Chapter 24
EXOTIC PLANT INVASIONS IN TROPICAL FORESTS: PATTERNS AND HYPOTHESES
Julie S. Denslow and Saara J. DeWalt
OVERVIEW lie tropics, exotic plants have been widely introduced for industrial timber. for land reclamation and lorage crops. and In I as orriamentals. In spite of the apparent opportunity for naturalization and spread. invasive exotic plants are scarce in many continental tropical Forests. We examine several conditions under which exotic species do pose substantial threats to tropical ecosystems or to their maniigcment. These include island ecosystems. open-canopied thrests,fragincnted or disturbed ecosystems and forests managed for timber or crops. We explore four h ypotheses to account for the scarcity exotic species because they of exotic species in manY tropical forests: (1) tropical forests are resistant to invasions b y are rich in species and functional groups: (2) native rainborest species competitively exclude exotic species: (3) high pest loads and high pest diversit y in the tropics deter establishment and spread of exotic species: and (4) low propagule availability contributes to the rarity of exotic species in many tropical forests. While current research suggests that high species diversity per se is not likely to be sin impediment to exotic species. Functional group diversity, high competitive exclusion rates, and high pest loads all may confer a certain biotic resistance to the establishment and spread of exotic species in tropical forests. Similarly, high junctional diversity and high productivity may increase the resilience of tropical forests to the kinds of ecosystem changes etkcled by invasive species in other ecosystems. y evaluate these hypotheses and their interactions in the absence oh a better assessment However, we are unable to full Its from seed addition expermnients to test the or the actual exposure of tropical forests to exotic propigules and results relative importance of biotic resistance and dispersal limitation in limiting the spread of exotic species into tropical Forests.
INTRODUCTION were reported only from treefall gaps. Similarly. exotic species constitute small percentages of the Tropical forests face myriad threats from human floras ol two tropical held stations. La Selva Bio- activities. including land conversion and habitat logical Station in Costa Rica (7.6%) and Burro fragnscntation. altered fire cycles, and defauna- Colorado Island in Panailia (2 1i0, where exotic species are confined to pastures, clearings, or other lion (Sala et iii. 2000). With some exceptions. however, few continental tropical forests appear highly disturbed sites (Foster and Hubbell 1990. Hammel 1991)). A global survey of threats to to he affected strongly by invasive exotic plants hiodiversity suggests that biotic exchange is sec- (e.g.. Rarnakrishnati 1991. Whitmore 1991, RejmItnek 1996. Pine 2002). Rejmsmnek (1996) ondary to other factors such as land-use change for tropical forests as it is for most forest ecosys- found only 42 exotic plant species known to invade tropical rainforests: of those, about half were tems (Sala et id. 2000). The apparently low impact Of exotic species on tropical forest ecosystems known to invade forests onl y on islands and eight 1 410 Julie S. Denslow and Saara J DeWalt
could reflect biotic resistance (Mack 1996) to processes. Propagule pressure, resource availabil- exotic invaders and/or historically low exposure to ity, and pressure from natural enemies all influ- propagules from exotic species (Fine 2002). Both ence the probability that an exotic species will biotic resistance (in the form of impact from com- establish a reproducing population and the rate petitors, predators, and pathogens) and propagule of growth of that population. Habitat fragmen- availability (via reproductive output, vegetative tation increases exposure of forests to propagule spread, and dispersal) are important components pressure from exotic species in nearby disturbed or of plant community composition (e.g., Turnbull managed ecosystems. Available resources, such as et al. 2000) and have figured in rates of biotic light and space, also are increased by disturbance change throughout evolutionary time. Of inter- and habitat fragmentation and decreased when est here is their role in the spread and impacts pre-empted by native species via competition. of exotic invasive species in tropical forest ecosys- Rates of competitive exclusion are thought to be tems. In this chapter we examine patterns of exotic highest where primary productivity and growth plant invasions in tropical and subtropical forests rates are high (e.g., Rosenzweig and Abramsky and explore four hypotheses proposed to account 1993). Similarly, high species and functional for these patterns. group richness is thought to reduce resources Our perception of the vulnerability of an ecosys- available to newly establishing exotic species. tem to invasive species has at least two com- The complexity of the invasion process and ponents (D Antonio and Dudley 1995): (1) the scarcity of appropriate data preclude evaluation ease with which exotic species are able to estab- of the relative importance of the many factors lish and spread, and (2) the tendency for exotic affecting the impact of exotic species on tropi- species to alter ecosystem and community pro- cal forests. Many of the processes illustrated in cesses. Here we will use the term ecosystem Figure 24.1 are interdependent and most stud- resistance" to describe the degree to which com- ies focus on situations in which invasive species petition, predation, and disease limit the ability present substantial threats to the biotic integrity of exotic species to establish reproducing popula- of ecosystems. tions. A community with low ecosystem resistance Moreover, there is a strong historic compo- will be more highly invasible than a community nent to current distributions of invasive exotic with high resistance. "Ecosystem resilience" will plants. For example, Wu et al. (2004) suggest be used to describe the tendency for ecosystem that the low number of naturalized exotic plant processes to remain unchanged following exotic species per log (area) in Taiwan versus Japan invasion. Thus ecosystem processes such as dis- reflects Taiwan s shorter history of introductions. turbance frequency or resource supply rates will The apparent vulnerability of Hawai i s forests remain relatively unchanged following establish- to invasive species reflects, in part, a history ment of an exotic species in a resilient community. of large-scale introductions. Between 1910 and Propagule pressure - a key component of the 1960. some 1026 taxa, all exotic except for invasion cycle (D Antonio and Dudley 1995) - 78 native species, were out-planted into forest is a function of sizes of source populations, reserves statewide (Woodcock 2007). This enter- seed production, and propagule dispersal, all of prise, carried out to restore Hawai i s watersheds. which reflect the ecology and introduction his- also provided opportunity for the establishment tory of the invader rather than attributes of the and spread of invasive species into native forests at ecosystem. an unprecedented scale, and certainly affects our Figure 24.1 illustrates some of the processes perceptions today of the vulnerability of Hawai i s that affect the establishment and impacts of a forests to exotic species. potential exotic invader. The impact of an exotic Our objective here is to consider the circum- plant species on an ecosystem will be a func- stances under which invasive exotic plants have tion both of its abundance (population size and had strong ecological impacts on tropical ecosys- density) and of its capacity, relative to estab- tems and to use these examples to provide insight lished species, to alter ecosystem structure and into the attributes of some tropical rainforests that
Exotic Plant Invasions in Tropical Forests 411
Species diversity
Functional Disturbance and habitat diversity fragmentation
Compet P rod U ctivi
Resource availability
Exotic propagule supply I Herbivores and ] (,/1 pathogenstos
Exotic population growth
Relative per capita exotic impact
Impact of an invasive species
Figure 24.1 Conceptual diagram of factors affecting the impact of exotic plant invasions on a tropical forest ecosystem. Positive effects are shown with solid lines and negative effects with dashed lines. The diagram depicts a variety of interacting processes, some of which reflect attributes of the invaded community and contribute to its resistance to the establishment of new species. Others are attributes of the invading species that affect its ability to reach suitable establishment sites and to alter local ecosystem processes. HI through H4 refer to hypotheses addressing these processes discussed in the text.
might account for the scarcity of exotic species in so we will draw insights from examples on their them. Our examples are drawn from the available fringes. For the same reason, we have defined trop- literature, which necessarily addresses ecosystems ical forests broadly to include forests in the tropics that may be vulnerable to the establishment of and subtropics under a wide range of climatic and exotics by virtue of location (islands, peninsulas) edaphic conditions. We discuss several hypotheses or exposure to frequent or historic disturbances. that might account for scarcity of exotic plants in Cited examples are listed in Table 24.1 for ease of many tropical forest ecosystems, review the avail- reference. We have found few examples of investi- able information, and offer suggestions for future gations in large tracts of intact continental forests, research.
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414 Julie S. Denslow and Saara J DeWalt -fl,I
INVASIBLE TROPICAL note that, on average, islands have about twice as ECOSYSTEMS many exotic plant species as comparable mainland habitats. While many tropical forests appear to be sub- However, not all tropical islands are character- stantially weed-free, invasjves can have strong ized by high densities of exotic species. In their impacts on mainland forest ecosystems where summary of 20 island floras, Wit ci al. (2004) canopy structure is naturally open, where rain- show that tropical islands do not have notably forests are fragmented or disturbed, or where more naturalized exotic species per unit log (area) forests are exploited for crops or timber, and than islands elsewhere nor do oceanic islands have on island ecosystems, where both disturbed and a higher species density than continental islands intact forest ecosystems are vulnerable. (see also Rejrnánek 1996, Sax ci al. 2002). These patterns suggest that factors other than isola- tion or latitude likely affect invasibility of island Islands ecosystems.
Tropical islands are often seen as invasive-species hotspots because of both the abundance of exotic Open-canopied forests species and their impacts in those ecosystems (D Antonio and Dudley 1995, Sax ci al. 2002, Invasive exotic species strongly affect some main- Denslow 2003, Wu ci al. 2004). The effects land tropical forests as well, especially those of these species are not confined to highly dis- with naturally open canopies, even when rela- turbed areas. For example, the flora of Hawaii tively undisturbed. Melaleuca qninqnencrvia (Cay. contains similar numbers of native (989) and S.T. Blake (Myrtaceae( invasion is altering the naturalized exotic (1044) species (Wagner ci al. structure of the Florida Everglades where it 1999), among which are many that invade invades scrub cypress habitats in the ecotone and alter native forests (Smith 1985). These between upland pine forests and cypress swamps include subcanopy trees, such as Psidiiim cat- (Ewel 1986). Annona qiara L. (Annonaceae), tielanuni Sabine (Myrtaceae), Morella Jinja (Ait.) a native of Florida and Central America, cre- Wilbur (Myricaceac), and Schinns terebin(hiJb/ius ates dense thickets where it invades Queensland Raddi (Anacardiaceae); large herbs like Hedy- (Australia) Melaleuca swamp forests (Humphries chinni çjardnericmum Ker Gawl (Zingiberaceae); ci al. 1991). lalcataria inolnccwia (Miq. ) Barneby shrubs such as Clidemia hirta (L) D. Don and and J.W. Crimes (Leguminosae), a large nitrogen- Mc!asioma candidum D. Don (Melastornataceae); fixing tree, invades undisturbed but open- canopied and vines such as Passiflora tarminiana Cop- Met rosideros forests on recent lava flows pens & Barney (Passifloraceac). Examples of in Hawaii (Hughes and Denslow 2005). These forest invaders abound from other islands as examples also emphasize that high-stress habitats, well. I ittospornm undnhitum Vent. (Pit losporaceae) such as frequently flooded or shallow soils, are invades montane rainforests of Jamaica (Belling- also vulnerable to invasions if exposed to exotic ham et al. 21)05); Cinchona pnbesccns VahI (Rubi- species with appropriate physiological tolerances. aceae) is a major forest conservation concern in the Galapagos highlands (MacDonald et al. Disturbed forests 1988): Rubus aceifolins Poiret (Rosaceae) invades the forests of Christmas Island and Reunion Chronic disturbances open forest canopies and (Baret et al. 2003): Cinnamo,,,i,,i zci/!anicum provide opportunities for the spread of aggres- Blume (Lauraceae) invades forest in the Seychelles sive exotics. Such disturbances long have been (Fleischmann 1997): and the neolropical under- recognized to predispose plant communities to story shrub Piper aduiwwn L. (Piperaceae) is exotic species establishment, in part because of spreading in lowland forest in Papua New Guinea the increase in resource availability they cause (Rogers and 1-lartemink 2000). Sax ci al. (2002) (Rcjmhnek 1989, Kit avama and Mueller-Dombois Exotic Plant Invasions in Tropical Forests 415
1998). Naturally 1995. Mueller-Dombois 1995. Davis ci al. 2000. )Laurance 199 7, DiStefaflo et al. ychelles are Mack i t al. 2002). On the continental island of fragmented riparian forests in Se Singapore, numbers of exotic species are positively heavily invaded ( Fleisehniann 1997). In North correlated with canopy openness, but intact rain- Queensland. Australia. forest fragments are forest appeared to be resistant (Teo et al. 2003). degraded further by a suite of exotic vines which In Florida (Horvitz et aL 1995) and Jamaica smother canopy trees and underslory (Humphries 1991). a common pattern iii fragmented (Bellingham et al. 2005). canopy opening blow- et (l!. ing hurricanes facilitated the growth of exotic tropical forests (Laurance 1997). Native vines species already present in the seed and seedling and lianas have similar impacts on fragmented pooi. The forests of the Western Ghats in India sup- forests in Brazil (Tabáncz ci al. 199 7). In contrast, port large populations of native ungulates )Bagchi extensive intact Queensland rainforest appears ci al. 2004) and indigenous human populations resistant to invasions by exotic species. even practicing swidden agriculture. [ he understorics when disturbed by occasional severe windstorms OF these forests are dominated by dense stands (Humphries and Stanton 1992). One conse- quence of forest fragmentation has been the of Lantana camaro I,. Verbenaceae ) . Mikan in oncron( ha FIB. K. (Asteraceae). and C/i ro!no!oeno alteration of successional trajectories by exotic odorota (L.) R.M. King and H. Robinson (Aster- species and the establishment oil agri- aceae), all of neotropical origins (Chandrashekara cultural land of new forest types sometimes domi- and Ramakrish nan 1994, Chandrasckaran and nated initially by exotic species )Lugo and Helmer Swamy 2000). 2004). Browsing and rooting by exotic ungulates fre- quently is associated with invasions of exotic plant species. In Hawai i. pigs contribute to tree and Managed ecosystems shrub death, churn the soil, and disperse seeds Of exotic species, facilitating the spread of Psithinn When coupled with exotic seed sources, distur- cauleuinien into moist forests (Aplet et (!. 1991). bance and canopy opening due to logging and Fensham et al. (1994) described high densities swidden agriculture also facilitate the spread invades of Lantaiia camaro in dry rainforest in northern of invasive species. Cliromoku na odorata Australia following impacts of pig digging and tropical dry forest. in Thailand after extraction ground lire. In Pasoh Forest Reserve in Peninsular of Sliorea siwiiensis Miq. DipterocarpaCeae) for Malaysia, the native pig Sus scram, strongly modi- limber (Chazoul 2004). In South and Central lies the forest understory (Ickes et al. 2001) which America, invasive African grasses, such as may facilitate the spread of the neotropical under- Panicoin i naxim ooi Jacq. ( Poaceac ) and ii rocli!oa niotica (Forssk.) T.Q. Nguyen (Poaceae), impede story shrub C !idemia 10cm. Thus the disturbances associated with ungulate foraging are associated forest regeneration following logging or swidden with the spread of exotic plant species both where agriculture and carr y lire into the edges of intact ungulates are recent introductions and where forest (Uhl and Kauffman 1990. l) Antonio and ungulates are a historic component of the forest Vitousek 1992). The high productivity, aggres- ecosystem. sive spread, and nutritious loliage of these exotic grasses have been important drivers of the conver- sion of Central and South American tropical forest Fragmented forests to cattle pasture (I)arsons 1972). The considerable cost of controlling weeds in Where rainforests are highly fragmented. they are managed ecosystems in the tropics also is indica- subject to edge encroachment from grass fires, tive of their potential to affect the course of penetration of wind and light into the forest inte- secondary succession. barest restoration projects, rior, high rates of canopy daniage, and seed rain and long-term forest management. For exam- from adjacent clearings, all of which facilitate ple, competition from exotic grasses and related the establishment of disturbance-adapted species increased lire frequencies are major impediments 416 Julie S. Denslow and Saara J. DeWalt
to the restoration of tropical dry and mesic for- Hypothesis 1. Tropical forests are est ecosystems (l) Antonio and Vitousek 1 992, resistant to invasions by exotic species Cabin ci al. 2000). Along with nutrient depletion, because they are rich in species and weed encroachment is a principal cause of field functional groups abandonment in swidden agriculture (Nye and Greenland 1960). Early fallow vegetation in trop- The idea that species-rich communities are less ical rainforest environments often is dominated invasible than species-poor communities dates by native pioneer species, but Ramakrishnan and from the writings of Elton (1958), who suggested Vitousek (1989) note that reducing the time that more resources were likely to he pre-empted between clearings in northeast India increased and more niches filled in species-rich than in the dominance of invasive exotics such as Lantana species-poor communities. It has been offered as and Chromolaeiio and other pantropical weeds. In one of the central organizing tenets of invasion tropical tree plantations, competition from both ecology (see reviews by Levine and D Antonio exotic weeds and native pioneer species is an 1999. Mack ii al. 2002) and is an often-used important determinant of the success or failure example of the effects of diversity on ecosystem of tree establishment (Wadsworth 1997). Tropi- processes (Hooper et al. 2005). The relationship cal forest ecosystems may he especially vulnerable between native and exotic species diversity is to the spread of exotic plants from swidden or negative when plot sizes are small (e.g.. Fridley logging operations. These activities not only pro- et al. 2004) and experimental manipulations of vide disturbances that facilitate the establishment community structure have shown that species- of exotic species, but are also the vehicle for the rich communities resist establishment of new fl() reinent of novel species and varieties into lands species more effectively than do less rich corn- adjacent to forest reserves (Denslow 2002). niunities (Levine and D Antonio 1999, Levine This brief review suggests several generaliza- 2000. Tilman et al. 2001, Kennedy et al. 2002). tions: (] ) exotic species are not perceived as In contrast, studies of grasslands (Stohlgreri ci al. a threat to most continental tropical forests; 1999). riparian ecosystems (Levine 2000), islands 2) nonetheless, invasive alien species do affect (Lonsdale 1999, Sax ci al. 20)12), and conti- some tropical forest communities severel notably nental ecosystems (Stark et al. 2006) show that those on islands, those with an open canopy struc- at regional scales both native and exotic species ture, and those frequently disturbed or highly richness are similarly correlated wilh environ- fragmented; and (1) invasive alien species present mental gradients - that is, native and exotic substantial problems in managed ecosystems in species richness are positively correlated and both tropical environments where they alter succes- increase along gradients of increasing resource sional trajectories, impede restoration, and may supply. In the absence of direct evidence, how- become propagule sources driving invasion into ever, these patterns are not sufficient to document intact ecosystems. competitive exclusion or resistance of diverse communities to exotic invaders. Two recent stud- ies have shown that these patterns of negative IMPACTS OF EXOTIC PLANTS ON and positive correlations do not differ from that TROPICAL FORESTS predicted by a neutral model of no species inter- actions and that the relationship between exotic These examples stand in strong contrast to intact and native species richness depends on the area close-canopied hrests where exotic plants are rare. and/or number of individuals sampled (Fridley even in treef all gaps. We discuss several hypothe- et al. 2004. Herben et al. 2004). At small plot ses to account for the apparently high resistance of sizes, native and exotic richness are negatively intact continental tropical forests to the establish- correlated because the number of individuals ment of invasive exotic plants. These hypotheses and species sampled is necessarily limited. At address different processes in exotic invasions as large plot sizes, the number of individuals and indicated on Figure 24.1. species sampled in a plot is more variable and or
Exotic Plant Invasions in Tropical Forests 417
native and exotic species richness are positively tropical forests, a heavy infestation of banns - correlated. exotic or native - can kill or damage canopy Thus there appears to be little support for trees, prevent sapling growth. and contribute to the hypothesis that species richness makes corn- the gradual degradation of rainforest structure munities more resistant to the establishment (Humphries ci a). 1991. Tabánez ci a). 1997, of exotic species. Diverse communities can he Horvitz et al. 1998). invaded where propagule pressure is high (levine and l) Antonio 1999). At Semliki Forest Reserve. I Iganda. high-diversity forests were no more resis- Hypothesis 2. Native rainforest tant to exotic invasion than were the low-diversity species competitively exclude exotic plantations (Rejniânek 1996). The effectiveness species with which the native communit y pre-empts avail- able resources may be more important than The ability of the native plant community to diversity per se in impeding the establishment of exclude potential invaders also will be a function, exotic species (Davis ci a). 1998, 2000. Shea and in part, of growth and dispersal rates of native Chesson 2002. Denslow 200 i and see Hypothesis species and of their ability to rapidly pre-empt 2). Although key functional groups are more likely resources. Two functional groups in particular to be present in species-rich than in species-poor may play important roles in reducing seedling assemblages (Hooper ci a). 200), diverse ecosys- establishment, thus contributing to invasion resis- tems may be highly invasible when key functional tance in tropical forests (e.g.. Rejniänck 1996, groups are missing, as has been proposed for 1999, Fine 2002): (1 (fast-growing pioneers of tropical islands (Kitavamna 1996. Kitayama and several growth forms that effectivel y occupy space Itow 1999, Lonsdale 1999, Fine 2002, Denslow and pre-empt resources in high-light environ- 2003). ments, and (2) broad-leaved understory species I lip h diversity of functional groups may bufler that are able to persist in low-light environments. continental tropical forests against the kinds I ugh-light-demanding pioneers, including fast- of ecosystem and structural alteration caused growing trees. shrubs, large herbs, and lianas, by exotic species iii other ecosystems. When are important components of forest regenera- invasive exotic species represent novel func- tion processes because they quickly establish in tional groups they are likely to alter community large trecfall openings or other disturbed areas, structure, disturbance regimes, or soil processes such as landslips or riparian corridors. l hese with ecosystem-wide consequences (Vitousek sites also provide establishment opportunities for 1986). Tropical forests may be resilient to such exotic species in forest ecosystems (e.g.. Rejmiinek ecosystem-altering consequences of exotic inva- 1996, Knapp and Canham 2000. Webb ci al. sions when exotics do not add new functional 2000. McDowell and Turner 2002). In I lawai i groups to the plant community or have high several exotic Eubus species compete with the per capita impacts relative to native species. native Rnbmis lmowam n.sis A. Gray for gap estab- Ecosystem processes such as nutrient and mois- lishment sites (Gerrish ci al. 1992) and, in the ture supply rates are not easily altered in rainforest Budongo Forest, Uganda, spread of the exotics environments where moist ore supply. nitrogen Cassia spectuhilis DC. (Fahaceae ) and Bronssonctia turnover rates, and net primary productivity are pajmjrifi ra (I.) L l-lér. ex Vent. (Moraceae) is facili- naturally high (Vitousek and Sanford 1987). The tated by gap openings (Shell ci al. 2000). principal impact of exotic species on rainforest High rates of competitive exclusion in pro- communities thus is likely to he through competi- ductive wet tropical forests have been sug- tion for space and resources rather than through gested as a niechanismn for the hump-shaped alteration of ecosystem processes or disturbance pattern of diversity across productivity gradi- regimes. Exotic vines and lianas may he an excep- ents (e.g.. Rosenzweig and Abranisk y 1993) and tion to these generalizations. While this is a high competitive exclusion rates likely reduce well-represented functional group in mainland establishment success of exotic species as well as 418 Julie S. Denslow and Saara J. DeWalt
Ilahive Species. For cXaniiJIc. IICSV hir chill ()f)cJi- lily be more critical than the number of species, iugs are colonized by a combination of large- redundancy within hinctional groups is likely to caved herbs, vines, palms. and last-growing. increase their distribution and impact. light-demanding trees, which rapidly reduce light levels near the ground (Walker et al. 1996, Dcnslow eta!, 1998. Schnitzer et(i!. 2000). Genera Hypothesis 3 High pest loads and high such as Ceeropia, I rema, Balsa, and Maearanqa pest diversity in the tropics deter exhibit some of the highest growth rates observed establishment and spread of exotic among woody plants (Wadsworth 1997). with species life-history characteristics similar to many inva- sive exotics. Where they are abundant, vines lii tropical forests, high diversit y and abundance and lianas suppress seedling establishment and of natural enemies (herbivores and pathogens) sapling growth in gaps (Putz 1991. Schnitzer occasionally may lead to high impacts of native ci al. 2000). Where such pioneer species are Pests on exotic species (e.g., Nair 2001. Novotny rare, forests may be particularly vulnerable to et a]. 2003). Certainly, rates of leaf dam- the establishment of exotics. E-lorvitz etal. (1995) age by herbivores and pathogens tend to he comment on the scarcity of pioneer species in high, although variable among species, in trop- the hardwood hammock flora of south Florida ical ]crests (Coley and Aide 1991. Coley and and speculate that exotic species (especially vines) Barone 1996), Thus, native generalist herbivores, iii these hammocks usurped that role follow- pathogens. and viruses may provide a biotic bar- ing the passage of llurricane Andrew in 1992. rier to invasion (Mack 1996, Parker et (i]. 2006) Oil such as the Galapagos and Hawaii, if they are able to exploit exotic plants. High species with pioneer growth characteristics are diversities of both pests and host plants. which sparse. possibly contributing to the invasibility reach their peak in the wet tropics for many of these ecosystems (Kitayama and [tow 1999, taxa, may increase the probability that an exotic l)cnslow 2003). These species are able to convert plant is suppressed by native herbivores, as shown high resource availability into rapid growth and by Prieur-Richard et al. (2002) in a Mediter- high rates of production. Where invasive species ranean plant community. In addition, generalist increase productivity, such as through nitrogen Pest species may play important regulatory roles in addition to nitrogen-poor soils, competitive exclu- population dynamics of tropical plants. For exam- sion rates are expected to increase as well. For ple, Augspurgcr (1984) describes the importance example, where the nitrogen-fixing tree 1 aleataria of damping-off fungi as a source of seedling mor- oio/nccana invades Hawaiian Metrosideros for- talit y in the tropical forest understory. ()omycetes, est on nitrogen-poor soils, productivity increases a common group of clamping-off fungi, can per- but the native Met rosideros declines (Hughes and sist in the soil in the absence of hosts and l)cnslow 2005). exhibit low host specificity (Augspurger 1984, At the other end of the shade-tolerance spec- Hood etal. 2004). Among insect herbivores, most trum, understory palms, shrubs, ferns, and species are not monophagous but feed on multi- herbs produce dense shade at ground levels ple species within a genus or famil y (Coley and (Montgomery 2004). Where these species are Barone 1996). Some common foliage-feeding her- common, seedling establishment is suppressed bivores. such as leaf-cutter (Attinc) ants (Fowler and seedling densities are low (Denslow ci al. et al. 1989, Farji-Brener 2001, Wirth et (i!. 2003) 1991, Farris-Lopez et al. 2004, Harms et(i!. 2004. and orthoptera (Novotny ci al. 2004), have broad Wang and Augspurger 2004). The inhibitory diets. Leaf-cutier ants in particular are serious effect is strong on native species and likel y would predators of a number of exotic crops, includ- affect exotic species as well. The combined effect ing citrus, eucalyptus, coffee, and cacao: Chei ett of fast-growing pioneers and shadc-tolerani herbs (1989) suggests that the susceptibility of so many and shrubs is to reduce site occupancy by seedlings crop species to this pest is clue in part to their and increase the importance of recruitment lack of defenses. A meta-anal ysis by Parker ci al. limitation in rainforest d ynani ics. While density (2006) showed that exotic invaders often are Exotic Plant Invasions in Tropical Forests 419 repelled by native herbivores. We suggest that Does a biotic barrier in the form of high pest such generalist natural enemies may contribute loads contribute to the relative dearth of invasive to the apparent invasion resistance of tropical exotic species in tropical forests? Does escape from forests. natural predators give exotic species an advantage This biotic barriers hypothesis runs counter to where they are introduced? Both of these h ypothe- one of the principal explanations of invasiveness - ses are compelling and supported by examples. the enemy release hypothesis (ERH).Thts hypothe- Further evaluation awaits more information on sis proposes that the accidental or even intentional the population-level effects of natural enemies on introduction of plants awa y from their native exotic species. range is accomplished most often without con- comitant introduction of the specialist herbivores, pathogens, and viruses that attack and limit their Hypothesis 4. Low propagule availability populations in their native range. II native species contributes to the rarity of exotic are limited by their own suite of natural enemies species in many tropical forests where exotics are introduced, then exotics may proliferate because of their relatively lower pest The distribution and abundance of man y forest loads (Elton 1958, Maron and Vila 2001, Keane plant species, in temperate as well as in tropical and Crawley 2002). Indeed, there is evidence that. forests, are limited by failure to recruit seedlings to where introduced, some exotic tropical species sites otherwise suitable to their establishment and have lower pest loads in their invasive than in growth (Clark ci al. 1998, 1 999a, Turnbull ( i a). their native range and lower pest loads than local 2000. Beckage and Clark 200). Svenning and native species in their invasive range. For exam- Wright 2005). Factors contributing to recruit- ple. invasive species oil the main island ment limitation include those affecting the size of the tropical Seychelles, suffered less leaf area of the seed crop (fecundit y and the density and loss to herbivores than native woody species (Dietz distribution of adult trees), close and distant dis- etal. 2004). Native pioneer species were especially persal (Clark ci of. 1999h), and post-dispersal susceptible to herbivores (C. Kueffer pers.cornin.). Factors such as pests and pathogens which affect In addition, a biogeographical comparison of the germination and seedling establishment (Clark impact of natural enemies on the neotropical ci al. 1998, Nathan and Muller-Landau 2000. 2000). shrub Clideuna !iirta in its native and introduced Turnbull et al. 2000. Zimmerman ci al. ranges found that plants were heavily attacked Dispersal and recruitment limitation increasingly by insect herbivores and fungal pathogens in the are seen as major determinants of the relative native range, particularly in forest undersiory. but abundances of species in forest ecos ystems (Clark that they were relatively pest free in the introduced et a). 1999h, Harms ci al. 20€ 0. Nathan and range (DeWall et al. 2004). The consequences of Muller-Landau 2000, Hubbell 2001. Denslow pest-load reduction to C. Idita appear to include et al, 2006). not only proliferation in the introduced range, but Propagule supply also plays a major role in also invasion of forest understor y, where it does exotic species invasions (Von I toile and Simberloff not occur in its native range (DeWalt ci al. 2004). 2005). For example. some of the strongest predic- The relative success of plantations of exotic species tors of invasiveness are those that alicet propag- such as rubber (lievea brasilicnsis )Willd.) Much.- ule distribution and abundance, including the Arg. !Euphorbiaceiie!) and Eucalyptus (Myrtaceae) duration, frequency, and area at exotic species in the tropics is also attributable in part to their introductions (Richardson 1999. Lockwood et al. escape from heavy pest loads, particularly from 2005). Forests most likely to be free of exotic specialists in their native ranges (Rosenthal et (1!. species are those with low exposure to propag- 1979. (1adgil and Bain 1999). Thus, some tropi- ules from urban or agricultural areas (Aragon and cal plant populations may he regulated by natural Morales 2004. Sullivan ci al. 2005). Disturbed enemies to the extent that release from these forests may be free of exotic species if propag- enemies leads to their proliferation in introduced ule input is low. In Hawaii Volcanoes National ranges (DeWalt 21)05). Park. montane rainforests heavily damaged by pig 420 Julie S. Denslow and Saara J. DeWalt
browsing are little affected by exotic species where pose the greatest threat to Hawaii s native ecosys- human traffic is low ( L Tuntson personal commu- tems were introduced as ornamentals. Note- nication). Forest fragmentation, road cons( ruc- worthy examples of shade-tolerant ornamentals tion, and other sources of human disturbance are that have become invasive in tropical forests likely to expose adjacent forests to seed rain from include Micon ia cal vesrm us DC, (Melastonlataceue), exotic species. Fine (2002) has suggested that the a neotropica I tree invasive in native forests of scarcity of exotic species in tropical forests may French Polynesia (Meyer 1996) and F-lawai i reflect a more recent history of disturbance and (Conant ci al. 1997); /lrdisia elliptica Thunh. fragmentation in tropical than in temperate for- (Myrsinaceae), which has become invasive in est. Although forest clearing and fragmentation hammocks of south Florida )Horvitz ci al. 1998): is a more recent phenomenon in tropical than in and numerous vines and lianas with shade- temperate forests, human populations have lived tolerant juvenile stages. such as Merremia tnherosa in and exploited tropical forests for centuries. Fur- L.) Rendle )Convolvulaceae) and Jasininion ther, natural disturbance regimes in wet tropical dichotomnoi Vab I (Oleaceae) (I Iorvitz ci al. 1998), forests are high (Denslow 1987). It is unlikely that also invasive in south Florida. disturbance alone accounts for the distribution of In the absence of experimental additions of exotic species. seeds (Turnbull et al. 2000). it is dtl licult to eval- Low exotic species abundances may reflect a uate the role of propagule availability in limiting historic lack of seed availability from species with exotic species in tropical forests. Tropical forests, appropriate physiological characteristics, such as like their temperate counterparts, are not likely to shade tolerance, for establishment in tropical rain- be strongly affected by exotic plant invasions if the forest. Exotic plants, especially woody species, have forests are buttered from exposure to propagule been widely introduced in the tropics, often at sources (e.g., Pyck etal. 2002). grand scales. Extensive forestry, agricultural, and land-reclamation projects juxtapose large popu- lations of exotic species with native forest. Many CONCLUSIONS of these planted exotic species have life-history attributes similar to those of native pioneers and The scarcity of exotic plants recorded from intact gap colonizers (Wadsworth 1997). For example, continental tropical forests suggests that tropi- fast-growing species in the genera l inns. Tectona. cal forests may be resistant to invasions of exotic Eucahjptns, and Ginelioo commonly have been plants. I ligh species and functional group diver- planted for industrial timber (Wadsworth 1997), sity, high competitive exclusion rates, and high while many species and genotypes of Leuraeno. pest loads all ma y confer a certain biotic resistance Albizia. Acacia, and Calbandra have been intro- to the establishment and spread of exotic species in duced as utility species to rehabilitate degraded tropical forests. Similarly, high diversity and high soils and provide fodder and firewood (Hughes productivity may increase the resilience of tropical and Styles 1989, Hughes 1994). Tropical forests forests to the kinds of ecosystem changes effected may not be immune to the spread of such by invasive species in other ecosystems. However. high-light-demanding exotic species, which may we are unable to evaluate these hypotheses fully appear in natural forest clearings where they can because we cannot evaluate exposure levels of impede regeneration of native species )Rejinánck tropical forests to propagules of exotic species. 1996). there are exceptions to the general pattern of A more likely source of shade-tolerant species sparse exotic species in tropical forests. Prevention is ornamental plants which have been widely and control of invasive species o il in frag- introduced into tropical habitats and are the mented or disturbed ecosystems, and in managed source of many invasive species (Meyer and ecosystems are all major conservation and man- Lavergne 2004, Wu ci (i!. 2004). Daehlei- (per- agement concerns in tropical forest environments. sonal communication) estimates that 39% of the Lessons from islands and exploited ecosystems approximately 100 naturalized exotic species that suggest that control of invasive exotic species p Exotic Plant Invasions in Tropical Forests 421
Will assume increasing importance in the con- exposure to new species capable of taking advan- servation of forest preserves Lis habitats become tage of local environmental opportunities. fragmented and exposed to increasing varieties ot exotic species. Our review highlights several areas in which ACKNOWLEDGMENTS further research would be productive. For exam- ple, what is the role of natural enemies (herbiv- We are pleased to acknowledge our debt to the orous pests and pathogens) in regulating native faculty and students of the Department of Botany and exotic plant populations? We know little of the University of Hawai i at Manoa during about the extent to which top-down factors con- i.S.O s tenure as CE Wilder Visiting Professor and trol tropical plant populations, macli less about to the Department of Ecology and Evolutionary their role in plant invasions. Basic research on Biology at Rice University during S.J,l). s appoint- the role of pests and pathogens in regulating ment as a Huxley Research Fellow. We are also species abundances may provide insight into grateful for comments from C. Kueffer, two ad hoc the mechanisms of invasion as well as eluci- reviewers and from W. Carson which were helpful dating factors structuring plant communities. in improving the manuscript. These issues also are related directly to the devel- opment of sale and effective biological control agents for wildiand weeds (l)enslow and Johnson REFERENCES 201)6). Asso- What are the roles of seemingly minor species Aplet . C.H .. Anderson, SI . . and Stone. CE 1991 ) ciation between feral pig disto rba nec and the coin- such as unclerstory shrubs and pioneer trees in pos ion of some alien plant assemblages in Eiawa ii regulating resource availability in tropical forest Volcanoes National ark. Veqeta(io 9 5. 55-02. ecosystems? Our review suggests that competition Aragon. R. and Morales, J.M. (2004) Species compo- from native pioneers may be critical in invasion sition and invasion in NW Argentinian secondary resistance, yet these species are relatively sparse in forests: effects of land-use history, environment intact rainforests. Recent research documents the mid landscape. Journal of Veqelation Science 14, importance of undcrstory vegetation in reducing 195-204. light levels near the ground (Montgomery 2004). Augspurger. C. 1984) Seedling survival of tropical tree Thus shrubs, ferns, and understory palms could species: interactions of dispersal distances, light gaps. 65. 1 705-I 712. play important roles in limiting exotic species and pathogens. Ecohyjy Bagchi, S., Coyal. SE.. and Sankar, K. (2004) Herbivore establishment. densit y and biomass in a semi-arid tropical dry dccid- Experimental additions of seeds. propagu Ics, or uous lorest of western India. Journal of Tropical Ecology seedlings in tropical forest environments would )0,475-478. provide important insights into processes lim- tlaret. S.. Nicolini, F., I.e Bourgeois. I.. and Strashcrg. U. iting the establishment and spread of species (201)1) Developmental patterns of the invasive bram- (e.g.. Turnbull ci (!. 2000) antI how those pro- ble (Ri /sis alceijiAiiis Poiret. Rosaceae( in Rcunion cesses vary within forests and across landscapes. island: an architectural and morph met nc analysis. regions, and species. A ,inals vi Bolwuj 9 1. 39-48. While farests in general, and tropical rainforests Iteckage. B. antI Clark, J.S. (2001) Seedling survival and in particular, often appear more resistant to the growth of three loresi tree species: the role of spatial 84. 1849-] 561 establishment of exotic species than many other heterogeneity. L cologi ltelhingham. Ej.. Tanner. E.VJ.. and Healey. J.R. (2005) ecosystem types (Rejminek 1989. Fine 2002). H urrica lie disturbance accelerates invasion by the global change is likely to increase their vul- alien tree Pitlosporitol iindulaiwu in Jamaican mon- nerability. Changing climate, altered disturbance tane rain f rcsts.Joii mi of Vt qei (((toil Science 1 6. regimes. and increased forest fragmentation and 675-684. exploitation (Sala et (i!. 2000) may open for- Cabin. RI., Weller. S.C., l.orencc. D.H. eta). (2000) Effects est canopies, and increased global movement of of long-term ungulate exclusion and recent alien species, biotypes. pests, and diseases will provide species control on the preservation and restoration 422 Julie S. Denslow and Saara J. DeWalt
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