Different responses of congeneric consumers to an exotic food resource: who gets the novel resource prize?

Exotic species can provide abundant food resources for native consumers, but predicting which native species will respond positively remains a challenge. We studied the foraging behavior of black-capped (Poecile atricapillus) and mountain (P. gambeli) chickadees in western Montana to compare the degree to which these congeric and syntopic consumers exploited larvae of Urophora, an exotic biological control insect living within the seedheads of the invasive forb, spotted knapweed (Centaurea stoebe). Chickadees typically forage within tree or shrub cover, whereas knapweed and hence Urophora larvae thrive in open grassland away from cover. We found that black-capped chickadees were much more likely than mountain chickadees to forage for Urophora. Black-capped chickadees strategically minimized time spent in open habitats by flying out from cover to retrieve knapweed seedheads and immediately returning to cover to extract the larvae. Black-capped chickadees also employed an atypical hovering technique nearly twice as often as their congeners did, particularly when foraging away from cover. Via this hovering technique, birds were able to gather knapweed seedheads from erect plants rather than searching for seedheads on the ground. These shifts in foraging behavior allowed black-capped chickadees to exploit Urophora larvae to a much greater degree than their congeners while minimizing exposure to a high-risk habitat, an outcome with potentially important community-wide consequences. Behavioral flexibility has been used to predict the success of invading species. We suggest that behavioral flexibility may also be used to predict how native species will respond to invasions, particularly the availability of exotic food resources.     

Interactions and effects of multiple biological control insects on diffuse and spotted knapweed in the Front Range of Colorado

Abundances and interactions among biological control insects and their effects on target invasive plants were monitored within the flower heads and roots of diffuse knapweed, Centaurea diffusa, and in spotted knapweed, Centaurea stoebe, along the Colorado Front Range. Flower weevils, (Larinus species) and root-feeders (Cyphocleonus achates and Sphenoptera jugoslavica) were released on knapweed that already supported biological control gall flies (Urophora species). At a single monitoring site, seed production by C. diffusa declined from 4400 seeds m⁻² in 1997 to zero seeds m⁻² on the monitoring sites in 2006, while the flowering stem density of C. diffusa declined from a peak of almost 30 stems m⁻² in 2000 to zero stems m⁻² in 2006. The average abundance of Urophora and Larinus in flower heads fluctuated independently during the 2001–2006 interval, while the relative abundance of C. achates and S. jugoslavica in roots exhibited a weak inverse relationship that appeared driven by climate effects. The relative abundance of insects on a population of C. stoebe was monitored for five years as Larinus species and C. achates became established on spotted knapweed that already supported Urophora species. Spotted knapweed seed production on our monitoring site declined from 4600 seeds m⁻² in 2003 to zero seeds m⁻² in 2006. Unlike C. diffusa, substantial numbers of rosettes of C. stoebe remained present. Larinus consumed almost all Urophora encountered in C. diffusa, and consumed about 40% of the Urophora in co-infested flower heads of C. stoebe (ca. 10–15% of the total Urophora population). No negative correlations between the relative densities of flower head and root-feeding insects were observed. The effects of these insects on target plants have produced results consistent with the ‘cumulative stress hypothesis’ for biological control of Centaurea species.     

Biological control agents elevate hantavirus by subsidizing deer mouse populations

Biological control of exotic invasive plants using exotic insects is practiced under the assumption that biological control agents are safe if they do not directly attack non-target species. We tested this assumption by evaluating the potential for two host-specific biological control agents ( Urophora spp.), widely established in North America for spotted knapweed ( Centaurea maculosa ) control, to indirectly elevate Sin Nombre hantavirus by providing food subsidies to populations of deer mice ( Peromyscus maniculatus ), the primary reservoir for the virus. We show that seropositive deer mice (mice testing positive for hantavirus) were over three times more abundant in the presence of the biocontrol food subsidy. Elevating densities of seropositive mice may increase risk of hantavirus infection in humans and significantly alter hantavirus ecology. Host specificity alone does not ensure safe biological control. To minimize indirect risks to non-target species, biological control agents must suppress pest populations enough to reduce their own numbers.     

Establishment and Dispersal ofUrophora affinis(Diptera: Tephritidae) andMetzneria paucipunctella(Lepidoptera: Gelechiidae) in Southwestern Virginia

Two European gall-producing insects,Urophora affinisFrfld. (Diptera: Tephritidae) andMetzneria paucipunctella(Zeller) (Lepidoptera: Gelechiidae) were introduced into Virginia in 1986 for biological control of spotted knapweed (Centaurea maculosaLam.). Adults ofU. affinis(n = 2625) andM. paucipunctella(n = 450) were released at two sites in Montgomery County, Virginia, and their populations were monitored yearly by dissecting spotted knapweed flower heads. Beginning in 1992, knapweed samples collected at various distances from the release sites were checked for dispersal.U. affinisis well established and is spreading slowly. The number of larvae per flower head and the seed numbers are inversely related as plants with the greatest number of larvae per spotted knapweed head had the lowest number of seeds. Knapweed density has declined at one of the release sites which had the highest rate of infestation byU. affinis.Establishment of the moth,M. paucipunctella,is less certain as it has been recovered at a very low level from only one site.     

Effects of plant competition,seed predation,and nutrient limitation on seedling survivorship of spotted knapweed (<Emphasis Type="Italic">Centaurea stoebe</Emphasis>)

We measured seed germination and seedling survivorship of spotted knapweed, Centaurea stoebe, in a series of laboratory and field experiments to evaluate the efficacy of seed limitation as a management focus. This work was initiated 6 years after introduction of several biological control agents. The soil seed bank of the site used in this study contained a mean density of 5,848 seeds/m² (ranging from 0 to 16,364 seeds/m²), and 92% of the seeds isolated from soils were shriveled, discolored, and/or partially decayed. Additionally, none of the intact seeds germinated, suggesting that the viable seed bank at our field study site has been exhausted. Centaurea stoebe seeds were planted into pots under a range of soil nitrogen (N) availability, with half of the pots containing a single density of previously established seedlings of a native cool-season grass, slender wheatgrass (Elymus trachycaulus). A watering regime mimicking local precipitation was applied. Spotted knapweed exhibited large biomass responses to N addition, but the presence of grasses suppressed the ability to exploit this N. Surprisingly, low soil N conditions improved knapweed survivorship in the presence of grasses. Nevertheless, recruitment and biomass were still far below the levels reached in the absence of competition. To evaluate the effect of density on successful recruitment, Centaurea stoebe seed was introduced into a meadow at three densities matching reduced levels of seed production under the constraints of seed predators. These densities were sown with or without a seed mixture of native species, into an existing plant community lacking C. stoebe, and seedling recruitment was recorded over 2.5 years. Across all plots and densities sown (568–2,272 seeds m⁻² year⁻¹), seedling recruitment was less than 1%. The invasion potential of spotted knapweed was greatly diminished when realistic levels of plant competition and biological control limit seed production. We therefore conclude that a combination of seed limitation and shortage of ‘safe sites’ within undisturbed vegetation can limit densities of C. stoebe.     

Plant size preference of Agapeta zoegana L. (Lepidoptera: Tortricidae), a root-feeding biological control agent of spotted knapweed

Agapeta zoegana L. (Lepidoptera: Tortricidae) is an oligophagous herbivore that was introduced to North America as a biological control agent of spotted knapweed, Centaurea stoebe L. subsp. micranthos (Gugler) Hayek (often called Centaurea maculosa Lam.). Spotted knapweed is a perennial plant that usually increases in size each year. A previous field study reported that more larvae were found on larger plants and that infested plants tended to be larger than uninfested ones. Precisely quantifying the size-specific attack rate can help us model the impact of this agent on the weed population and better understand the interspecific interactions to improve the effectiveness of biological control. Field data were analyzed to determine the relative preference of attack for each size class of the host plant. Plants were classified based on root diameter at 2 cm below the root crown. Although small plants (<3 mm root diameter) were more abundant in the field population, the highest infestation rates occurred in large plants. Chesson’s electivity index was generally positive for root diameters >3.5 mm, indicating preferential attack of large plants. Because of its host-size preference, A. zoegana is expected to primarily affect large plants, which is contrary to previous expectations. Quantifying the insect’s direct impact is a difficult challenge, which may require several field seasons of measuring accumulated damage on individual plants. In order to complement the biological control agents already established, foreign exploration should focus on finding an agent that attacks young knapweed plants. These results also indicate that the efficiency of sampling roots in the field to detect the presence of A. zoegana can be improved by choosing only the largest plants.     

How do biological control and hybridization affect enemy escape?

Two mechanisms often linked with plant invasions are escape from enemies and hybridization. Classical biological control aims to reverse enemy escape and impose top-down population control. However, hybridization has the potential to alter interactions with enemies and thus affect biological control. We examined how introductions of biological control agents affect enemy escape by comparing specialist enemy loads between the native and introduced ranges of two noxious weeds (spotted and diffuse knapweed; Centaurea stoebe L. and C. diffusa Lam.) that have been the targets of an extensive biological control program. Hybrids between spotted and diffuse knapweed are often found within diffuse knapweed sites in North America, so we also compared enemy loads on plants that appeared morphologically like diffuse knapweed and hybrids. Finally, we tested the preference for diffuse knapweed, hybrids, and spotted knapweed of one of the agents thought to be instrumental in control of diffuse knapweed (Larinus minutus; Curculionidae). In North America spotted knapweed has largely escaped its root herbivores, while seedhead herbivore loads are comparable in the introduced and native ranges. Diffuse knapweed exhibited seedhead herbivore loads five times higher in the introduced compared to native range. While this pattern of seedhead herbivory is expected with successful biological control, increased loads of specialist insect herbivores in the introduced range have rarely been reported in the literature. This finding may partially explain the better population control of diffuse vs. spotted knapweed. Within North American diffuse knapweed sites, typical diffuse knapweed and hybrid plants carried similar herbivore loads. However, in paired feedings trials, the specialist L. minutus demonstrated a preference for newly created artificial hybrids over North American diffuse knapweed and for European diploid spotted knapweed over North American tetraploid spotted knapweed. Overall though, hybridization does not appear to disrupt biological control in this system.     

The lesser of two weevils: physiological responses of spotted knapweed (Centaurea stoebe) to above- and belowground herbivory by Larinus minutus and Cyphocleonus achates

The physiological responses of plants to variable levels of root and shoot herbivory in the field may yield valuable insights regarding potential compensation or tolerance responses for herbivory. In an infestation of Centaurea stoebe (spotted knapweed) located in the Colorado foothills, we measured physiology, biomass, and flower production of individual plants undergoing a natural range of herbivory by the above- and belowground biological control insects, Larinus minutus and Cyphocleonus achates. Over the growing season, net carbon assimilation rate, transpiration, stomatal conductance, and intercellular leaf [CO₂] (C _i) all decreased, while water use efficiency increased. The decrease in these physiological traits was due to an increase in the intensity of L. minutus damage over time; effects of C. achates root damage to plant physiology, including transpiration were only marginally significant. The effects of these two species on plant physiology were not interactive, and Larinus minutus was found to exert larger negative effects on this invasive plant in terms of plant physiology and potential reproductive output than C. achates. While previous studies have shown C. achates to have significant negative effects on population densities of spotted knapweed, the addition of Larinus minutus to the suite of insects used in biological control of spotted knapweed should facilitate continued or enhanced reduction in densities of this noxious weed.     

Herbivory and novel weapons: no evidence for enhanced competitive ability or allelopathy induction of <Emphasis Type="Italic">Centaurea diffusa</Emphasis> by biological controls

Biological control of weeds by arthropod herbivores is thought to work by reducing the competitive ability of the weed relative to the surrounding vegetation. However, the assumption that herbivory reduces plant competitive ability has not been tested in most biological control systems, and counter to expectation, recent research on the impact of biological control agents on invasive Centaurea species suggests that this genus may respond to herbivory by increased competitive ability through enhanced plant re-growth and/or by inducing increased production of phytotoxic allelochemicals. We examined the impact of two biological control agents of the invasive plant diffuse knapweed (C. diffusa) to see if feeding by either of these insects would enhance the plant’s competitive ability or allelochemical output. Sub-lethal herbivory by either of the biological control agents significantly reduced knapweed performance when the plant was grown in competition with either of two native species. Competition with knapweed significantly reduced the performance of both native species (Artemisia frigida and Bouteloua gracilis), and herbivory by one of the biocontrol agents resulted in a small but significant increase in both native species’ performance. Diffuse knapweed’s putative allelochemical 8-hydroxyquinoline was not detected in experimental or field collected soils from knapweed-infested sites. In contrast to other studies on the impacts of biological control on other Centaurea species, these data support the premise that biological control agents may reduce invading plant competitive ability. We find no evidence for diffuse knapweed allelopathy mediated by 8-hydroxyquinoline or enhanced allelopathy in response to herbivory by biological control agents.     

Tick infestation (Acari: Ixodidae) in roe deer (<Emphasis Type="Italic">Capreolus capreolus</Emphasis>) from northwestern Spain: population dynamics and risk stratification

During the 2007 and 2008 hunting seasons (April–October) the skin of 367 roe deer (Capreolus capreolus L.), hunted in different preserves from Galicia (Northwestern Spain), were examined for ticks (Acari: Ixodidae). The overall prevalence of infestation by ticks was 83.1%. The predominant species was Ixodes ricinus (83.1%), whereas a single Dermacentor marginatus specimen appeared in one roe deer. All developmental stages of I. ricinus were found parasitizing roe deer, the adults being the most frequent (82.2%), followed by nymphs (45.6%) and larvae (27.2%). The mean intensity of infestation by I. ricinus was 43.2 ± 49.85; most of them were adults (30.7 ± 31.64) and in a lesser extend nymphs (16.9 ± 24.74) and larvae (10.7 ± 29.90). Ixodes ricinus was present all over the study with percentages that oscillated between 100% in spring and 57.4% in autumn. CHAID algorithm showed the sex of roe deer as the most influential factor in tick prevalence, followed by the climatic area. The different developmental stages of I. ricinus were more frequent in males than in females, and the prevalence of adults and larvae were higher in roe deer from coastal areas than in those from mountainous and central areas, whereas nymphs were more frequent in mountainous areas. Host age and density were not determinants for tick infestation. Our results confirm that roe deer are important hosts for I. ricinus in northwestern Spain, serving as a vehicle for the geographic distribution of these ticks.     

Influence of seed head-attacking biological control agents on spotted knapweed reproductive potential in western Montana over a 30-year period

Five insect biological control agents that attack flower heads of spotted knapweed, Centaurea stoebe L. subsp. micranthos (Gugler) Hayek, became established in western Montana between 1973 and 1992. In a controlled field experiment in 2006, seed-head insects reduced spotted knapweed seed production per seed head by 84.4%. The seed production at two sites in western Montana where these biological control agents were well established was 91.6-93.8% lower in 2004-2005 than 1974-1975, whereas the number of seed heads per square meter was 70.7% lower, and the reproductive potential (seeds/m(2)) was 95.9-99.0% lower. The average seed bank in 2005 at four sites containing robust spotted knapweed populations was 281 seeds/m(2) compared with 19 seeds/m(2) at four sites where knapweed density has declined. Seed bank densities were much higher at sites in central Montana (4,218 seeds/m(2)), where the insects have been established for a shorter period. Urophora affinis Frauenfeld was the most abundant species at eight study sites, infesting 66.7% of the seed heads, followed by a 47.3% infestation by Larinus minutus Gyllenhal and L. obtusus Gyllenhal. From 1974 to 1985, Urophora spp. apparently reduced the number of seeds per seed head by 34.5-46.9%; the addition of Larinus spp. further reduced seed numbers 84.2-90.5% by 2005. Path analysis indicated that both Larinus spp. and U. affinis contributed significantly to reduction of seed production over the 30-yr period. Spotted knapweed density may not decrease significantly until the seed bank falls below a critical threshold.     

Effects produced by the feeding of larvae of <Emphasis Type="Italic">Ornithodoros</Emphasis> aff. <Emphasis Type="Italic">puertoricensis</Emphasis> (Acari: Argasidae) on laboratory mice

The clinical picture produced by the feeding of larvae of Ornithodoros aff. puertoricensis on laboratory mice, was studied using different larval infestation protocols that included 30, 40 or 50 larvae per mouse and control uninfested groups. Clinical effects appeared around 72 h of larval feeding, having a first stage characterized by hyperaemia in both nasal and ocular mucosa, followed by respiratory symptoms (96–120 h) and nervous incoordination (120–144 h). No one mouse evidenced paralysis, and nervous symptoms were never observed in animals infested with only 30 larvae. High mortality (commonly up to 70%) was observed in mice with respiratory symptoms, while 100% of animals in the nervous phase died between 168 and 192 h after the beginning of larval feeding. When some infested mice were treated with a solution of Amitraz the larvae were killed and reversion of symptoms was observed. These effects are ascribed to the presence of a toxin in the saliva of the feeding larvae.     

Interspecific interactions between the gall-fly Urophora affinis Frfld. (Diptera: Tephritidae) and the weevil Larinus minutus Gyll. (Coleoptera: Curculionidae), two biological control agents released against spotted knapweed, Centaurea stobe L. ssp. micranthos

Interspecific competition has been suggested as an explanation for the failure of some insects as biological control agents for weeds. Enclosure and exclusion cages were used, in southern British Columbia, Canada to evaluate the importance of interspecific competition between a seedhead weevil, Larinus minutus, and a gall-inducing fly, Urophora affinis, two biocontrol agents released against spotted knapweed in North America. At the seedhead scale, U. affinis, which is an inferior biological control agent based on knapweed seed mortality, was the superior competitor. Larinus minutus attack rates were significantly lower in the presence of U. affinis compared to release treatments where L. minutus was attacking alone. Reduced L. minutus attack rates were apparent in seed heads expected to contain both species, assuming insect distributions were random, but instead only contained U. affinis. L. minutus did not significantly affect U. affinis density. Although overall attack rates on knapweed seedheads were higher when both species were together at a site, the consequence of the antagonistic interaction is that overall seed destruction was not as high as it could have been if the weevil were attacking on its own. These results support minimizing the number of biocontrol agents released that use similar resources on the target weed, to avoid negative interactions between control agents and potential reductions in biocontrol efficacy resulting from competitive exclusion.     

Influence of Nutrient Availability on the Interaction Between Spotted Knapweed and Bluebunch Wheatgrass

Centaurea maculosa (Lam.) (spotted knapweed) reduces wildlife and livestock habitat biodiversity and increases erosion. Nutrient availability to plants may be used to accelerate succession away from spotted knapweed. Early‐successional plant communities often have high nutrient availability, whereas late‐successional communities are often found on lower nutrient soils. We hypothesized that removal of nutrients would change the competitive advantage from spotted knapweed to Pseudoroegneria spicatum (bluebunch wheatgrass) (late seral). In two addition series matrices, background densities of Secale cereale (annual rye) and Elymus elimoides (bottlebrush squirreltail) (3,000 seeds/m²) were used to remove nutrients from the soil. In another set of addition series matrices, nitrogen (33 kg/ha) or phosphorus (33 kg/ha) were added to the soil. Nutrient analysis of soil and vegetation indicated that annual rye and bottlebrush squirreltail reduced nutrient availability in soils. In another matrix, neither a background density nor nutrients were added. Data were fit into Watkinson's curvilinear model to determine the competitive relationship between bluebunch wheatgrass and spotted knapweed. This allowed comparison of the equivalence ratios (C) generated from each addition series. The C parameters are the per‐plant equivalent of bluebunch wheatgrass or spotted knapweed and can be interpreted as the ratio of intra‐to‐interspecific competition. The C parameters are also the equivalence ratio of the number of spotted knapweed it takes to have equivalent effect on bluebunch wheatgrass or the number of bluebunch wheatgrass having the equivalent effect on spotted knapweed. Without nutrient manipulation, spotted knapweed was more competitive than bluebunch wheatgrass. The C for bluebunch wheatgrass was 0.17, indicating that 0.17 knapweed plants were competitively equivalent to one wheatgrass. Annual rye changed the competitive balance in favor of bluebunch wheatgrass (C = 9.9). Addition of nitrogen, phosphorus, or the mid‐seral species did not change the competitive relationship between the two species. This preliminary study suggests that succession from spotted knapweed to late‐seral bluebunch wheatgrass community may be accelerated by altering resource availability.     

Field cage assessment of interference among insects attacking seed heads of spotted and diffuse knapweed

Field studies were conducted to determine the competitive interactions between introduced biological control agents that attack the seed heads of spotted knapweed (Centaurea stoebe ssp. micranthos) and diffuse knapweed (Centaurea diffusa). Two weevils, Bangasternus fausti and Larinus minutus (Coleoptera: Curculionidae), were each paired with the previously established fly, Urophora affinis (Diptera: Tephritidae). Each species was released either alone or in pair-wise combinations inside screen cages placed over existing knapweed plants at six field sites in Montana and one in Oregon. Larinus minutus produced almost three times as many progeny on diffuse knapweed as on spotted knapweed. Larinus minutus reproduction was not affected by competition with U. affinis, but U. affinis reproduction was reduced by the presence of L. minutus (by 71% on spotted and 77% on diffuse knapweed). Bangasternus fausti reproduction generally was not affected by competition with U. affinis, nor was U. affinis affected by B. fausti on either host plant. There were extremely few cases of successful production of both weevil and fly in the same capitulum, which was probably because weevil larvae consume the developing flies. Both weevils increased the total proportion of seed heads infested on diffuse knapweed, and B. fausti increased it on spotted knapweed. However, the release of either weevil did not significantly further reduce seed production on either plant. The results and experimental design are discussed in light of the subsequent establishment and impact of these agents.     

Can R*s Predict Invasion in Semi-arid Grasslands?

We estimated R*s and tested the applicability of R* theory on nonindigenous plant invasions in semi-arid rangeland. R* is the concentration of a resource that a species requires to survive in a habitat. R* theory predicts that a species with a lower R* for the most limiting resource will competitively displace a species with a higher R* under equilibrium conditions. In a greenhouse, annual sunflower (Helianthus annuus L.), bluebunch wheatgrass (Agropyron spicatum Pursh), and spotted knapweed (Centaurea maculosa Lam.) were grown in monoculture and 2- and 3-species mixtures for three growth periods in an attempt to reduce soil NO₃-N concentrations below each species’ R*. At the end of each growth period, aboveground biomass by species and soil plant available nitrogen were sampled. Decreasing biomass coupled with decreasing soil plant available nitrogen was used to quantify R*s for the three species. R*s for annual sunflower, bluebunch wheatgrass, and spotted knapweed were estimated to be 0.6±0.16 ppm NO₃⁻, less than 0.05 ppm NO₃⁻, and 0.6±0.13 ppm NO₃⁻, respectively. Estimated R*s did not predict the outcome of competition among species. To successfully predict plant community dynamics on semi-arid rangeland with and without the presence of a nonindigenous invasive species, a more comprehensive model that includes mechanisms in addition to competition may have to be considered. We speculate that R* theory may prove most useful for predicting the outcome of competition within functional groups.     

Host plant testing ofUrophora quadrifasciata [Diptera: Tephritidae] againstCarthamus tinctorius and two North American species ofCentaurea

Host specificity ofUrophora quadrifasciata (Meig.) [Dipt.: Tephritidae], an introduced biological control agent of diffuse and spotted knapweed, was investigated by exposing flies to safflower,Carthamus tinctorius L., and 2 native knapweeds,Centaurea americana Nutt. andC. rothrockii Greenman. Results of the tests, and literature records indicate thatU. quadrifasciata is host specific to a few closely related plants of introduced knapweed species, and thus poses no threat to economically and ecologically important plant species in the United States.      

Influence of Centaurea biebersteinii patch size on Urophora quadrifasciata (Dipt. Tephritidae) in Michigan, USA

Abstract:  Host plant patch size plays an important role in the distribution and densities of many insect species. Understanding how the host plant patch size influences the population of a biological control agent is necessary to monitor the success of a biological control programme. Urophora quadrifasciata (Dipt. Tephritidae) was released in the early 1970s to control the spotted knapweed, Centaurea biebersteinii (Asteraceae) in North America. The studies reported here investigated the influences of spotted knapweed patch size and stem density on U. quadrifasciata larval populations overwintering within capitula in the Upper Peninsula of Michigan, USA. An inverse relationship was found between the percentage of capitula with U. quadrifasciata larvae and spotted knapweed patch size in 2002 from Houghton county, MI. In 2003, an inverse relationship was also found in the south region of the study area in Houghton and Keweenaw counties, Michigan. The percentage of capitula with U. quadrifasciata larvae and spotted knapweed patch size were positively related for the central region. No relationship was found for the North region in 2003. Dispersal of U. quadrifasciata is directed north-east along the Keweenaw Peninsula, Michigan. With this directed spread, areas with well-established populations of U. quadrifasciata would provide source individuals for new colonization. Spotted knapweed patch size may play an important role in the overwintering populations of U. quadrifasciata as a result of dispersal.     

Introduced deer reduce native plant cover and facilitate invasion of non-native tree species: evidence for invasional meltdown

Invasive species are a major threat to native communities and ecosystems worldwide. One factor frequently invoked to explain the invasiveness of exotic species is their release in the new habitat from control by natural enemies (enemy-release hypothesis). More recently, interactions between exotic species have been proposed as a potential mechanism to facilitate invasions (invasional meltdown hypothesis). We studied the effects of introduced deer on native plant communities and exotic plant species on an island in Patagonia, Argentina using five 400 m² exclosures paired with control areas in an Austrocedrus chilensis native forest stand. We hypothesized that introduced deer modify native understory composition and abundance and facilitate invasion of introduced tree species that have been widely planted in the region. After 4 years of deer exclusion, native Austrocedrus and exotic Pseudotsuga menziesii tree sapling abundances are not different inside and outside exclosures. However, deer browsing has strongly inhibited growth of native tree saplings (relative height growth is 77% lower with deer present), while exotic tree sapling growth is less affected (relative height growth is 3.3% lower). Deer significantly change abundance and composition of native understory plants. Cover of native plants in exclosures increased while cover in controls remained constant. Understory composition in exclosures after only 4 years differs greatly from that in controls, mainly owing to the abundance of highly-browsed native species. This study shows that introduced deer can aid the invasion of non-native tree species through negatively affecting native plant species.