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Mechanisms driving avoidance of non-native plants by lizards
Article first published online: 20 NOV 2006
Journal of Applied Ecology
Volume 44, Issue 1, pages 228–237, February 2007
How to Cite
VALENTINE, L. E., ROBERTS, B. and SCHWARZKOPF, L. (2007), Mechanisms driving avoidance of non-native plants by lizards. Journal of Applied Ecology, 44: 228–237. doi: 10.1111/j.1365-2664.2006.01244.x
- Issue published online: 20 NOV 2006
- Article first published online: 20 NOV 2006
- Received 12 January 2006; final copy received 3 August 2006 Editor: Chris Dickman
- alien plant species;
- habitat selection;
- introduced plants;
- invasive species;
- resource availability;
- riparian habitat;
- rubber vine;
- 1Introduced plant species modify the environment and alter ecological interactions in communities, often to the detriment of native fauna, but the causes driving negative effects on fauna are rarely examined. We used native Australian scincid lizards Carlia munda and Carlia pectoralis and the introduced weed rubber vine Cryptostegia grandiflora as a model system to determine the possible underlying mechanisms driving habitat selection by native fauna in an environment invaded by weeds.
- 2Lizards were allowed to select between rubber vine and native eucalypt leaf litter in semi-natural enclosures. To determine the mechanisms of habitat preference, we examined differences in temperature, prey (arthropod) availability and composition, and leaf shape of naturally occurring rubber vine and native vegetation.
- 3Lizards discriminated between leaf litter types: 85% of Carlia pectoralis and 80% of Carlia munda chose native leaf litter over rubber vine, clearly indicating a preference for native habitat.
- 4In the field, rubber vine leaf litter was cooler at the surface than native leaf litter, and during peak lizard activity was below the temperature range of Carlia. Rubber vine also contained significantly fewer arthropod taxa and a significantly different composition of arthropod taxa, with fewer preferred prey items of Carlia than native vegetation.
- 5Finally, rubber vine leaves were significantly shorter than native leaves and the lizards themselves. The shape of rubber vine leaves was different from that of the lizards, potentially making the lizards more obvious on rubber vine litter. This may increase the susceptibility of the lizards to detection by predators.
- 6Synthesis and applications. In comparison with native habitat, rubber vine provided a suboptimal environment for litter-dwelling lizards because of the lower ambient temperatures, reduced availability of prey and a reduction in camouflage from predators (dissimilar leaf and lizard shapes). Our study has identified three possible mechanisms by which an introduced plant species can alter the availability of resources in an environment, making it less attractive to native fauna. Our results highlight the importance of understanding how alien plants alter the environment and further emphasize the critical need for management of plants that replace native habitat with a suboptimal environment.
Introduced plants, particularly invasive species, can have severe negative effects on environments and economies throughout the world (Sakai et al. 2001) and are a significant contributor to anthropogenically mediated, global environmental change (Daehler & Gordon 1997; Vitousek et al. 1997). Invading alien plant species threaten communities by changing ecosystem-level processes and properties (Gordon 1998), including nutrient cycles (Vitousek & Walker 1989; Witkowski 1991; Evans et al. 2001), hydrological cycles (Le Maitre et al. 1996; Blossey 1999), light levels (Standish, Robertson & Williams 2001), habitat structure (Ogle et al. 2000; Grice 2004) and fire regimes (D’Antonio & Vitousek 1992; Rossiter et al. 2003; Brooks et al. 2004). Invasive plants are also associated with changes in wildlife community structure and composition, including reduced native plant species richness (Groves & Willis 1999; Higgins et al. 1999) and colonization rates (Yurkonis, Meiners & Wachholder 2005), reduced vertebrate and invertebrate species richness and abundance (Friend 1982; Braithwaite, Lonsdale & Estbergs 1989; Griffin et al. 1989; Herrera & Dudley 2003; Ferdinands, Beggs & Whitehead 2005) and changes in plant and animal assemblage structure (Wilson & Belcher 1989). The loss of biodiversity caused by invasive alien plants may have cascading trophic effects (Sakai et al. 2001) that alter fundamental ecosystem processes (Knops et al. 1999; Hulme 2006). Occasionally, alien plant species benefit specific wildlife (Braithwaite & Lonsdale 1987; Safford & Jones 1998) and even increase faunal diversity (Marshall et al. 2003). However, the impacts of alien plants, particularly invasive species, are typically negative (Hulme 2006).
The majority of research examining wildlife responses to alien plant species has focused on responses of the native floristic community. Few studies have examined the ecological responses of vertebrates to alien plant species, or the underlying mechanisms driving wildlife responses (Adair & Groves 1998; Blossey 1999; Levine et al. 2003; Grice 2004). Understanding the mechanisms driving faunal responses to disturbances, including invasive alien plant species, is important for predicting how organisms will respond to increasingly modified habitats. The responses of fauna to invasive alien plant species are thought to occur as a consequence of habitat alteration and changes in trophic interactions (Sakai et al. 2001). For example, a change in habitat structure may lead to altered levels of predation compared with native habitat (Schmidt & Whelan 1999). Hence differences among key traits of native and alien plant species are likely to alter the behaviour and survival of fauna in the habitats where alien plants occur (Levine et al. 2003), but this assumption remains untested.
Rubber vine Cryptostegia grandiflora (Roxb.) Brown (Asclepiadaceae) is a widespread, globally distributed, invasive species. It is a free-standing woody liane with the ability to climb and smother trees. Endemic to Madagascar, rubber vine was introduced to several countries as an ornamental shrub or as a source of potential rubber in the late 1800s and early 1900s (Tomley 1998). Rubber vine principally occupies tropical regions but also extends into equatorial and subtropical climatic zones, and is now distributed in a number of biogeographical regions, including northern, central and southern America, south-east Asia, Australia and other Pacific islands (McFadyen & Harvey 1990; Kriticos et al. 2003). In Australia, rubber vine has invaded several plant communities throughout Queensland, including eucalypt woodlands and vine thickets, but favours riparian habitats (Humphries, Groves & Mitchell 1991; Tomley 1998). Because of the severe negative effects on the agricultural, economic and biodiversity values of invaded habitat (McFadyen & Harvey 1990; Humphries, Groves & Mitchell 1991; Tomley 1998), rubber vine is listed as a weed of national significance (Commonwealth of Australia 1999).
Reptiles are strongly dependent on habitat structure for their survival (Pianka 1989) and are therefore excellent model organisms with which to examine faunal responses to disturbances such as invasions of alien plant species. Field observations of reptiles in habitat invaded by rubber vine recorded only a single lizard in rubber vine vegetation compared with 131 lizards in nearby native vegetation (Valentine 2006). Further, several studies have recorded negative correlations between the presence of other alien plants and reptile species richness and abundance (Braithwaite, Lonsdale & Estbergs 1989; Griffin et al. 1989; Smith et al. 1996; Jellinek, Driscoll & Kirkpatrick 2004), suggesting that reptiles may be sensitive to changes in the environment caused by alien plant species.
If reptiles discriminate between alien and native vegetation, this process could influence habitat choice and provide a mechanism by which alien plant species affect local abundance and distribution patterns of reptiles. To examine the influence of alien plants on reptiles, we observed whether litter-dwelling lizards discriminated between litter from native vegetation and the introduced plant rubber vine in semi-natural enclosures. In addition, we compared habitat attributes, including temperature, prey (arthropod) availability and the physical structure of litter, between rubber vine and native habitat patches, in an environment invaded by rubber vine, to determine the possible underlying mechanisms driving habitat choice.
behavioural experiments: leaf litter choice
The two species of lizards examined in this project, Carlia pectoralis De Vis and Carlia munda De Vis, are small (snout to vent 44–52 mm), terrestrial, diurnal skinks that are locally common in the litter of open eucalypt forests of northern Queensland, Australia (Wilson & Swan 2003). We examined skinks occurring along seasonally dry creeks dominated by Melaleuca fluviatilis Barlow, Melaleuca leucadendra (L.) L., Melaleuca bracteate Muell., Casuarina cunninghamiana Miq. and Corymbia tessellaris (Muell.) Hill and Johnson where rubber vine was a component of the vegetation. In this environment, rubber vine occurred as a small shrub, with some towering structures that climbed trees.
A sample of 20 adult Carlia pectoralis was captured by hand, between 11 and 20 April 2005, from Campus Creek, James Cook University (19°19′33″S, 146°45′41″E), and Bohle Creek, Joleka homestead (19°22′31″S, 146°42′22″E), Townsville, Queensland. Twenty adult Carlia munda were also captured by hand between 25 and 29 April 2005 from Bend Creek (20°16′06″S, 146°37′52″E) and Camp Creek (20°16′35″S, 146°41′55″E) at Dreghorn station, 110 km south of Townsville. Both sexes were used in the experiments. Following capture, lizards were transferred to individual plastic cages (33 length × 22 width × 13 height cm) and provided with water, food (cricket Acheta domestica L.), a thermal gradient and a neutral substrate (commercial potting soil), to avoid influencing habitat preference experiments, for example by causing chemosensory habituation to either native or rubber vine leaf litter. Behavioural experiments were conducted between 14 April and 12 May 2005 outdoors at James Cook University. Experiments were conducted in 1000-L oval, plastic enclosures (200 length × 50 height × 100 width cm). A mosaic of sun and shade was provided by commercially available ‘shade cloth’ that blocked 80% of incident solar radiation, attached to a plastic frame positioned at a 45° angle from the rim of each enclosure, allowing some direct sunlight to enter the enclosures but always providing large patches of shade. Such a mosaic is typical of habitats used by these lizards (L. E. Valentine, personal observation). The base of each enclosure was covered with washed river sand. Rubber vine and native eucalypt leaf litter (depth 4 cm) was provided at opposite ends of each enclosure, with allocation of leaf litter type randomly determined. The two leaf litter types were divided by a gap of bare sand, 35 cm wide, and water was provided at both ends of each enclosure.
All leaf litter used in the experiment had been stored in clear plastic bags in the sun for 2 days, killing most invertebrates. In addition, any visible prey items were removed from enclosures prior to use. Thus prey availability during the experiments was assumed to be equally limited. To determine available temperatures within enclosures, data loggers (Thermochron iButtons™, Dallas Semiconductor Corp., Texas), programmed to record the temperature every 15 min, were placed in the centre of each type of leaf litter in each enclosure during the Carlia munda experiments. Temperatures recorded on a typical sunny day showed that a similar thermal regime was available in both the rubber vine and native leaf litter sections of the enclosures. Temperature over a 24-h period ranged from 18·8 °C [± 0·7 °C, 95% confidence interval (CI)] to 32·2 °C (± 2·1 °C), with an average of 23·8 °C (± 0·4 °C) in the native leaf litter section, and from 18·9 °C (± 0·8 °C) to 34·2 °C (± 4·0 °C), with an average of 24·1 °C (± 0·5 °C) in the rubber vine leaf litter section. This indicated that both ends of the enclosures experienced similar temperatures during the experiment.
After the enclosures were established, a single, randomly chosen lizard was released in the centre of the sand gap between the two leaf litter types in each enclosure, and the initial choice of habitat was recorded. Lizards were left undisturbed for 2 days to become accustomed to the new environment. Previous behaviour experiments conducted in these enclosures indicated that the exploratory and escape behaviour of lizards had decreased to a low level, and lizard behaviour was typical of field behaviour within 48 h of release (Langkilde, Schwarzkopf & Alford 2004). Habitat choice was quantified by quietly approaching each enclosure between 09:00 and 10:00 h and recording which habitat contained the lizard. A wooden barrier was placed across the sand gap separating the two habitat types, prohibiting the movement of lizards once observations began. If a lizard was detected immediately, its location (i.e. type of leaf litter) was recorded. If not, active searching was conducted until the lizard was located. Chi-squared goodness-of-fit tests, using Yate's correction, were used to determine habitat choice for each species.
temperature in the field
Temperature is an important variable influencing habitat selection of lizards (Heatwole & Taylor 1987) and may vary between habitat types in the field. Seven piles of leaf litter dominated by rubber vine, and seven piles of native eucalypt leaf litter, were selected along Camp Creek. Sites were chosen where leaf litter was deep (6–10 cm) and each site was separated by at least 50 m. We measured the temperature at each pile by placing temperature data loggers (Thermochron iButtons™) at the top (1–2 cm below surface) and bottom (6–10 cm below surface) of each pile. Temperatures were recorded every 15 min for 2 sunny days from midnight, and an average temperature was calculated over a 24-h period for each pile, allowing us to compare temperature at two depths between native and rubber vine leaf litter.
prey availability in the field
Lizards from the genus Carlia are predators of small arthropods (Wilson & Swan 2003) and habitat choice of lizards may be influenced by potential prey availability. We compared arthropod abundance, taxon richness and assemblage composition between native and rubber vine habitat. Arthropods were collected on 7 August 2003 from six patches of native habitat and six patches of rubber vine habitat along Camp Creek. Arthropods were collected from each site using equal-sized leaf litter samples (bags of 21 width × 30 length cm) and time-constrained (5 min) beating techniques of small shrubs (either native or rubber vine, depending on habitat type). Arthropods collected using beating techniques were captured on a 1 × 1-m calico fabric tray and transferred to alcohol. Leaf litter samples were placed into Berlese funnels for 6 days, until the litter was completely dry and searches of the remaining litter did not reveal any insects. Insects escaping the funnels were preserved in alcohol. Arthropods were later sorted and identified to order using the taxonomy of Harvey & Yen (1989). We combined arthropods captured at each patch using different techniques to examine average arthropod abundance and taxon richness between rubber vine and native habitat patches using t-tests (SPSS version 12) on the log-transformed data. Arthropod assemblages (rare taxa removed) were compared between habitat patches using principal component analysis (PCA; SPSS version 12) of the covariance matrix, on the log (n + 1)-transformed arthropod order abundance.
characteristics of leaf litter piles in the field
We compared characteristics of leaf litter occurring in the field by measuring leaf litter structure and leaf shape between rubber vine and native leaf litter piles (sites described above). Leaf litter pile structure was examined by comparing the proportion of fine, coarse and very coarse particulate matter between rubber vine and native leaf litter piles. At each site, a 19-cm diameter core sample of leaf litter and debris was removed. All leaves and fine particulate matter were sieved through a series of 10-, 5- and 1-mm sieves. For each size category, the total mass of material was weighed to the nearest gram using a 100-g Pesola™ spring balance. The average proportion of each size category in native and rubber vine leaf litter was compared using a manova (SPSS version 12) following arc-sine transformation of the proportional data (Quinn & Keough 2002). The average size of leaves (i.e. length and width) for each pile was also compared between native and rubber vine habitat. Eight randomly selected leaves were measured to the nearest millimetre at each pile using a transparent plastic ruler. Leaf length was measured from the base of the stem to the tip of the leaf, and leaf width was measured at three equidistant locations from 1 cm from the tip to 1 cm from the base, to produce an average width per leaf. Average leaf lengths and widths of leaves were compared between native and rubber vine leaf litter piles using a manova on the log-transformed data.
To examine similarities in lizard and leaf shape, we compared the lengths of the two species of lizards to native and rubber vine leaf lengths. The total lengths of 20 Carlia munda and 20 Carlia pectoralis were measured from snout to tail tip, to the nearest millimetre, with a transparent plastic ruler. Leaf length measurements were obtained by compiling the data described above and randomly selecting 20 leaves from each litter type. An anova on the log-transformed data compared mean lengths among lizard species and leaf litter types. We did not compare lizard widths to leaf widths as lizards from the genus Carlia are slender and both the species observed in this study were obviously much thinner than either rubber vine or native leaves (average lizard width approximately 5 mm).
behavioural experiment: leaf litter choice
During active searching for lizards in the field, we occasionally observed lizards in leaf litter piles that contained both native and rubber vine leaf litter, but lizards were never observed within leaf litter piles that were dominated by rubber vine. We captured 10 male and 10 female Carlia pectoralis and seven female and 13 male Carlia munda. Once animals were released into enclosures, the choice of leaf litter immediately sought was recorded. Both species of lizards dispersed evenly between the native and rubber vine leaf litter (Carlia pectoralis, = 0·05, P > 0·05; Carlia munda, = 0·05, P > 0·05). After 2 days in the semi-natural enclosures, significantly more individuals of both lizard species were observed in native leaf litter compared with rubber vine leaf litter (Carlia pectoralis, = 8·45, P < 0·01; Carlia munda, = 6·05, P < 0·05; Fig. 1), clearly indicating a habitat preference by both lizard species for native leaf litter.
temperature in the field
Temperature was recorded at two depths (top, 1–2 cm deep; bottom, 6–10 cm deep) within leaf litter in the field, to obtain average daily temperature ranges in rubber vine and native leaf litter (Fig. 2). Temperatures at the bottom of leaf litter piles were similar. However, temperatures at the top of leaf litter piles differed considerably, with native leaf litter experiencing higher temperatures than rubber vine leaf litter for the majority of daylight hours (Fig. 2). During peak periods of lizard activity (7:00–11:00; Langkilde, Schwarzkopf & Alford 2003), native leaf litter was within the preferred body temperature range for the genus Carlia, typically between 28 °C and 32 °C (Wilhoft 1961; Singh, Smyth & Blomberg 2002; L. Schwarzkopf, unpublished data; Fig. 2). In contrast, the available temperature at the top of rubber vine leaf litter was similar to the temperature at the bottom of both kinds of leaf litter for most of the day.
prey availability in the field
A total of 17 arthropod orders (Chelicerata, three orders; Uniramia, 14 orders) were identified from beating and leaf litter samples. Although there was a trend for lower abundances of arthropods in rubber vine habitat, there was no significant difference in abundance between habitat types (log abundance t-test, assuming equal variances, t10 = 1·785, P > 0·05; Fig. 3a). However, lower arthropod taxon richness was observed in rubber vine habitat compared with native habitat (log order richness t-test, assuming unequal variances, t6·44 = 2·430, P < 0·05; Fig. 3b). A PCA on the arthropod composition of 12 orders of arthropods (observed in three or more sites) also revealed differences between rubber vine and native habitat (Fig. 4), with significant separation of sites based on habitat type along the first principal component (PC1 site scores t-test, assuming equal variances, t10 = 4·108, P= 0·002). Native habitat was associated with higher number of bugs (Hemiptera), mites (Acarina) and spiders (Aranea), while rubber vine habitat was associated with larvae of butterflies and moths (Lepidoptera; Fig. 4).
characteristics of leaf litter piles in the field
The proportion of fine, coarse and very coarse organic matter (such as leaves, leaf debris and plant litter) was used to describe the structural composition of the two types of leaf litter. Both native and rubber vine leaf litter piles were similar in overall organic matter composition and contained similar proportions of leaf litter within each sieve size category (manova Wilks’ lambda, F3,10 = 0·776, P > 0·05). However, rubber vine leaf litter had shorter and thicker leaves compared with native leaf litter (rubber vine leaves, mean length 64·0 ± 3·9 mm, mean width 30·1 ± 2·4 mm, 95% CI; native leaves, mean length 100·5 ± 10·1 mm, mean width 20·8 ± 4·0 mm, 95% CI; manova Wilks’ lambda, F3,10 = 18·720, P < 0·001; log leaf length anova, F1,12 = 53·367, P < 0·001; log leaf width anova, F1,12 = 15·181, P= 0·002).
In addition, rubber vine leaves were significantly shorter than Carlia munda, Carlia pectoralis and native leaves (log length anova, F3,76 = 21·151, P < 0·001; Tukey's HSD, P < 0·01; P < 0·001; P < 0·001, respectively; Fig. 5). Interestingly, native leaves were not different in length from either lizard species, even though Carlia pectoralis was longer than Carlia munda (Tukey's HSD, P < 0·01). In summary, rubber vine leaves were markedly shorter than either species of lizard, with rubber vine on average 20 mm shorter than Carlia munda and 50 mm shorter than Carlia pectoralis (Fig. 5).
behavioural experiment: leaf litter choice
Both Carlia pectoralis and Carlia munda discriminated between litter from native and rubber vine vegetation, with a clear preference for native leaf litter. This confirms field observations showing that lizards, including both species of skinks examined here, were avoiding rubber vine vegetation (Valentine 2006). Low use of alien plant habitat has been observed previously in reptiles in Mimosa pigra L.- and Tamarix aphylla (L.) Karst-dominated areas (Braithwaite, Lonsdale & Estbergs 1989; Griffin et al. 1989), where the alien plant species altered the vegetation structure or floristics in a manner presumed unfavourable to reptiles. Both of these studies compared reptile (and other vertebrate) abundance and species richness between native vegetation and habitat dominated by an alien plant species. Our study focused on specific aspects affecting a species’ habitat selection in a semi-natural environment, and identified potential mechanisms driving lizard choice where introduced rubber vine is a component of the vegetation.
temperature in the field
We measured aspects of native vegetation and introduced rubber vine habitat that may contribute to the discrimination made by lizards between these two habitats. Temperature differed markedly between native plant and rubber vine leaf litter. The biological and ecological functions of reptiles are dependent upon body temperature, and thermal preferences may influence habitat selection of reptiles (Heatwole & Taylor 1987), including Carlia (Singh, Smyth & Blomberg 2002). During peak periods of lizard activity, native leaf litter was within the preferred body temperature range of Carlia for longer, and throughout the day maintained higher temperatures than rubber vine leaf litter. As the body temperature of small lizards is largely dependent upon habitat temperatures (Heatwole & Taylor 1987), native leaf litter may provide a more thermally suitable environment for the two Carlia species. Additionally, the lower temperatures observed within rubber vine leaf litter may preclude its use by other reptiles. Differences in temperature between litter types were probably related to the surrounding vegetation structure. Rubber vine has a smothering, weeping growth form that, although allowing dappled light to penetrate, produces larger shade patches than native understorey vegetation in the same community. The growth form of an introduced plant may amplify the impacts of changes in habitat structure, particularly when an introduced plant displays a growth form not normally encountered in the native environment (Grice 2004), as is the case with rubber vine in Australian tropical savannas.
prey availability in the field
Small lizards are predators on a wide variety of arthropods (Wilson & Swan 2003), and the stomach contents of three species of Carlia indicated that the main prey items were spiders, grasshoppers, bugs and the larvae of beetles, butterflies and flies (James 1983). The higher taxon richness of native habitat, including greater numbers of spiders and bugs, may provide more foraging opportunities for lizards. In contrast, only the larvae of butterflies and moths were strongly associated with rubber vine habitat, and these arthropods may be unpalatable to lizards. Rubber vine contains a latex (Tomley 1998) and lepidopteran larvae that feed on plants with toxic substances often sequester the compounds, rendering them unpalatable to predators (Nishida 2002). The lepidopterans observed in rubber vine habitat were probably either larvae of the Madagascan rubber vine moth Euclasta whalleyi Popescu-Gorj and Constantinescu, introduced as a biological control of rubber vine (Mo, Trevino & Palmer 2000), or larvae of the native common crow Euploea core corinna Macleay, a species that regularly uses rubber vine as a host-plant (Scheermeyer 1985). Hence rubber vine habitat, with lower taxon richness, fewer preferred prey items and potentially unpalatable caterpillars, may provide inferior food resources for lizards. The presence of a chemical compound, such as latex, in decaying leaf litter may also influence skink habitat choice.
characteristics of leaf litter piles in the field
Although differences in the thermal range and food availability of native and rubber vine leaf litter were observed in the field, lizards selected native leaf litter over rubber vine leaf litter even in experiments when temperature ranges were similar and food was limited. Avoidance of rubber vine leaf litter under these conditions suggests that either lizards have had previous experience of the negative properties of rubber vine leaf litter prior to capture, and have learned to avoid it, or that there are factors other than temperature and food that influenced their habitat choice in the enclosures. One factor that may contribute to the habitat selection of lizards is the appearance or structural properties of the environment (Losos 1990; Irschick & Losos 1999). We found no differences in the organic particulate composition of leaf litter types, but we did observe differences in the shape of leaves, particularly when compared with lizards. Differences in the appearance of leaves may influence habitat discrimination between native and rubber vine vegetation, as both colour and shape of background objects are important aspects of background matching for camouflage (Endler 1978, 1984; Merilaita & Lind 2005). Native leaf litter was composed of longer and thinner leaves, more similar to Carlia body shape, than rubber vine leaves. As rubber vine leaves are shorter than both species of lizards they may be visually more obvious on such litter, which may increase their susceptibility to detection by predators. In contrast, native leaf litter may provide more desirable habitat with the longer leaves, perhaps concealing the lizards. In addition, although we did not do detailed colour analyses, the colour of native leaf litter appeared more similar to Carlia dorsal coloration to human eyes (both the lizards and the leaves appear light brown) than the rubber vine leaf litter (which appears yellowish brown). Although we did not quantify the observation, it was much harder for us to see Carlia on native leaf litter than on rubber vine leaf litter, and this may be true for visual predators with similar visual abilities. Given this, the selection of native leaf litter may reflect background habitat matching by these cryptic skinks.
ecological significance and management implications
Our study provides conclusive evidence that two species of small litter-dwelling skinks discriminate between leaf litter from native and rubber vine vegetation. This discrimination probably influences habitat choice in the field and provides a mechanism by which lizards may be affected by the introduced plant. Differences in native and rubber vine leaf litter piles observed in the field identified three possible underlying mechanisms influencing habitat choice of lizards. First, the top of native leaf litter piles experienced warmer temperatures, in the preferred temperature range of Carlia, during peak lizard activity. Secondly, native habitat contained higher arthropod taxon richness and more preferred prey items than rubber vine habitat. Thirdly, native leaves were similar to Carlia body size and shape, while rubber vine leaves were shorter than both species of lizards. Overall, rubber vine provides suboptimal habitat in comparison with native habitat, by having lower temperature ranges, supporting less favourable prey items and offering reduced opportunities for camouflage (dissimilar leaf size to lizard). Future directions for research may involve isolating the relative importance of each possible mechanism and any interactions. While ambitious, a fully factorial experiment may be useful in elucidating these relationships. In addition, the presence of latex in rubber vine vegetation, and any role it might play in lizard habitat selection, also requires further investigation.
Rubber vine is a globally widespread invasive species and is one of Australia's most serious environmental weeds, with the ability to invade, dominate and degrade susceptible plant communities throughout northern Australia (Humphries, Groves & Mitchell 1991; Adair & Groves 1998). Based on our results, we suggest that, where rubber vine has invaded native communities, litter-dwelling skinks are disadvantaged by the fragmentation and replacement of native habitat with a suboptimal environment. The absence of ground-dwelling lizards within rubber vine leaf litter is also likely to have flow-on effects to higher order predators, including larger reptiles and birds. Given this, rubber vine represents a substantial threat to biodiversity, particularly to the fauna that utilize the riparian waterways where rubber vine is prolific.
Techniques for managing rubber vine include chemical and mechanical methods, biocontrol and fire, although the success of these methods varies. Mechanical and chemical treatments can be effective at removing small or isolated patches of rubber vine (McFadyen & Harvey 1990; Tomley 1998) but, given the weed's extensive distribution, such treatments are unsuitable for wide-scale use. Instead, two biocontrol agents have been introduced in Australia, the leaf-feeding moth Euclasta whalleyi (McFadyen & Harvey 1990; Mo, Trevino & Palmer 2000) and a fungal rust Maravalia crptostegiae (Cumm.) Ono that may be effective at defoliating plants and reducing seedling emergence (Radford 2003; Tomley & Evans 2004). Fire is by far the most economical management tool and is often used for controlling other invasive alien plant species (Emery & Gross 2005). Fire effectively reduces rubber vine survival, density and vegetative growth (Grice 1997; Bebawi & Campbell 2000, 2002), but management burning may also adversely affect native wildlife, particularly in riparian zones. Further research is required to evaluate the effects of fire management on native fauna. Despite the potential negative consequences on native biota, management of rubber vine is required to address its deleterious impacts. As for all invasive alien species, a model for integrated weed management should incorporate a variety of management strategies (Hulme 2006), such as that recommended for the invasive shrub Mimosa pigra (Buckley et al. 2004).
Introduced invasive plant species are a cause of global environmental change (Vitousek et al. 1997) and can alter habitat structure, species composition, ecosystem pathways and ecological interactions in native communities (Gordon 1998; Blossey 1999; Sakai et al. 2001; Grice 2004). Such changes in habitat structure can have cascading consequences by altering the resources available to organisms in the modified environment. When this happens, the habitat created by the introduced species may not meet the requirements of native fauna, disadvantaging certain species. Knowledge of the mechanisms underlying differential use of native and introduced plant habitat is crucial for understanding how introduced plants alter the environment, and will enable managers to better predict faunal responses to disturbances from introduced species.
Funding for the study was provided by the School of Tropical Biology, James Cook University, Tropical Savannas Co-operative Research Centre and the Linnean Society of New South Wales. Access to the study sites was kindly provided by land owners K. Smith, B. Smith, P. Valentine and V. Valentine. We thank B. Byrne for assistance in the field, F. Christidis for identification of arthropods, P. Valentine and A. Grice for useful discussions, and C. Johnson, I. Radford, B. Murray, B. Fox and an anonymous referee for valuable comments on the manuscript. All data collected adhered to the legal requirements of Australia (Scientific Purposes Permit WISO00130802) and the ethical guidelines for treatment of animals of James Cook University (Animal Ethics Approval A714-02).
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