Defenders of the peace: New Zealand's marine parasites versus exotic crabs?

By Annette Brockerhoff, Postdoctoral Research Fellow, School of Biological Sciences, University of Canterbury, Colin McLay, Associate Professor, School of Biological Sciences, University of Canterbury, Daniel Kluza, Senior Adviser, Risk Analysis (Marine), Biosecurity New Zealand

In recent years, several species of exotic crabs have arrived in New Zealand seas. In 2000, a Japanese paddle crab (Charybdis japonica) was found in Auckland Harbour, and in 2002/2003 two exotic rock crabs (Romaleon gibbosulus and Glebocarcinus amphioetus, formerly in the genus Cancer) were found in the Harbours of Lyttelton, Timaru, Wellington, Bluff and Gisborne. Increasing ship traffic in New Zealand waters has probably been the source of these new arrivals, and more can be expected in the future.

Some exotic crab species have been extremely successful in establishing invasive populations in many places across the world, and are known to have detrimental effects on local biodiversity and marine industries. For example, the European shore crab (Carcinus maenas) is now established in Australia, Japan, South Africa and North America. This crab is a highly competitive generalist predator which can dramatically alter species composition and dynamics in the invaded habitat (Grosholz et al 2000), and it has contributed to the collapse of shellfish fisheries on the American east coast (Smith et al 1955). In contrast, other crab species have become established outside of their native range but are not currently invasive, such as the New Zealand pie crust crab (Metacarcinus novaezelandiae) in South Australia and Tasmania.

Good news and bad for invasive species

One hypothesis of why invasive species are so successful is that they typically leave their natural enemies behind. In its native range, a species is kept in check by predators, parasites and diseases; when introduced to an environment without these natural enemies, a species can survive and reproduce more successfully (the ‘enemy release hypothesis’; Keane and Crawley 2002).

Counteracting this is the ‘biotic resistance’ a species will meet when introduced to a new location: exotic species may be poorly adapted for coping with native predators, parasites and diseases (Parker and Hay 2005). In theory, this means that the more diverse a new habitat is, the more likely one of the native species will either prey on or infect the exotic species. For example, predation by the North American native blue crab (Callinectes sapidus) appears to limit the southern distribution of the invasive European shore crab (DeRivera et al 2005).


Yellow sac on the underside of the crab
is the rhizocephalan parasite.

Against the backdrop of ‘enemy release’ and ‘biotic resistance’ hypotheses, we are currently investigating whether native New Zealand marine predators or parasites could potentially limit the abundance and distribution of introduced crabs. The New Zealand marine fauna has few reported parasites that could attack exotic crabs and thereby defend our shores. Elsewhere in the world, a variety of parasites have a strong impact on crustacean populations (e.g. Rohde 2005).

Two recent discoveries in native crabs – a castrating parasite (a barnacle) and an egg predator (a ribbon worm) – suggest that New Zealand’s coastal waters may have some natural defences against exotic crabs.

In May 2006 we re-discovered a rhizocephalan (a parasitic barnacle) in the common New Zealand endemic pie crust crab (see photos) in Wellington Harbour. This barnacle is most likely a New Zealand endemic species new to science, which has been previously overlooked (except Bennett 1964).

Bizarre life cycle

Rhizocephalans are fascinating animals that have evolved an elaborate parasitic life cycle. By appearance, adult rhizocephalans aren’t much more than blobs of tissue – they have no limbs, no body segments, and few internal organs. We know these animals are crustaceans only because rhizocephalan larvae are very similar to those of rock barnacles. Rhizocephalan larvae are free-swimming, and females attach and insert themselves to a crab. The female grows a root-like system into the crab’s body, drawing nutrients from the host, and then produces an egg sac under the crab’s abdomen.

Male rhizocephalans are also parasitic, but there’s a twist: their hosts are female rhizocephalans. After being part of the zooplankton for a few days, a male larva will settle on a female’s sac and moult into a mature adult; unlike females, mature males are dwarfs and remain larval-sized for life. The adult male enters the egg sac, attaches himself to the chamber, and starts fertilising the eggs within. The male will spend the rest of his life attached to the female, deriving nutrients from her and fertilising eggs.

Hosts castrated

It gets even more bizarre when we look at the impact of a rhizocephalan on a male crab. Female crabs have wide abdomens, an adaptation for carrying their fertilised eggs on their underside, whereas male crabs have much narrower abdomens. Regardless of the host’s sex, a rhizocephalan will produce an egg sac on the crab’s abdomen. In female crabs, the rhizocephalan egg sac is produced in exactly the same place where the host usually carries its eggs, and the crab will care for the parasite’s eggs as if they were its own. For rhizocephalans, parasitising male crabs pose two key challenges: their abdomens are too narrow for egg sacs, and males don’t tend egg masses. To get around this problem, rhizocephalans feminise male crabs by making their abdomens grow much wider, and inducing egg care behaviour. Practically all infected crabs become castrated during parasitisation, effectively eliminating them from the reproductive population; rhizocephalans therefore have the potential to influence host population dynamics.

In North America, the European rhizocephalan Sacculina carcini is being investigated for its potential as a biological control agent for the highly invasive European shore crab (Goddard et al 2005). In addition, European shore crabs may also encounter biotic resistance in new locations from local rhizocephalans.

South Pacific rhizocephalans have received almost no scientific attention; of the approximately 250 species worldwide (Høeg et al 2005), less than a tenth are known from Australasia. There are only four records of rhizocephalans in New Zealand, and none of these have been identified to species (Bennett 1964; Mc Laughlin and Gunn 1992).

Ribbon worm discovery

A second new discovery is a ribbon worm (genus Carcinonemertes) found on red rock crabs (Plagusia chabrus; Grapsidae) (see photos) in the North and South Islands. There are currently 12 recognised species of Carcinonemertes worldwide, and these worms are egg predators of crabs. The worm’s intriguing life cycle typically includes a larval resting stage that hides under the abdomen of the crab. When a female crab lays eggs and attaches them under her abdomen, the worms come out to feed, mature, mate and reproduce on the eggs; as a result, a female crab may lose up to 100 percent of her brood.

Members of the genus Carcinonemertes have the potential for large scale ecological and economic impact. In North America, for example, widespread outbreaks of C. errans and C. regicides in the 1970s and 1980s led to extensive reproductive failure in Dungeness (Cancer magister) and red king crabs (Paralithodes camtschaticus), and caused significant damage to these fisheries (Jensen & Sadeghian 2005). With respect to biotic resistance, the North American ribbon worm Carcinonemertes epialti has been shown to cause significant brood mortality on the exotic European shore crab, demonstrating the potential for population-level impacts on non-native crabs (Torchin et al. 1996).

Parasite and predator may help foil exotic crabs

The discoveries of a new rhizocephalan parasite and a nemertean egg predator are important for our understanding of the population dynamics of native and exotic New Zealand crabs. For example, the localised occurrence of these new species indicates that some crab populations are fairly isolated. Moreover, these newfound species might play an important role in the biotic resistance of New Zealand’s marine environment by lowering densities of exotic crabs.

References:

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Page last updated: 30 April 2008