Nature: Parasites Lost

news and views Parasites lost Keith Clay

Why do some plants and animals become pests when they are introduced to new areas? Part of the answer seems to be that they have left most of their parasites behind, gaining vigour as a consequence.

nvasive species can be a real bother. These are plants or animals that, when they are ab c Iaccidentally or deliberately moved from one region to another, flourish to the extent of getting out of hand and becoming pests BOTANICAL RY/AA-Z in their naturalized environment. They tend to reduce biodiversity, and can have adverse effects on human well-being1,2. Much effort is devoted to controlling them after they are established, but a better understanding of why species become invasive offers the possi- bility of taking pre-emptive measures. de f In companion papers on pages 625 and 628 of this issue, Mitchell and Power3 and Torchin et al.4 illuminate the biology of invasiveness. They report the results of surveying parasite loads of invasive plants and animals in their naturalized and native ranges. They find that parasitism is significantly reduced in organisms in the introduced range, so supporting the ‘enemy release hypothesis’ — the idea that species are more likely to Figure 1 Invasive species in the United States. a, b, Two species that have caused widespread ecological become invasive when they are released from damage to native communities are the nutria, or coypu (Myocastor coypus), and purple loosestrife control by their natural enemies. (Lythrum salicaria). c, d, Other species such as the Asian rice eel (Monopterus albus) and mile-a- This hypothesis is one of several (not minute weed (Polygonum perfoliatum) are limited in their distribution but threaten to become mutually exclusive) explanations put for- severe problems as they expand into areas to which they are well adapted. e, f, Examples of a ward to account for why some species worrisome group of species that could prove serious pests should they arrive are the brown increase uncontrollably when introduced tree snake (Boiga irregularis), which decimated bird life on Guam following its introduction into new areas. In The Ecology of Invasions by from Indonesia but has not yet successfully invaded Hawaii, and witchweed (Striga spp.), which in Animals and Plants5, Charles Elton favoured parts of Africa has a highly adverse effect on cereal yields. a more general form of this hypothesis, the ‘ecological resistance hypothesis’, which for continental habitats where species diver- were more likely to be released from control proposes that competition with native sity is high and all ecological niches seem by fungal pathogens than by viruses. species and attack by native predators and to be taken, yet where invasive species are Mitchell and Power also quantified the (A) L. RICHARDSON/CORBIS; (B) E. CRICHTON/CORBIS; (C) MOLLUSCAN PICTURES; (D) M. C. PERRY/USGS; (E) RONENZILBERMAN/AP; (F) J. F (F) J. (E) RONENZILBERMAN/AP; (D) M. C. PERRY/USGS; PICTURES; (C) MOLLUSCAN (A) L. RICHARDSON/CORBIS; (B) E. CRICHTON/CORBIS; pathogens keep invaders in check6,7. Island numerous. A good example is the eastern characteristics of each plant species from the systems such as those of Hawaii or Australia United States, where nutria, an aquatic frequency of reports naming that species as may be particularly prone to invasion, for rodent, and purple loosestrife, a wetland noxious (defined as a weed that poses a high several reasons — their lower species diver- plant, are just two of many introduced risk to agriculture) or an invader of natural sity and population density; the absence species that have had or could have adverse areas. Species that ranked higher on the of particular groups (placental mammals effects (Fig. 1). Mitchell and Power3 and scales of noxiousness and invasiveness in Australia, for instance, and snakes in Torchin and colleagues4 provide a more showed greater release from their parasites. Hawaii); and the lack of coevolutionary his- mechanistic explanation of why these The authors found that invasive plant species tory with invaders, in which host and para- species are problematic. do accumulate parasites from their natural- site have had a long time to coadapt to each Both groups compiled published infor- ized range, but the overall parasite load other and have reached a stable state8. This mation on parasitism of invasive species in tended to be less than in their original home. lack of coadaptation is dramatically illustrat- their native and their naturalized ranges. Finally, they also found that invasive plant ed by the lack of resistance of native species Mitchell and Power3 quantified the number species with higher rates of pathogen accu- to introduced pathogens. More generally, of fungal pathogens and viruses infecting mulation were less likely to be noxious, an communities with high diversity may be 473 plant species that are native to Europe observation that again supports the ecologi- more resistant to invasions9. but have become naturalized and invasive cal resistance hypothesis. This provides a The ecological resistance hypothesis in the United States. They found that these ray of hope: if invasive species accumulate suggests why certain habitats might be more species were infected on average by 77% parasites in their naturalized range relatively or less prone to invasion, but does not fewer fungal and viral species in the United rapidly10, the problems they cause may be predict why certain species are more or less States than in Europe, strongly supporting temporary. likely to invade that habitat. In particular, the enemy release hypothesis. Interestingly, Torchin and colleagues4 examined 26 this hypothesis cannot provide explanations in their naturalized range, invasive plants invasive animal species ranging from mol-

for parasites with complex life cycles, their Box 1 Tansy ragwort: a case history alternative hosts must also accompany the primary host into the new range, requiring The tansy ragwort (Senecio the cinnabar moth (Tyria migration of three or more species. jacobaea, pictured) is native jacobaeae) from France and the The new results3,4 lend support to the idea to Eurasia but has been ragwort flea beetle (Longitarsus that invasive species can be controlled by introduced into North and South jacobaeae) from Italy. Cinnabar speeding up their accumulation of parasites. America and the Australian caterpillars feed on developing They may be less helpful for predicting region. In the western United ragwort inflorescences and which plant and animal species will prove NIALL BENVIE/CORBIS States it aggressively invaded leaves, and can totally strip a invasive in the future11. But we can be sure range lands, where it displaced plant of foliage; flea beetles that biological invasions will continue and species of forage plant and chew holes in the leaves. that the actions of humans, the most success- poisoned livestock with its The decline of ragwort ful invasive species of all, will remain their pyrrolizidine alkaloids. In 1976, populations clearly followed primary contributor. ■ aerial photography showed that the establishment of these Keith Clay is in the Department of Biology, Indiana the species covered more than natural enemies from the University, Bloomington, Indiana 47405, USA. 12,000 km2 in western Oregon. ragwort’s native range, and e-mail: [email protected] But by 1988 the area infested ragwort density has since 1. Pimentel, D. (ed.) Biological Invasions: Economic and had been reduced by 60–90% remained low12. The same Environmental Costs of Alien Plant, Animal and Microbe Species and more desirable vegetation group has experimentally (CRC Press, Boca Raton, 2002). 12 2. Westbrooks, R. G. Invasive Plants: Changing the Landscape of was recovering, a change confirmed that the America (Federal Interagency Committee for the Management that can be attributed to introduction of the natural was indeed responsible for of Noxious and Exotic Weeds, Washington DC, 1998). the deliberate introduction of enemies from its home range controlling the ragwort. K.C. 3. Mitchell, C. E. & Power, A. G. Nature 421, 625–627 (2003). 4. Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J. & Kuris, A. M. Nature 421, 628–630 (2003). 5. Elton, C. The Ecology of Invasions by Animals and Plants luscs such as the common periwinkle, Litto- the biocontrol agent finds native species to (Univ. Chicago Press, 2000; orig. edn Methuen, 1958). rina littorea, to the black rat, Rattus rattus. be equally, or more, attractive. 6. Maron, J. L. & Vila, M. Oikos 95, 361–373 (2001). Like most of the cases examined, these Why are parasites and pathogens often 7. Keane, R. M. & Crawley, M. J. Trends Ecol. Evol. 17, 164–170 (2002). species are native to the Old World but have left behind when their hosts migrate? There 8. Carlquist, S. Island Biology (Columbia Univ. Press, New York, been introduced to the New World. In addi- may be several reasons. The colonization of 1974). tion to quantifying the number of parasite new habitats is often by just a handful of indi- 9. Tilman, D. Ecology 74, 2179–2191 (1993). species hosted, the authors also analysed viduals, increasing the likelihood that all are 10.Strong, D. R. & Levin, D. A. Proc. Natl Acad. Sci. USA 72, parasite prevalence (the percentage of free of infection. In addition, if parasite dis- 2116–2119 (1975). 11.Ehrlich, P. R. in Biological Invasions: A Global Perspective individuals infected within a population) in persal occurs independently of the host, two (eds Drake, J. A. et al.) 315–328 (Wiley, London, 1989). the native and naturalized ranges. The para- successful migrations are required. Similarly, 12.McEvoy, P. & Cook, C. Ecol. Appl. 1, 430–442 (1991). sites documented were exclusively helminths — flatworms or roundworms. There is a rich database on parasitic helminths, reflect- Applied physics ing their great diversity and their ecological significance. Torchin and colleagues’ results are simi- Solar cells to dye for lar to those of Mitchell and Power, in that an Michael Grätzel average of 16 parasite species per host species occurred in the native range compared to The idea of producing electricity from sunlight is attractive, but in practice seven in the naturalized range. On average, the technology to do so is expensive. A new device, moving away from the only three of the native parasites accompa- traditional silicon design, shows promise. nied the host to the naturalized range. Hosts were also infected by four parasite species hotovoltaic conversion of solar energy and it must then conduct these carriers to from the new environment, again showing — from photons to electrons — has the current collectors. To achieve all this that introduced species accumulate new Pso far been dominated by solid-state simultaneously, materials of very high parasites. But overall parasite prevalence was devices, usually made of silicon and profiting purity are needed, and consequently silicon- much lower in the host species’ naturalized from the expertise of the semiconductor based solar cells are too costly to compete range. industry. That dominance is now being chal- with conventional means of producing Taken together, these studies3,4 constitute lenged by new generations of photovoltaic electric power. further evidence for the enemy release cells. On page 616 of this issue, McFarland In contrast, the device developed by hypothesis. Invasive species appear to suffer and Tang1 present an intriguing embodi- McFarland and Tang1 has a multilayer struc- from fewer parasites and pathogens in their ment of a converter that is based on light har- ture that physically separates the processes of naturalized range than in their native range; vesting by dye molecules on a metal surface. light absorption and charge-carrier trans- so, presumably, they are more poorly regu- Contrary to expectation, their device shows port (Fig. 1). Photons are harvested by dye lated by parasites in their new environment. a strikingly high internal quantum efficiency molecules adsorbed on the surface of a thin This provides conceptual support for one for electric-current generation. gold film, which in turn rests on a layer of approach to biological control of such The silicon used in most of today’s solar titanium dioxide (TiO2). Spontaneous elec- species, in which parasitic organisms from cells must fulfil several tasks. It must absorb tron flow from the semiconducting TiO2 plants or animals in native habitats are iden- sunlight, converting photons into negative- layer to the metallic gold layer imparts a tified and introduced into the naturalized and positive-charge carriers (electrons and slight negative charge to the gold, leaving a environment (see Box 1). This strategy can, holes, respectively); it must transmit an elec- slight positive charge on the TiO2. The result- however, prove a double-edged sword when tric field to separate the electrons and holes; ing local electrostatic field creates a potential