Flowers at the front line of invasion?

Authors


Jaboury Ghazoul, Department of Environmental Science and Technology, Imperial College, Silwood Park, Ascot SL5 7PY, U.K. E-mail: j.ghazoul@ic.ac.uk

The spread of alien plants into novel environments is the subject of much discussion and concern among ecologists and conservationists. Alien plants often succeed at the expense of naive native species by direct competition for limiting resources (Callaway & Aschehoug, 2000) or by changing the natural disturbance regime to the detriment of natives (Gentle & Duggin, 1997); however the probability of successful establishment by alien species and their subsequent rate of spread through novel environments are highly variable, and many repeated introductions may be necessary before an alien spreads successfully through a community. It is conceivable that the establishment of aliens may be accelerated by usurping key ecological interactions upon which native species depend. Competition among seeds for suitable germination sites may be a key factor in determining the successful spread of alien invaders (Crawley, 1986) even before competition for resources such as nutrients and light becomes relevant, and seed plant regeneration processes will obviously contribute to this dynamic. Insects are key interactors in seed plant reproductive processes, principally as pollinators, but also as seed and flower predators, seed dispersers, and vectors of plant diseases. At later plant life stages, insects and other invertebrates can structure plant communities through their actions as herbivores of seedlings and saplings (Crawley, 1989). In novel environments, the invertebrate seed predators and herbivores associated with an invading species in its native range may be absent, potentially giving the alien a competitive advantage over native species (Cox & Elmqvist, 2000). On the other hand, aliens may depend on forging new alliances with pollinators and seed dispersers for their success, as their normal mutualists may not occur in the new environment (Simberloff & Von Holle, 1999), and indeed many invasive plants reproduce vegetatively or are self-compatible (Crawley, 1986).

Sympatric plants that share pollinators may compete for those pollinators, often leading to the evolution of temporally staggered nectar production among plant species that minimises competition for pollinator visits (Willmer & Corbet, 1981). Plants that produce relatively large amounts of floral resources or make resources available over prolonged periods may compete successfully for pollinators and, where pollinators limit seed set, such an outcome is likely to have implications for relative seed set among competing species. Many successful alien invaders, such as Ligustrum robustum (Lavergne et al., 1999), Tibouchina herbacea (Almasi, 2000), Lantana camara (Schemske, 1983), and Mimosa pigra (Lonsdale, 1993), have such characteristics of profuse nectar and prolonged flower production. From the perspective of pollination and seed production, usurpation of pollinators by resource-rich alien plants ensures that alien seed production is favoured over that of native plant species. Coupled with the prolonged flowering period of many aliens, promoting a more or less continuous seed rain (and therefore attracting seed dispersers), elevated seed set of aliens together with depressed native seed production may facilitate and accelerate the spread of aliens into new environments. Such a scenario might entail no more than a shift in the foraging behaviour of pollinators, a change that is often overlooked by observers of community change, who tend to focus on the numerical composition of the fauna.

Is there evidence for such shifts in pollinator flower visitation and foraging behaviour, and for consequent effects on seed production of aliens relative to native plants? Recently Chittka and Schurkens (2001) reported that Impatiens grandulifera, an invasive of European river banks, competes successfully with native plants for pollinators, in this case bumble bees, by offering substantially higher floral rewards. Consequently, in the presence of I. grandulifera, seed set of native plants was reduced significantly. Reported here is a similar scenario where the pollination of a native tree is disrupted by changes in the foraging behaviour of butterflies that preferentially visit more visually attractive or economically rewarding alien plants.

Reduction of canopy cover by illegal logging of Shorea siamensis in seasonally dry deciduous forest at Huay Kha Khaeng Wildlife Sanctuary in Thailand facilitated an increase of understorey herbaceous cover, which included the alien invasive Chromolaena odorata Asteraceae (Table 1). In disturbed forest sites, C. odorata flowers were visited preferentially (pers. obs.) by several pierid and papilionid butterfly pollinators of Dipterocarpus obtusifolius, a canopy tree that is not itself harvested and therefore retains its natural population density. Consequently, butterfly pollinator visits to D. obtusifolius flowers, pollination of these flowers, and the quality of deposited pollen all declined at disturbed sites (Table 2), even though the abundance of butterfly pollinators remained unchanged (Ghazoul, 2002).

Table 1.  Understorey ground cover of flowering herbaceous plants at disturbed, moderately disturbed, and undisturbed sites in dry deciduous forest in Thailand. Disturbance was logging of Shorea siamensis trees. Percentage ground covered by flowering C. odorata was estimated visually at 6 m radius plots at three positions along 20 widely spaced and independent transects. Values are presented as mean ± SE (median). Kruskal–Wallis ( H -statistic) or anova tests were applied to arcsin-transformed data as appropriate.

Site
Tree density (per 0.25ha)
(mean ± SE)
Understorey cover (%)
[mean ± SE (median)]
C. odorata (% cover)
[mean ± SE (median)]
Undisturbed117±812.3±0.6 (12.3)0.08±0.08 (0)
Moderately disturbed101±1012.3±1.8 (10.3)0.33±0.26 (0)
Disturbed73±842.4±4.8 (43.5)30.8±2.8 (30)
StatisticF2 =6.4 H(2) =25.657 H(2) =161.5
P -value P =0.003 P <0.001 P <0.001
Table 2.  Activity of butterfly pollinators, and conspecific and interspecific pollen deposition at D. obtusifolius trees at sites differing in S. siamensis logging intensity. Pollinator activity was recorded as mean number of butterfly pollinators in D. obtusifolius canopies during 1 min observations at 15 min intervals for a 3 h period at each tree. The proportion of pollinated flowers on each tree was determined by examining pollen deposition on 30 randomly selected flowers exposed to a single day of pollinator activity. Flowers pollinated with both conspecific and interspecific pollen are included in both categories. Trees included in the analysis numbered 37 at undisturbed sites, 29 at moderately disturbed sites, and 22 at disturbed sites. Values are presented as mean ± SE (median). Kruskal–Wallis ( H -statistic) or anova tests were applied to arcsin-transformed data as appropriate.

Site
Butterfly pollinator
activity at D. obtusifolius
Flowers receiving
conspecific pollen (%)
Flowers receiving inter-
specific pollen (%)
Undisturbed0.86±0.11 (0.52)74.6±2.0 (76.7)4.9±1.0 (3.3)
Moderately disturbed0.70±0.16 (0.43)68.3±2.4 (70.0)7.9±1.0 (6.7)
Disturbed0.10±0.03 (0.07)52.3±2.4 (51.7)18.5±1.5 (18.3)
StatisticH(2) =30.1 F(2,85) =22.0 F(2,85) =35.3
P -value P <0.001 P <0.001 P <0.001

The interaction between anthropogenic disturbance, exotic species, and native plant pollination and seed production could be extremely relevant to the spread of invasives and native tree regeneration. As flowering plants often compete interspecifically for pollinator visits (Stone et al., 1998; Chittka & Schurkens, 2001), changes in the behaviour of pollinators brought about by alien invasives may reduce both the quantity of pollen received by native plants and its quality by transfer of non-compatible pollen, potentially leading to reduced seed and fruit set. Pollination success is a function of pollinator flower constancy, which is affected by floral density (Levin & Anderson, 1970). Declining floral constancy associated with increased relative abundance of a floral competitor has the dual impact of reducing both visitation frequency and pollination success per pollinator visit, as observed for D. obtusifolius. By reducing the fitness of neighbouring plants, exotics may facilitate their own spread, particularly at the front line of alien invasion where native and alien propagules compete for germination sites. As such, competition for seed dispersal agents may be just as important as competition for pollinators. Native species may escape such competition by temporal segregation of flowering and fruiting phenologies, but some invasives [e.g. Lantana camara (Gentle & Duggin, 1997) and Mimosa pigra (Lonsdale, 1993)] produce abundant flowers and fruit almost continuously and may compete with a wide variety of native plants regardless of their phenologies.

Dipterocarpus obtusifolius fruit set is resource limited ( Ghazoul, 1997 ) and was, consequently, similar across disturbance regimes. Additionally, there was compensation for the decline in butterfly pollinator activity by alternative pollinating agents (birds and moths) ( Ghazoul, 1997 ). Thus pollinator-limited native plants that share pollinators with invasives may be buffered from potential competition by attracting a diversity of pollinating agents ( Bond, 1994 ). Characteristics likely to increase susceptibility to novel competition for pollinators and seed dispersers include a limited suite of biotic pollinators and seed dispersers, low pollinator constancy, shared and restricted flowering and fruiting phenologies, few floral rewards, relatively low flower and seed production, and pollinator-limited seed set. Such traits are common to many plants in seasonal tropical forests ( Levin & Anderson, 1970 ; Bawa, 1990 ) where logging and road building are facilitating the spread of invasives, with often disastrous results.

Thus the spread of invasive plant species into novel environments may result in changes to the spatial distribution of floral resources and, consequently, the foraging behaviour of native pollinators and seed dispersers. This largely unrecognised threat may actually be more relevant to the interacting dynamics of alien and native plant populations than possible changes in pollinator populations or composition. Indeed, it seems that insect pollinators (and seed dispersers) are mostly generalist in their resource preferences (Waser et al., 1996) and may not be affected numerically by changes in plant species composition. Extinctions or reductions in pollinator fauna following species introductions have been shown previously (Cox & Elmqvist, 2000) but only on isolated oceanic islands with depauperate and specialised communities. A key question for entomologists is to determine not only how generalist insect pollinators and seed dispersers (notably ants and dung beetles) are, but also how generalist insect seed predators are. If seed predators are highly species specific, alien plants might gain the double advantage of appropriating pollinators at the expense of natives while escaping from density-dependent seed predation that might otherwise favour the less productive natives and ameliorate the alien competitive advantage.

The threat to global biodiversity from the spread of plant invasives is all too apparent, and in at least two cases (Chittka & Schurkens, 2001; this paper), this spread appears to be facilitated by changes in the foraging behaviour of insect pollinators. It remains to be seen how widespread this phenomenon is, but the emphasis among pollination biologists on declines and extinction of pollinators following the spread of alien species (e.g. Cox & Elmqvist, 2000) may actually have little relevance to the processes leading to the initial establishment and spread of invasives with which native pollinators may be intimately involved. In failing to recognise and document changes in the behaviour of insect pollinators among flowering plant communities, early steps in the establishment of invasive plant pests may be missed.

Acknowledgements

Mick Crawley and Claire de Mazencourt commented on an earlier draft of this manuscript. Andy Macgregor and Katharine Liston contributed to fieldwork in Thailand. Mr Chatchawan Pisdamkham, Mr Preecha and the staff of Huay Kha Khaeng Wildlife Sanctuary gave permission and support throughout the fieldwork period. This paper describes research from a CIFOR project ‘In situ conservation of plant genetic resources’ in Thailand in collaboration with Dr Chaweewan Hutacharern of the Royal Forest Department in Thailand and funded by the Department for International Development U.K. (DFID). Permission to conduct research in Thailand was granted by the National Research Council of Thailand.

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