lutzen, 1995. The life cycle of the parasite involves a mature female,
which is situated in the abdominal brood chamber of the host, is fertilized by one or two cryptic dwarf males and which subsequently releases a series of broods of nauplii. The
nauplii develop lecithotrophically, metamorphose into cypris larvae after about 5–6 days and become competent to settle after another 3–4 days in the plankton. Female cyprids
settle on the exoskeleton of a host crab at the base of a plumose seta Delage, 1884 and metamorphose into a special stage known as the kentrogon. The kentrogon penetrates the
exoskeleton of the crab with a hollow stylet and injects the primordial parasite into the
¨ hemocoelic fluid. After an internal phase of a few months to 3 years Lutzen, 1984, the
parasite produces an external virginal reproductive body externa situated under the abdomen of the host. The externa attracts male cyprids, which implant as dwarf males
Høeg, 1987, remain with the female externa for the duration of the latter’s lifetime and fertilize all its broods. Externae failing to receive at least one male cannot mature and
eventually perish.
S . carcini has severe and lasting effects on the growth, morphology, physiology, and
behavior of the host crab. It arrests the moult cycle of the host, which therefore suffers increased fouling. More importantly, the parasite castrates both male and female crabs
and feminises the males. The behavior of both sexes is altered such that both respond to the externa and parasite’s eggs as their own eggs. In effect, the sacculinized host
becomes a parasite genotype with a crab phenotype.
These features suggest S . carcini could be a useful biological control agent against C.
maenas Lafferty and Kuris, 1996. The key issue, however, is the degree of host specifi- city. Host specificity in rhizocephalans is highly variable. Many attack only one or a few
closely related host species, whereas others appear to be less host specific Høeg and ¨
Lutzen, 1995. S . carcini appears to be in the latter group. In Europe, it occurs not only on
C . maenas, but also on C. aestuarii, Liocarcinus depurator and some other Portunidae
Høeg, 1995 and is even known from Perimela denticulata Perimelidae. Recent genetic work Murphy and Goggin, 2000 appears to refute the hypothesis that S
. carcini is a com- plex of cryptic species, each showing a high degree of host specificity Høeg, 1995.
We undertook a series of experiments to assess the host specificity of the parasite when exposed to potential non-native hosts. These experiments address three issues.
First, since there are few experimental tests of host specificity in rhizocephalans and ¨
none on the genus Sacculina Høeg and Lutzen, 1995, the current study provides direct information on host specificity. For comparative purposes, we also undertook a brief set
of experiments using a native Australian sacculinid, Heterosaccus lunatus, tested against its native host, Charybdis callianassa Stephenson et al., 1957 and the introduced C
. maenas, to assess possible generalities in patterns of and mechanisms underlying host
specificity. Second, we exposed specimens of several species of Australian crabs to S .
carcini, to determine the likelihood that these non-native hosts would be acceptable to it. These results bear on the safety of using the parasite as a control agent against the
introduced population of C . maenas in Australia. Third, our study is the first attempt to
use protocols derived from terrestrial pest control programs to assess the specificity of a possible biological control agent in the marine environment. The trials, therefore, could
indicate some of the problems associated with undertaking such tests.
40 R
.E. Thresher et al. J. Exp. Mar. Biol. Ecol. 254 2000 37 –51
2. General materials and methods
