REGROWTH WOODLANDS ARE VALUABLE HABITAT FOR COMMUNITIES

Melissa J Bruton 1, Clive A McAlpine 12, Martine Maron 12

1The University of , Landscape Ecology and Conservation Group, School of Geography, Planning and Environmental Management, St Lucia, 4067 2The University of Queensland, ARC Centre of Excellence for Environmental Decisions, St. Lucia, Australia 4067 Corresponding author: Melissa Bruton - [email protected] +61 409 875 780

ABSTRACT: Protection of passive regrowth, or secondary vegetation, offers the potential to cost-effectively alleviate biodiversity declines caused by deforestation. This potential often goes unrealised because the habitat value of regrowth is generally considered marginal. However, the habitat value of regrowth varies among taxa. Disturbed subtropical woodland landscapes provide large-scale passive restoration opportunities. Subtropical woodlands are also rich in reptile diversity. We addressed the question: ‘What is the habitat value of subtropical regrowth woodlands for reptile communities?’ We identified five commonly-observed models of regrowth habitat value and then surveyed reptile communities in 43 cleared, regrowth and remnant Acacia- and Eucalyptus -dominated woodland sites in subtropical Queensland, Australia. Reptile richness, diversity, dominance and community composition followed the “regrowth = remnant” model of high regrowth value, where the habitat values of regrowth and remnant woodlands were similar, and higher than that of cleared land. Unexpectedly, the proportion of juveniles was highest in cleared sites and lower in both regrowth and remnant sites. Our findings challenge the view that the habitat value of regrowth is limited. Consistency in findings between contrasting woodland types suggest that our results may apply in other similarly disturbed woodlands. We conclude that although remnant woodlands are irreplaceable, regrowth woodlands provide valuable habitat for reptile communities and the protection of such regrowth should be a high priority in disturbed subtropical woodland systems.

KEY WORDS

Reptile, Eucalyptus woodland, Acacia woodland, disturbance, subtropical, passive restoration

Citation: Bruton M. J., McAlpine, C. A., Maron, M. (2013) Regrowth woodlands are valuable habitat for . Biological Conservation 165: 95-103

Full article: www.sciencedirect.com/science/article/pii/S0006320713001687

Page 1 of 31

1. INTRODUCTION

Globally, the loss of habitat is the primary cause of biodiversity declines (Dirzo and Raven 2003; IUCN 2008). Habitat restoration attempts to redress this loss, although there is little evidence that any restoration method can ultimately restore full biodiversity or ecosystem function (Allen 1995; Munro et al. 2007; Rey Benayas et al. 2009). Despite this, forests and woodlands in the regrowth phase of restoration can contribute to biodiversity recovery (Plieninger and Gaertner 2011) and have inherent conservation value (Bowen et al. 2009; Chazdon et al. 2009; Lindenmayer et al. 2012). However, the habitat value of regrowth is difficult to quantify and varies among taxa (Barlow et al. 2007). This has led to the biodiversity conservation value of regrowth being overlooked in vegetation management plans (e.g. Government of South Africa 2010; Queensland Government 1999). To maximise restoration and biodiversity benefits in disturbed landscapes, it is vital to understand how regrowth contributes to habitat availability for different biota.

Whilst the spatial extent of active restoration is limited by costs and logistics, passive regrowth can provide important restoration and biodiversity benefits for large areas at minimal cost (Geddes et al. 2011; Guerrero 2010; Prach and Hobbs 2008). Passive regrowth is prominent in subtropical woodlands that have been cleared for agriculture, particularly in the most extensively deforested woodland areas of the world such as the Chaco in South America (Dinerstein et al. 1995; Grau et al. 2005) and the Brigalow Belt and Mulga Lands in Australia (Australian State of the Environment Committee 2001). Woodlands in these regions are high in biodiversity, particularly of reptiles (Covacevich et al. 1998; Leynaud and Bucher 2005; Uetz 2010); however many species are declining due to historical and contemporary habitat loss (IUCN 2010).

Regrowth is generally considered to have intermediate habitat value between cleared or cultivated, and intact vegetation, based on studies focusing on bird and invertebrate communities (Bowen et al. 2007; Gardner et al. 2007a; Gibson et al. 2011). However, the responses of different taxonomic groups to the same disturbance can vary considerably, with regrowth vegetation ranging in habitat value from minimal to high (Barlow et al. 2007). Such findings highlight the limited capacity to generalise the responses of one or two taxa, and the need to understand the impact of disturbance and recovery on all components of biodiversity (Barlow et al. 2007; Wolters et al. 2006). To date, the impact of disturbance and recovery on reptile communities has received minimal attention (Gardner et al. 2007a).

Studies assessing the value of regrowth as habitat for reptile communities are geographically biased towards tropical regions and (Shvidenko et al. 2005), with few studies in subtropical or temperate woodlands (Bowen et al. 2007). Those studies located in cooler and drier regions tend to suffer from insufficient sample size and statistical power (e.g. Green and Catterall 1998), or compare reptile communities in regrowth and remnant vegetation, but not disturbed areas (e.g. Cunningham et al. 2007; Michael et al. 2011). Given the lack of research in the subtropics, and little consensus on the value of regrowth for reptiles in tropical and areas (e.g. Gardner et al. 2007b; Kanowski et al. 2006; Luja et al. 2008), it is difficult to infer the value of subtropical and temperate regrowth woodlands for reptile communities.

In Australia, controls on clearing that were recently introduced have resulted in large areas of subtropical woodland regrowth (Geddes et al. 2011; McAlpine et al. 2009) that have the potential to increase the amount of habitat available to reptiles and aid in arresting declines (Driscoll 2004). Yet the value of such regrowth as habitat for reptiles is not known (Munro et al. 2007). Therefore, empirical assessments of the capacity for regrowth woodlands to help conserve and restore reptile diversity are vital in these highly disturbed regions.

We addressed the question: Do regrowth woodlands have equivalent, lower, or higher habitat value for reptile communities than remnant woodlands and cleared areas? To answer this question, we developed five models of regrowth habitat value for taxonomic communities in disturbed and intact vegetation. We then surveyed

Page 2 of 31

reptile communities in cleared, regrowth and remnant woodlands in sub-tropical Queensland, Australia, and compared our field data against these models. This process enabled us to determine the relative habitat value of passive regrowth in comparison to cleared and remnant woodlands for reptile communities.

2. METHODS

2.1 Habitat value models

To assess the value of regrowth vegetation as habitat for reptile communities, we first defined three levels of regrowth habitat value – limited, moderate and high – based on published taxonomic community trends in disturbed, regrowth and remnant vegetation (Figure 1, Appendix A). Disturbed sites were defined as those experiencing ongoing disturbance that prevents ecosystem regeneration (e.g. regular clearing, cultivation etc.). Regrowth sites were those that had experienced historical clearing but no recent structural disturbance, and are naturally regenerating ecosystems. Remnant sites were those with no record of historical clearing or recent structural disturbance. The most commonly observed trends in fauna diversity, abundance and community composition in these three vegetation states were used to develop five competing models of regrowth habitat value (Figure 1b), which form the conceptual framework for our analyses. A detailed description of the studies we reviewed in formulating the models can be found in Appendix A. The models are:

1) “Null” model: No difference in community measures (diversity, abundance, biomass etc.) between cleared/cultivated, regrowth and remnant vegetation; and community compositions in cleared/cultivated, cleared and remnant vegetation do not differ. Regrowth is of limited habitat value for biodiversity restoration. 2) “Cleared = regrowth” model: Community measures do not differ significantly between cleared/cultivated areas and regrowth vegetation, but are significantly lower than in remnant vegetation (Figure 1b); and community compositions in cleared/cultivated and regrowth vegetation are similar to each other but divergent from that of remnant areas. Regrowth is of limited habitat value for biodiversity restoration. 3) “Increasing” model: Community measures increase from cleared/cultivated to regrowth to remnant vegetation (Figure 1b); and community composition is nested, with cleared/cultivated communities containing a subset of species found in regrowth, and regrowth containing a subset of species found in remnant vegetation. Regrowth is of moderate (intermediate) habitat value for biodiversity restoration. 4) “Regrowth = remnant” model: Community measures do not differ significantly between regrowth and remnant vegetation, but are significantly higher than in cleared/cultivated areas (Figure 1b); and community compositions in regrowth and remnant vegetation are similar but divergent from that of cleared/cultivated areas. Regrowth is of high habitat value for biodiversity restoration. 5) “Complementary” model: Community compositions differ significantly between cleared/cultivated, regrowth and remnant vegetation, and are not nested (Figure 1b). This model applies to community composition only. Regrowth is of high habitat value for biodiversity restoration because it contains a unique community composition.

Page 3 of 31

a) Original vegetation

Disturbance No disturbance

Ongoing Temporary

Cleared/ Regenerating Original cultivated vegetation vegetation

Cleared/cultivated Regrowth Remnant

b) MODEL COMMUNITY TREND REGROWTH VALUE

“Null” Low

“Cleared = Regrowth” Low

Moderate “Increasing”

High “Regrowth = Remnant”

“Complementary” High

Figure 1: Conceptual model : a) disturbance history leading to cleared/cultivated, regenerating and remnant vegetation areas; and b) the value of regrowth as habitat according to the most commonly reported trends in taxonomic community measurements (e.g. species richness) for cleared/cultivated, regrowth and remnant vegetation.

2.2 Predicting reptile community trends

In our literature search, we found only five studies that had assessed reptile communities in cleared/cultivated, regrowth and remnant woodlands (Appendix A): four in tropical rainforest, one in tropical and subtropical rainforest, and one in tropical woodlands. Reptile species richness and abundance trends varied in these studies; however, the “cleared = regrowth” model, indicating limited regrowth habitat value, was the most commonly observed model for both richness and abundance (Appendix A). Community composition was assessed in only two studies (n = 4 groups), with the “complementary” model dominating (Appendix A). Only one study assessed species diversity (Bowman et al. 1990) and another study assessed evenness (Gardner et al. 2007b), with both identifying “increasing” model trends (Appendix A). These findings were used to establish a priori predictions of the trends expected in our study (Table 1).

Page 4 of 31

2.3 Study area and habitat classification

We assessed reptile community trends in a regenerating woodland landscape in semi-arid subtropical Queensland, Australia (Sattler and Williams 1999, Figure 2). Rainfall at the closest meteorological station averages 530 mm per year, with temperatures averaging from 21-34 oC in summer, and 6-20 oC during winter (Bureau of Meteorology 2013).

North

Funnel Traps Brigalow Belt Bioregion Drift 5m Fence

Mulga Lands 5m 7m Bioregion Pit ST GEORGE Trap

Figure 2: The location of the study area and reptile survey sites, with the trap configuration at each survey site.

Forty-three survey sites were located at least 1km apart in three woodland states: i) “Remnant”: woodlands that had never been cleared (Queensland Government 2010), ii) “Regrowth”: areas that were first cleared 10- 23 years prior to this study and had regrown to approximately half the canopy height of remnant areas, and iii) “Cleared”: treeless paddocks containing a mixture of native and introduced pasture grasses. The specific land use history for the study area is uncertain prior to 2001 due to changes in ownership and tenure; however, historical aerial photographs show that regrowth areas were initially cleared between 1988 and 2006. The regrowth areas were all sparsely vegetated in 2006, suggesting that areas cleared between 1988 and 1998 may have been subjected to more than one clearing event. Regrowth areas were de-stocked for at least 5 years prior to the surveys for this study. We assessed reptile communities in two different regrowth and remnant woodland types: i) open poplar box, Eucalyptus populnea -dominated (“ Eucalyptus ”), and ii) dense bendee, Acacia catenulata -dominated (“ Acacia ”) woodlands.

Variation in habitat structural complexity is known to influence reptile communities (Cunningham et al. 2007; Munro et al. 2007; Woinarski et al. 2009). Therefore, we identified and accounted for structural heterogeneity in our research design. We assessed each potential survey site for structural complexity using an additive habitat complexity score based on a rating of 0-3 for each structural element, with 0 indicating that the structure was absent and 1, 2 and 3 representing increasing amounts of the structural element present (Coops

Page 5 of 31

and Catling 2000; McElhinny 2002). To increase relevance for semi-arid woodland structure and reptiles, we used six structural elements: i) number of vegetation layers, ii) amount of fallen debris, iii) shrub cover, iv) ground vegetation cover, v) litter cover, and vi) number of termite mounds (Garden et al. 2007). Sites with cumulative scores of 1-8 (out of a maximum score of 18) were considered structurally simple, and sites with cumulative scores of 12-18 were considered structurally complex sites (adapted from Coops and Catling 2000). All of the potential cleared and regrowth Acacia survey sites initially assessed in the study area were structurally simple. In contrast, all of the potential regrowth and remnant Eucalyptus sites were structurally complex. Only remnant Acacia sites ranged from structurally simple to structurally complex, with ‘simple’ and ‘complex’ sites selected for surveys. Our final set of 43 selected survey sites comprised six habitat categories: i) cleared (n=7), ii) regrowth Eucalyptus (n=8), iii) remnant Eucalyptus (n=8), iv) regrowth Acacia (n=7), v) ‘simple’ remnant Acacia (n=6), and vi) ‘complex’ remnant Acacia (n=7) (Figure 2).

2.4 Reptile surveys

Sites were surveyed for reptiles using unbaited pit and funnel traps during the 2010/11 and 2011/12 austral warm seasons (October – April). Each survey site consisted of 4 × 20 L pitfall traps, 4 × 75cm long double- ended funnel traps, and 2 × 30 cm high drift fences (Figure 2). Pitfall traps and drift fences were installed 2–4 weeks prior to any surveys, with pit traps closed and drift fences laid flat outside survey periods. Ground cover and structures were disturbed as little as possible during trap line construction and maintenance. All trap lines were located on a north-south axis. Each site was surveyed during three separate periods for a total of twelve trap nights per trap per site. To reduce the confounding effect of weather on reptile activity, seven or eight sites were grouped for simultaneous surveys, with sites from at least five of the six habitat categories in each group. Group composition varied between survey periods. During surveys, traps remained open for 96 hours, and were checked between 4 am and 10 am daily by one observer (M.B.). All captured reptiles were identified to species level, marked with permanent ink on the ventral surface, measured for snout-vent length (SVL), and immediately released. Recaptures within any 96 h trapping period were removed from analyses. Results from the three separate survey periods were pooled for each site.

2.5 Data analyses

The most commonly-reported community measures in habitat change studies are species richness and abundance (Bowen et al. 2007, Appendix A). In addition to these measures, we assessed four supplementary reptile community measures at each survey site: i) ‘true’ diversity (Hill 1973), ii) single-species dominance (Berger and Parker 1970), iii) proportion of juveniles and iv) community composition. ‘True’ diversity (exp[ H’]) is a Hill’s diversity index (Hill 1973; Jost 2006). We chose a priori to use this diversity measure because it is the most ecologically informative measure of diversity (Jost 2006; Tuomisto 2012). ‘True’ diversity weights rare and common species by their frequency to denote the effective number of species present (Jost 2006; Tuomisto 2012). Juveniles were classed as individuals <75% of the maximum snout-vent length (SVL) for each species (Shine and Charnov 1992), with maximum SVL calculated as the average SVL of the three largest individuals trapped, or the SVL of the largest individual trapped for species with five or fewer total records. Rarefaction curves for individual sites and for habitat types, and estimated number of species for each habitat type were calculated using the program EstimateS (Colwell 2009). The ICE species richness estimator was used due to the low sample sizes inherent in reptile surveys (Chazdon et al. 1998).

Reptile communities in Eucalyptus and Acacia woodlands were compared separately. Significant differences between cleared, regrowth and remnant woodland reptile communities were identified using planned contrasts for the five numerical reptile community measures (Abdi and Williams 2010; Rosenthal et al. 2000), and non- parametric ordination and permutation analyses for community composition comparisons. Planned contrasts were calculated using the ‘make.contrasts’ function from the ‘gmodels’ package (Warnes 2012) in ‘R’ (R

Page 6 of 31

Core Team 2012). The planned contrasts for Eucalyptus woodlands were: i) cleared vs. regrowth, and ii) regrowth vs. remnant. For Acacia woodlands the planned contrasts were: i) cleared vs. regrowth, ii) regrowth vs. the mean of simple and complex remnant, and iii) simple remnant vs. complex remnant. Dent and Wright (2009) argue that apparent divergences between regrowth and remnant rainforest communities were often due to low sample size. Therefore, to identify statistical artefacts due to insufficient survey effort, we tested the effect sizes for each planned contrast using Cohen’s d metric (Cohen 1994; McMillan and Foley 2011). Statistical significance was set at p <0.05.

Ordination and permutation analyses of community composition were undertaken in the statistical program ‘Primer’ (Clarke and Gorley 2006) using Bray-Curtis distances based on species abundance data. Differences in community composition between vegetation states were plotted using the non-metric multidimensional scaling (MDS) function in ‘Primer’ and statistically compared using the permutation based analysis of similarity (ANOSIM) function. Results from ANOSIM analyses did not differ between untransformed abundance data and square root, fourth root or presence-absence transformed data. We subsequently present and discuss the results from untransformed data.

To identify any effect of clumping in the location of our survey sites on species composition, we used the RELATE function in ‘Primer’ (Clarke and Gorley 2006) to assess the similarity between a Bray-Curtis distance matrix of species composition, and a Euclidian distance matrix of the spatial location of the survey sites. In this analysis, an Rho score of 1 represents a perfect match between the matrices, and a strong correlation between the location and species composition of survey sites, In contrast, an Rho score of 0 represents no correlation between the reptile species composition and spatial location of the survey sites (Clarke and Gorley 2006).

3. RESULTS

A total of 633 individual reptiles from 34 species were sampled during 4 128 trap nights (Appendix B). Reptile trapping success rate was 18 % per day for pit traps and 12 % per day for funnel traps. No individual reptiles were captured at more than one survey site, indicating no movement of marked individuals among sites. Twelve reptile species are known to occur in the study location but were not detected during this study due to rarity, large body size, and/or a known clumped distribution pattern (Appendix B). Sample-based rarefaction curves rarely reached an asymptote for any single survey site. However, effect size analyses suggest sufficient sample size and discriminatory power for all six reptile community variables assessed (Table 1). There was little influence of survey site location on species composition, with distance matrices of species composition and spatial location of the survey sites being dissimilar (Rho = 0.036, p = 0.437).

Page 7 of 31

Table 1: Predicted and observed reptile community measure model trends with significance (p) and effect size (d) results for planned contrasts. Eucalyptus populnea -dominated woodlands Acacia catenulata-dominated woodlands Community Cleared/ Regrowth/ Cleared/ Regrowth/ Simple/ Measure Predicted Model regrowth remnant Observed Model regrowth remnant complex Observed Model Species cleared=regrowth p= 0.003 p= 0.421 regrowth=remnant p= 0.037 p= 0.680 p= 0.498 regrowth=remnant Richness (low value) d= 1.57 d= 0.44 (high value) d= 1.44 d= 0.23 d= 0.52 (high value) increasing p= 0.002 p= 0.581 regrowth=remnant p= 0.002 p= 0.677 p= 0.378 regrowth=remnant Diversity (moderate value) d= 1.88 d= 0.25 (high value) d= 2.04 d= 0.16 d= 0.47 (high value) Dominance increasing p= 0.011 p= 0.951 regrowth=remnant p= 0.004 p= 0.873 p= 0.916 regrowth=remnant (evenness) (moderate value) d= 1.28 d= 0.10 (high value) d= 2.03 d= 0.17 d= 0.16 (high value) Community complementary p= 0.012 p= 0.135 regrowth=remnant p= 0.002 p= 0.085 p= 0.942 regrowth=remnant composition (high value) R= 0.461 1 R= 0.096 (high value) R= 0.858 R= 0.161 R= 0.147 (high value) Proportion of p= 0.016 p= 0.625 unusual 2 p= 0.041 p= 0.176 p= 0.665 unusual 2 juveniles insufficient information d= 1.19 d= 0.30 (cleared highest) d= 0.71 d= 0.23 d= 0.29 (cleared highest) cleared=regrowth p= 0.001 p= 0.035 unusual 2 p= 0.772 p= 0.367 p= 0.960 null Abundance (low value) d= 0.85 d= 0.58 (regrowth highest) d= 0.09 d= 0.47 d= 0.02 (low value) Bold text highlights statistically significant differences (p<0.05) with moderate to large effect size values ( d >0.5). 1 R= 1 corresponds to perfect separation (dissimilarity) of reptile communities and R= 0 corresponds to perfect overlap (similarity) of reptile communities. 2 A trend not included in the conceptual model

Page 8 of 31

1 3.1 Value of regrowth woodlands for reptile communities

2 Regrowth woodlands differed little from remnant woodlands in terms of habitat value for reptile 3 communities. Reptile richness, diversity, and dominance, in both E. populnea -dominated and A. 4 catenulata -dominated woodlands followed the “regrowth = remnant” model of high regrowth 5 value (Table 1, Figure 3). The composition of reptile communities in both woodland types also 6 followed the “regrowth = remnant” model, with no difference between regrowth and remnant 7 communities, but a distinct composition in cleared sites (Table 1, Figure 4). Regrowth and 8 remnant areas contained a similar proportion of juveniles, but cleared sites had a higher 9 proportion of juveniles than either regrowth or remnant areas (Figure 3, Table 1). Five of the six 10 reptile community trends measured were consistent between the two woodland types, with 11 abundance being the only trend to differ (Table 1, Figure 3). There were no significant 12 differences between reptile community measures for reptiles in simple and complex remnant 13 Acacia sites (Table 1). Overall, regrowth subtropical woodlands had higher habitat value than 14 cleared sites and equivalent habitat value to remnant areas for reptile communities (Table 1).

15

16 Figure 3: Trends in reptile communities from cleared to regrowth to remnant Eucalyptus populnea- and Acacia 17 catenulata -dominated woodlands. Scores for “Remnant Acacia ” are the mean of simple and complex remnant 18 Acacia sites. Reptile community measures are: (a) species richness, (b) diversity, (c) dominance of the most 19 abundant species, (d) the proportion of juveniles present, and (e) abundance. Statistically significant differences are 20 indicated by stars (*) within each woodland type. Error bars represent standard errors.

Page 9 of 31

21 3.2 Predictability of reptile community responses

22 None of the reptile community measures followed the models that we predicted based on the 23 literature (Table 1). Reptile species richness, diversity and dominance were predicted to follow 24 a low regrowth habitat value model (“cleared = regrowth”, with higher values in remnant); 25 however, we observed a high regrowth habitat value model for all three of these measures 26 (“regrowth = remnant” model, with lower values in cleared). In addition, the reptile community 27 compositions were predicted to differ between regrowth and remnant vegetation, but no such 28 difference was present in our study (Table 1, Figure 4). We also observed two uncommon and 29 unexpected trends that were not included in our models (abundance, proportion of juveniles – 30 Table 1, Figure 3). The habitat value models that we observed denote regrowth woodlands as 31 having higher habitat value for reptile communities than the models we predicted and have 32 previously been observed in tropical regions.

33

34 Figure 4: Multi-dimensional scaling (MDS) similarity plots for reptile communities in: a) Eucalyptus populnea - 35 dominated; and b) Acacia catenulata -dominated woodlands.

Page 10 of 31

36 4. DISCUSSION

37 Passively regrowing subtropical woodlands have higher habitat value for reptile communities 38 than is currently acknowledged (Bowen et al. 2007). This study has contributed the first 39 empirical evidence that supports the inclusion of passive regrowth areas as complementary 40 reptile habitat in disturbed subtropical woodland landscapes. The value of regrowth for reptile 41 communities was high in the two structurally different woodland types in this study, indicating 42 regrowth may also be of high habitat value for reptile communities in other subtropical 43 woodlands. Such findings suggest that the maintenance of reptile diversity is enhanced when 44 regrowth is retained in areas with extensive woodland clearing.

45 Although the cleared areas in our study harboured a distinct and depauperate reptile assemblage, 46 the reptile communities in regrowth and remnant woodlands were similar. This implies that key 47 resources that maintain viable reptile communities are provided in the woodlands that 48 regenerate following clearing (Hobbs 1993). Regrowth that succeeds clearing for grazing is a 49 novel ecosystem state (Hobbs et al. 2006) with a novel distribution of resources (Dennis et al. 50 2006; Nielson et al. 2010). The resources vital to reptile persistence in a habitat are likely to be 51 structural in nature (Fischer et al. 2004; Garden et al. 2007; Kanowski et al. 2006), with logs 52 and woody debris, standing dead trees, leaf litter and shrub cover identified as key habitat 53 components (McElhinny 2002). Although there were fewer of these structural resources in 54 regrowth than in remnant woodlands at our study site, they were present (Appendix C), and are 55 likely to have driven similarities among reptile communities in regrowth and remnant 56 woodlands.

57 Unexpectedly, juvenile reptiles were almost twice as prevalent in cleared areas as they were in 58 regrowth or remnant woodlands (Figure 3). Cleared areas were surveyed at the same time as all 59 the other habitats, and juvenile clumping was observed in only three surveys: at a remnant 60 Eucalyptus site, a regrowth Acacia site, and a cleared site. Therefore, it is unlikely that either 61 weather variability or a local nest emergence explain the significantly higher proportion of 62 juveniles in cleared sites. Cleared sites were dominated by a single large and common 63 heliothermic robustus , accounting for 79% of juvenile captures (Appendix D). 64 In contrast, the species compositions of regrowth and remnant Acacia and Eucalyptus 65 woodlands were relatively even, with proportionally fewer C. robustus adults and juveniles 66 (Figure 3, Appendix D). Therefore, it is likely that cleared areas are valuable breeding sites for 67 C. robustus . In both Eucalyptus and Acacia woodlands, the proportions of juveniles present was 68 similar in remnant and regrowth (Figure 3, Table 1), indicating that despite having a lower 69 frequency of juveniles than cleared sites, regrowth woodlands are comparable to remnant 70 woodlands in terms of reptile habitat quality for juveniles.

71 Abundance is one of the most frequently used taxonomic community measures in studies of 72 habitat value, but it is not a good discriminator of disturbance effects on biodiversity (Gibson et 73 al. 2011). During conceptual model development, we found that abundance was highly variable 74 with frequent reports of abundance trends that differed from our five most commonly observed 75 models (Appendix A). For reptiles, trends corresponding to “cleared = regrowth” (Kanowski et 76 al. 2006; Luja et al. 2008), “regrowth = remnant” (Woinarski et al. 2009), and “null” (Bowman 77 et al. 1990; Gardner et al. 2007b, this study) models have all been reported, and other trends are 78 common for this community measure (Kanowski et al. 2006, this study). Such variability in

Page 11 of 31

79 abundance trends between and within biomes suggests that raw abundance has limited use as a 80 measure of habitat value for reptile communities, and possibly other taxa (Gibson et al. 2011), 81 and may lead to spurious inferences regarding habitat quality for biodiversity.

82 We found species richness and raw abundance trends were decoupled (followed different 83 models) in both E. populnea - and A. catenulata -dominated woodlands, with abundance having 84 little influence on the reptile diversity and community composition trends that we observed. 85 This decoupling in reptile communities was first identified in a study by Nimmo et al. (2011) 86 and further supported in the review of Buckley et al. (2012). A posteriori analyses confirm that 87 decoupling of species richness and abundance is present in four of the five studies assessing 88 reptile communities in cleared, regrowth and remnant vegetation (Bowman et al. 1990; Gardner 89 et al. 2007b; Kanowski et al. 2006; Luja et al. 2008, Appendix A). These findings further 90 support limiting the use of raw reptile abundance, and placing greater value on reptile diversity 91 and composition measures, as indicators of habitat quality for reptile communities.

92 We urge caution in transferring our results to disturbance scenarios other than broadscale 93 clearing for grazing. Disturbance history has a strong influence on the habitat suitability of 94 regrowth for fauna with the original and subsequent disturbance methods, intensity, and 95 duration of the disturbance all affecting structural composition (Guariguata and Ostertag 2001). 96 The broadscale clearing that historically occurred in our study region was a relatively low- 97 intensity disturbance that can create high structural heterogeneity (e.g. large amounts of fallen 98 timber) in the regrowth woodlands that follow (Bowen et al. 2007). The positive correlation 99 between structural heterogeneity and reptile diversity and abundance (Fischer et al. 2004; 100 Garden et al. 2007; Kanowski et al. 2006) suggests that the structural relicts of broadscale 101 clearing in regrowth woodlands are likely to assist with rapid reptile re-colonisation. In contrast, 102 clearing for high intensity land uses such as surface mining and cropping destroys all existing 103 habitat structures (Shrestha and Lal 2011) and any successive regrowth (if it can occur) is likely 104 to be structurally depleted, limiting reptile re-colonisation opportunities.

105 4.1 Management implications

106 Policy makers and land managers may overlook the potential value of regenerating areas by 107 forming habitat value judgements based on a small number of indicator taxa (Barlow et al. 108 2007). To better understand the true value of a given habitat, it is important for researchers to 109 complement surveys of commonly-measured indicator taxa with surveys of taxa that have 110 demonstrated less predictable and different responses (Barlow et al. 2007; Wugt Larson et al. 111 2012). Our study has demonstrated that reptiles have an unpredictable and different response to 112 disturbance and recovery than commonly-used indicator taxa such as birds and invertebrates, 113 and so qualify as a good complementary taxon for habitat value and biodiversity assessments in 114 subtropical woodland areas.

115 The sites that were surveyed in disturbed areas (cleared and regrowth) during this study were all 116 within 700 m of remnant woodlands. Therefore, the opportunity for recolonisation via 117 adjacency to source populations was high in both cleared and regrowth sites (Baguette and Van 118 Dyck 2007). However, cleared sites remained species depauperate, confirming that these areas 119 are not suitable habitat for most woodland reptile species. In contrast, regrowth woodlands were 120 recolonised at the time of our surveys. These findings suggest that regrowth areas that are

Page 12 of 31

121 adjacent to remnant woodlands should be prioritised for protection. Currently, there is 122 insufficient landscape-level information available regarding reptile dispersal across different 123 matrices to determine if isolated regrowth areas are able to support a functional assemblage of 124 woodland reptiles (but see Schutz and Driscoll 2008).

125 When the goal is to increase biodiversity in a disturbed landscape, passive regrowth woodlands 126 offer cost-effective (Prach and Hobbs 2008) and valuable complementary habitat to remnant 127 woodlands, potentially contributing more to the conservation of biodiversity than is currently 128 acknowledged (Bowen et al. 2007). Our finding that regrowth is a high value habitat for reptile 129 communities provides critical empirical information that will assist in effective and cost- 130 efficient recovery of highly modified and reptile rich subtropical woodland regions such as the 131 Chaco and Cerrado of South America, and the Brigalow Belt of Australia: regions that have 132 been identified as opportunity areas for landscape restoration as part of the United Nations goal 133 of restoring 150 million hectares of degraded land (IUCN 2011; The Global Partnership on 134 Forest Lanscape Restoration 2010). Currently there is limited legal protection of subtropical 135 woodland regrowth in Australia ( Government 2003; Queensland Government 136 2011), including the regrowth areas at our study site. Therefore, it is important that our findings 137 are considered in any policy discussion regarding the fate of vast areas of regrowth in these and 138 other subtropical woodland areas.

139 Whilst our findings demonstrate that passive regrowth areas can effectively contribute to the 140 amount of high quality habitat available for reptile communities in disturbed subtropical 141 woodland landscapes, the conservation of existing woodlands must always be considered a 142 priority (Maron et al. 2012; Menz et al. 2013; Rey Benayas et al. 2009).

143 5. ACKNOWLEDGEMENTS

144 We thank Australia Zoo for allowing access to their conservation reserve, and for providing 145 long-term field accommodation facilities and support for this project. We also thank two 146 anonymous reviewers for their positive and constructive comments. The Wildlife Preservation 147 Society of Queensland and Warroo-Balonne Landcare provided supplementary funding for the 148 field component of this research. All procedures were carried out with approval from The 149 University of Queensland Ethics Committee (GPEM/187/10) and a Queensland 150 Environment Protection Agency permit (WISP07547310).

151 6. REFERENCES

152 Abdi, H., Williams, L.J., 2010. Contrast Analysis, In Encyclopedia of Research Design. ed. N. 153 Salkind. Sage, Thousand Oaks, CA, USA.

154 Allen, E.B., 1995. Restoration ecology: limits and possibilities in arid and semiarid lands, In 155 Proceedings of the Wildland Shrub and Arid Land Restoration Symposium. pp. 7-15. US 156 Department of Agriculture, Forest Service, Ogden, UT, Las Vegas, NV.

157 Australian State of the Environment Committee, 2001. Land Theme Report Part 2a: Physical 158 Changes to Natural Habitats, In Australian State of the Environment 2001. Independent Report 159 to the Commonwealth Minister for the Environment and Heritage. CSIRO publishing on behalf 160 of the Department of the Environment and Heritage, Canberra.

Page 13 of 31

161 Baguette, M., Van Dyck, H., 2007. Landscape connectivity and animal behavior: functional 162 grain as a key determinant for dispersal. Landscape Ecology 22, 1117-1129.

163 Barlow, J., Gardner, T.A., Araujo, I.S., Avila-Pires, T.C., Bonaldo, A.B., Costa, J.E., Esposito, 164 M.C., Ferreira, L.V., Hawes, J., Hernandez, M.I.M., Hoogmoed, M.S., Leite, R.N., Lo-Man- 165 Hung, N.F., Malcolm, J.R., Martins, M.B., Mestre, L.A.M., Miranda-Santos, R., Nunes-Gutjahr, 166 A.L., Overal, W.L.P., L., Peters, S.L., Ribeiro-Junior, M.A., da Silva, M.N.F., da Silva Motta, 167 C., Peres, C.A., 2007. Quantifying the biodiversity value of tropical primary, secondary, and 168 plantation forests. Proceedings of the National Academy of Sciences USA 104, 18555-18560.

169 Berger, W.H., Parker, F.L., 1970. Diversity of planktonic foraminifera in deep-sea sediments. 170 Science 168, 1345-1347.

171 Bowen, M.E., McAlpine, C.A., House, A.P.N., Smith, G.C., 2007. Regrowth forests on 172 abandoned agricultural land: a review of their habitat values for recovering forest fauna. 173 Biological Conservation 140, 273-296.

174 Bowen, M.E., McAlpine, C.A., Seabrook, L., House, A.P.N., Smith, G.C., 2009. The age and 175 amount of regrowth forest in fragmented brigalow landscapes are both important for woodland 176 dependent birds. Biological Conservation 142, 3051–3059.

177 Bowman, D.M.J.S., Woinarski, J.C.Z., Sands, D.P.A., Wells, A., McShane, V.J., 1990. Slash- 178 and-burn agriculture in the wet coastal lowlands of Papua New Guinea: response of birds, 179 butterflies and reptiles. Journal of Biogeography 17, 227-239.

180 Buckley, L.B., Hurlbert, A.H., Jetz, W., 2012. Broad-scale ecological implications of 181 ectothermy and endothermy in changing environments. Global Ecology and Biogeography 21, 182 873-885.

183 Bureau of Meteorology, 2013. Climate Data Online. Australian Government. 184 Retrieved 8 May, 2013

185 Chazdon, R.L., Colwell, R.K., Denslow, J.S., Guariguata, M.R., 1998. Statistical methods for 186 estimating species richness of woody regeneration in primary and secondary rain forests of 187 northeastern Costa Rica, In Forest Biodiversity, Research, Monitoring and Modelling: 188 Conceptual Background and Old World Case Studies. eds F. Dallmeier, J.A. Comiskey, pp. 189 285-309. The Parthenon Publishing Group, Washington, DC.

190 Chazdon, R.L., Peres, C.A., Dent, D.H., Sheil, D., Lugo, A.E., Lamb, D., Stork, N.E., Miller, 191 S.E., 2009. The potential for species conservation in tropical secondary forests. Conservation 192 Biology 23, 1406-1417.

193 Clarke, K.R., Gorley, R.N., 2006. Primer V6: User Manual/Tutorial. PRIMER-E, Plymouth.

194 Cohen, J., 1994. Statistical Power Analysis for the Behavioral Sciences, 2nd edn. Lawrence 195 Edbaum Associates, Hillsdale, New Jersey, USA.

Page 14 of 31

196 Colwell, R.K., 2009. EstimateS: Statistical Estimation of Species Richness and Shared Species 197 from Samples, Version 8.2, Persistent URL .

198 Coops, N.A., Catling, P.C., 2000. Estimating forest habitat complexity in relation to time since 199 fire. Austral Ecology 25, 344-351.

200 Covacevich, J.A., Couper, P.J., McDonald, K.R., 1998. Reptile diversity at risk in the brigalow 201 belt, Queensland. Memoirs of the Queensland Museum 42, 475-486.

202 Cunningham, R.B., Lindenmayer, D.B., Crane, M., Michael, D., MacGregor, C., 2007. Reptile 203 and arboreal marsupial response to replanted vegetation in agricultural landscapes. Ecological 204 Applications 17, 609-619.

205 Dennis, R.L.H., Shreeve, T.G., Van Dyck, H., 2006. Habitats and resources: the need for a 206 resource-based definition to conserve butterflies. Biodiversity and Conservation 15, 1943-1966.

207 Dent, D.H., Wright, S.J., 2009. The future of tropical species in secondary forests: a quantitative 208 review. Biological Conservation 142, 2833-2843.

209 Dinerstein, E., Olson, D.M., Graham, D.J., Webster, A.L., Primm, S.A., Bookbinder, M.P., 210 George, L., 1995. A Conservation Assessment of the Terrestrial Ecoregions of Latin America 211 and the Caribbean. The World Bank, Washington D.C.

212 Dirzo, R., Raven, P.H., 2003. Global state of biodiversity and loss. Annual Review of 213 Environment and Resources 28, 137-167.

214 Driscoll, D.A., 2004. Extinction and outbreaks accompany fragmentation of a reptile 215 community. Ecological Applications 14, 220-240.

216 Fischer, J., Lindenmayer, D., Cowling, A., 2004. The challenge of managing multiple species at 217 multiple scales: reptiles in an Australian grazing landscape. Journal of Applied Ecology 41, 32- 218 44.

219 Garden, J.G., McAlpine, C.A., Possingham, H.P., Jones, D.N., 2007. Habitat structure is more 220 important than vegetation composition for local-level management of native terrestrial reptile 221 and small species living in urban remnants: a case study from Brisbane, Australia. 222 Austral Ecology 32, 669-685.

223 Gardner, T.A., Barlow, J., Peres, C.A., 2007a. Paradox, presumption and pitfalls in conservation 224 biology: the importance of habitat change for and reptiles. Biological Conservation 225 138, 166-179.

226 Gardner, T.A., Ribeiro-Junior, M.A., Barlow, J., Cristina, T., Avila-Pires, S., Hoogmoed, M.S., 227 Peres, C.A., 2007b. The value of primary, secondary, and plantation forests for a neotropical 228 herpetofauna. Conservation Biology 21, 775-787.

Page 15 of 31

229 Geddes, L.S., Lunt, I.D., Smallbone, L.T., Morgan, J.W., 2011. Old field colonization by native 230 trees and shrubs following land use change: Could this be Victoria’s largest example of 231 landscape recovery? Ecological Management and Restoration 12, 31-36.

232 Gibson, L., Lee, T.M., Koh, L.P., Brook, B.W., Gardner, T.A., Barlow, J., Peres, C.A., 233 Bradshaw, C.J.A., Laurance, W.F., Lovejoy, T.E., Sodhi, N.S., 2011. Primary forests are 234 irreplaceable for sustaining tropical biodiversity. Nature 478, 378-383.

235 Government of South Africa, 2010. National Protected Area Expansion Strategy for South 236 Africa 2008, Department of Environmental Affairs and Tourism, Pretoria.

237 Grau, H.R., Gasparri, N.I., Aide, T.M., 2005. Agriculture expansion and deforestation in 238 seasonally dry forests of north-west Argentina. Environmental Conservation 32, 140-148.

239 Green, R.J., Catterall, C.P., 1998. The effects of forest clearing and regeneration on the fauna of 240 Wivenhoe Park, south-east Queensland. Wildlife Research 25, 677-690.

241 Guariguata, M.R., Ostertag, R., 2001. Neotropical secondary forest succession: changes in 242 structural and functional characteristics. Forest Ecology and Management 148, 185-206.

243 Guerrero, A.C., 2010. Passive restoration in biodiversity hotspots: consequences for an Atlantic 244 Rainforest taxocene. Biotropica 42, 379-387.

245 Hill, M.O., 1973. Diversity and evenness: A unifying notation and its consequences. Ecology 246 54, 427-432.

247 Hobbs, R.J., 1993. Can revegetation assist in the conservation of biodiversity in agricultural 248 areas? Pacific Conservation Biology 1, 29-38.

249 Hobbs, R.J., Arico, S., Aronson, J., Baron, J.S., Bridgewater, P., Cramer, V.A., Epstein, P.R., 250 Ewel, J.J., Klink, C.A., Lugo, A.E., Norton, D., Ojima, D., Richardson, D.M., Sanderson, E.W., 251 Valladares, F., Vila, M., Zamora, R., Zobel, M., 2006. Novel ecosystems: theoretical and 252 management aspects of the new ecological world order. Global Ecology and Biogeography 15, 253 1-7.

254 IUCN, 2008. Wildlife in a Changing World: An Analysis of the 2008 IUCN Red List of 255 Threatened Species, eds J. Vie, C. Hilton-Taylor, S.N. Stuart.

256 IUCN, 2010. IUCN Red List of Threatened Species. Version 2010.2. 257 Retrieved 17 June 2010

258 IUCN, 2011. Pathway to Restoring Lost Forests. < www.iucn.org/?uNewsID=8147 > Retrieved 259 10 Feb, 2012

260 Jost, L., 2006. Entropy and diversity. Oikos 113, 363-375.

Page 16 of 31

261 Kanowski, J.J., Reis, T.M., Catterall, C.P., Piper, S.D., 2006. Factors affecting the use of 262 reforested sites by reptiles in cleared rainforest landscapes in tropical and subtropical Australia. 263 Restoration Ecology 14, 67-76.

264 Leynaud, G.C., Bucher, E.H., 2005. Restoration of degraded Chaco woodlands: effects on 265 reptile assemblages. Forest Ecology and Management 213, 384-390.

266 Lindenmayer, D.B., Northrop-Mackie, A.R., Montague-Drake, R., Crane, M., Michael, D., 267 Okada, S., Gibbons, P., 2012. Not all kinds of revegetation are created equal: revegetation type 268 influences bird assemblages in threatened Australian woodland ecosystems. PLoS ONE 7, 269 e34527.

270 Luja, V.H., Herrando-Perez, S., Gonzalez-Solis, D., Luiselli, L., 2008. Secondary rain forests 271 are not havens for reptile species in tropical Mexico. Biotropica 40, 747-757.

272 Maron, M., Hobbs, R.J., Moilanen, A., Matthews, J.W., Christie, K., Gardner, T.A., Keith, 273 D.A., Lindenmayer, D.B., McAlpine, C.A., 2012. Faustian bargains? Restoration realities in the 274 context of biodiversity offset policies. Biological Conservation 155, 141-148.

275 McAlpine, C., Syktus, J., Ryan, J.G., Deo, R.C., McKeon, G.M., McGowan, H.A., Phinn, S.R., 276 2009. A continent under stress: interactions, feedbacks and risks associated with impact of 277 modified land cover on Australia’s climate. Global change biology 15, 2206-2223.

278 McElhinny, C., 2002. Forest and Woodland Stand Structure as an Index of Biodiversity: A 279 Review. Department of Forestry, Australian National University, Acton ACT.

280 McMillan, J.H., Foley, J., 2011. Reporting and discussing effect size: still the road less 281 travelled. Practical Assessment, Research & Evaluation 14, 1-11.

282 Menz, M.H.M., Dixon, K.W., Hobbs, R.J., 2013. Hurdles and opportunities for landscape-scale 283 restoration. Science 339, 526-527.

284 Michael, D.R., Cunningham, R.B., Lindenmayer, D.B., 2011. Regrowth and revegetation in 285 temperate Australia presents a conservation challenge for reptile fauna in agricultural 286 landscapes. Biological Conservation 144, 407-415.

287 Munro, N.T., Lindenmayer, D.B., Fischer, J., 2007. Faunal response to revegetation in 288 agricultural areas of Australia: a review. Ecological Management and Restoration 8, 199-207.

289 New South Wales Government, 2003. Native Vegetation Act no. 103, NSW Government.

290 Nielson, S.E., McDermid, G., Stenhouse, G.B., Boyce, M.S., 2010. Dynamic wildlife habitat 291 models: seasonal foods and mortality risk predict occupancy-abundance and habitat selection in 292 grizzly bears. Biological Conservation 143, 1623-1634.

293 Nimmo, D.G., James, S.G., Kelly, L.T., Watson, S.J., Bennett, A.F., 2011. The decoupling of 294 abundance and species richness in lizard communities. Journal of Animal Ecology 80, 650-656.

Page 17 of 31

295 Plieninger, T., Gaertner, M., 2011. Harnessing degraded lands for biodiversity conservation. 296 Journal for Nature Conservation 19, 18-23.

297 Prach, K., Hobbs, R.J., 2008. Spontaneous succession versus technical reclamation in the 298 restoration of disturbed sites. Restoration Ecology 16, 363-366.

299 Queensland Government, 1999. The Vegetation Management Act, Queensland Government.

300 Queensland Government, 2010. Regional Ecosystems 6.0, Queensland Department of 301 Environment and Resource Management.

302 Queensland Government, 2011. Regrowth Vegetation Code - on Freehold and Indigenous Land 303 and Leasehold Land for Agriculture and Grazing. Version 2., Department of Environment and 304 Resource Management.

305 R Core Team, 2012. R: A language and environment for statistical computing, R Foundation 306 for Statistical Computing, Vienna, Austria.

307 Rey Benayas, J.M., Newton, A.C., Diaz, A., Bullock, J.M., 2009. Enhancement of biodiversity 308 and ecosystem services by ecological restoration: a meta-analysis. Science 325, 1121-1124.

309 Rosenthal, R., Rosnow, R.L., Rubin, D.B., 2000. Contrasts and Effect Sizes in Behavioral 310 Research. Cambridge University Press, New York, USA.

311 Sattler, P., Williams, R. eds., 1999. The Conservation Status of Queensland's Bioregional 312 Ecosystems. Environmental Protection Agency, Brisbane.

313 Schutz, A.J., Driscoll, D.A., 2008. Common reptiles unaffected by connectivity or condition in 314 a fragmented farming landscape. Austral Ecology 33, 641-652.

315 Shine, R., Charnov, E.L., 1992. Patterns of survival, growth and maturation in and 316 . The American Naturalist 139, 1257-1269.

317 Shrestha, R.K., Lal, R., 2011. Changes in physical and chemical properties of soil after surface 318 mining and reclamation. Geoderma 161, 168-176.

319 Shvidenko, A., Barber, C.V., Persson, R., Gonzalez, P., Hassan, R., Lakyda, P., McCallum, I., 320 Nilsson, S., Pulhin, J., van Rosenburg, B., Scholes, B., 2005. Forest and Woodland Systems, In 321 Millenium Ecosystem Assessment: Current State & Trends Assessment. Island Press, 322 Washington DC.

323 The Global Partnership on Forest Lanscape Restoration, 2010. A World of Opportunity: The 324 World's Forests from a Restoration Perspective, The Global Partnership on Forest Lanscape 325 Restoration.

326 Tuomisto, H., 2012. An updated consumer's guide to evenness and related indices. Oikos 121, 327 1203-1218.

Page 18 of 31

328 Uetz, P., 2010. The . < www.reptile-database.org/ > Retrieved September, 2010

329 Warnes, G.R., 2012. R package 'gmodels', www.cran.r- 330 project.org/web/packages/gmodels/gmodels.pdf .

331 Woinarski, J.C.Z., Rankmore, B., Hill, B., Griffiths, A.D., Stewart, A., Grace, B., 2009. Fauna 332 assemblages in regrowth vegetation in tropical open forests of the , Australia. 333 Wildlife Research 36, 675-690.

334 Wolters, V., Bengtsson, J., Zaitsev, A.S., 2006. Relationship among species richness of different 335 taxa. Ecology 87, 1886-1895.

336 Wugt Larson, F., Bladt, J., Balmford, A., Rahbek, C., 2012. Birds as biodiversity surrogates: 337 will supplementing birds with other taxa improve effectiveness? Journal of Applied Ecology 49, 338 349-356.

339

340

341

Page 19 of 31

Appendix A : Summary of the literature reviewed to develop five models of taxonomic community trends in cleared/cultivated, regrowth and remnant vegetation.

The literature was sourced primarily from relevant papers in the reviews of Bowen et al. (2007) and Munro et al. (2007), and the findings from the large Jari River (Amazonia, Brazil) project on multiple taxa in cultivated, regrowth and remnant rainforest (e.g. Barlow et al. 2007 and other taxon specific papers). We complemented these papers with more recent studies in tropical, subtropical and temperate forests and woodlands, found through citation indexing and repeated database searches, using multiple combinations of search criteria such as ‘regrowth’, ‘vegetation’, ‘secondary’, ‘woodland’, ‘reptile’, ‘invertebrate’, ‘beetle’, ‘clear*’ etc. The final database search occurred in December 2012.

Taxon Biome Country Disturbance Richness Abundance Composition Other First two Year Key title phrase model model model models authors Reptiles Subtropical Australia cleared (clear=reg) 1 (unusual: reg Kanowski, 2006 …factors affecting…reforested…reptiles in rainforest highest, rem Reis cleared… middle) Reptiles Tropical Australia cleared (increase?) (clear=reg) Kanowski, 2006 …factors affecting…reforested…reptiles in rainforest Reis cleared…

Reptiles Tropical Papua New cultivated increasing null diversity: Bowman, 1990 Slash-and-burn agriculture in the wet rainforest Guinea increasing Woinarski coastal lowlands of Papua… Reptiles Tropical Mexico cleared null clear = regrowth complementary Luja, 2008 …not havens for reptile species in tropical rainforest Herrando- Mexico Perez Reptiles Tropical Australia cleared regrowth = regrowth = Woinarski, 2009 Fauna assemblages…Northern Territory… woodlands remnant remnant Rankmore Reptiles Tropical Brazil cultivated clear = null complementary evenness: Gardner, 2007 …plantation forests for a Neotropical (lizards) rainforest regrowth increasing Ribiero- herpetofauna Junior Reptiles Tropical Mexico cleared null clear = regrowth complementary Luja, 2008 …not havens for reptile species in tropical (lizards) rainforest Herrando- Mexico Perez Reptiles Tropical Mexico cleared clear = clear = regrowth clear = regrowth Luja, 2008 …not havens for reptile species in tropical (snakes) rainforest regrowth Herrando- Mexico Perez Amphibians Tropical Madagascar cultivated (reg=rem) (clear=reg) diversity: Vallan 2002 …anthropogenic environmental changes on Rainforest (reg=rem) diversity…

Page 20 of 31

Taxon Biome Country Disturbance Richness Abundance Composition Other First two Year Key title phrase model model model models authors Amphibians Tropical Madagascar cultivated (reg=rem) (clear=reg) diversity: Vallan 2002 …anthropogenic environmental changes on Rainforest (null) amphibian diversity… Amphibians Tropical Brazil cultivated increasing null complementary evenness: Gardner, 2007 …plantation forests for a Neotropical rainforest increasing Ribiero- herpetofauna Junior Amphibians Tropical Australia cleared null null Woinarski, 2009 Fauna assemblages…Northern Territory… () woodland Rankmore Amphipoda Subtropical Australia cleared (reg=rem) Catteral, 2004 …reforestation: perspectives, design issues (litter hoppers) rainforest Kanowski ...Australian… Amphipoda Tropical Australia cleared (increase) Catteral, 2004 …reforestation: perspectives, design issues (litter hoppers) rainforest Kanowski ...Australian… Ants Subtropical Australia cleared null Green, 1998 …fauna of Wivenhoe Park forest Catterall Ants Subtropical Australia cleared (inverse reg=rem/ Catteral, 2004 …reforestation: perspectives, design issues rainforest inverse Kanowski ...Australian… increasing) Ants Subtropical Australia cleared clear = regrowth Piper, 2009 …rapid assessment of epigaeic rainforest Catterall ants…Australia Ants Tropical Mexico cleared (inverse complementary est.rich Gove, Majer 2005 ...ants in the seasonally dry tropics of forest clear=reg) (ICE): Veracruz... reg=rem Ants Tropical Australia cleared clear = regrowth Dawes 2009 Impacts…termites and soil water open forest storage…Australian savanna Ants Tropical Costa Rica cultivated regrowth = (reg=rem) diversity: Roth, 1994 …management systems on ground-foraging rainforest remnant reg=rem, Perfecto ant diversity… evenness: increasing, dominance: reg=rem Ants Tropical Australia cleared (null) Catteral, 2004 …reforestation: perspectives, design issues rainforest Kanowski ...Australian… Ants Tropical Australia cleared clear = regrowth Piper, 2009 …rapid assessment of epigaeic rainforest Catterall ants…Australia Bats Tropical Mexico cultivated (increase) (unusual: reg Medellin, 2000 Bat diversity and rainforest high, rem low) Equihua abundance…disturbance…

Page 21 of 31

Taxon Biome Country Disturbance Richness Abundance Composition Other First two Year Key title phrase model model model models authors Bats Tropical Brazil cultivated clear = complementary Barlow, 2007 Quantifying the biodiversity value of rainforest regrowth Gardner tropical… Beetles Subtropical Australia cleared (clear=reg) Green, 1998 …fauna of Wivenhoe Park forest Catterall Beetles Subtropical Australia cleared (increase) Catteral, 2004 …reforestation: perspectives, design issues rainforest Kanowski ...Australian… Beetles Tropical Australia cleared regrowth = Dawes 2009 Impacts…termites and soil water open forest remnant storage…Australian savanna Beetles Tropical Australia cleared (clear=reg) Catteral, 2004 …reforestation: perspectives, design issues rainforest Kanowski ...Australian… Birds Subtropical Australia cleared (increase) (increase) Green, 1998 …fauna of Wivenhoe Park forest Catterall Birds Subtropical USA cleared (increase) Jounston, 1956 Breeding bird…piedmont of Georgia forest Odum Birds Subtropical Australia cleared regrowth = Catteral, 2004 …reforestation: perspectives, design forest remnant Kanowski issues...Australian… Birds Subtropical Australia cleared increasing Catteral, 2004 …reforestation: perspectives, design rainforest Kanowski issues...Australian… Birds Subtropical Australia cleared increasing regrowth = complementary Hannah, 2007 Impacts of clearing…bird fauna…Eucalypt woodlands remnant Woinarski savanna… Birds Tropical Australia cleared null Catteral, 2004 …reforestation: perspectives, design issues forest Kanowski ...Australian… Birds Tropical Panama cleared (increase) (reg=rem) (clear=reg) Petit, Petit 1999 Bird Rainforest communities…natural…modified…Panama

Birds Tropical Papua New cultivated clear = unusual: reg diversity: Bowman, 1990 Slash-and-burn agriculture in the wet rainforest Guinea regrowth lowest increasing Woinarski coastal lowlands of Papua… Birds Tropical Brazil cultivated clear = null, null complementary Barlow, 2007 …plantation forests for Amazonian birds rainforest regrowth, Mestre regrowth = remnant Birds Tropical Brazil cultivated increasing complementary Barlow, 2007 Quantifying the biodiversity value of rainforest Gardner tropical… Birds Tropical Australia cleared increasing complementary Catteral, 2004 …reforestation: perspectives, design issues rainforest Kanowski ...Australian…

Page 22 of 31

Taxon Biome Country Disturbance Richness Abundance Composition Other First two Year Key title phrase model model model models authors Birds Tropical Cameroon cultivated null inverse reg=rem regrowth = Waltert, 2005 From forest to farmland: Rainforest remnant Bobo habitat…afrotropical forest bird Birds Tropical Indonesia cultivated regrowth = increasing (complementary) est. rich Waltert, 2004 Changes of dung beetle…agroforestry Rainforest remnant (Jack1): Mardiastuti systems...Sulawesi reg=rem Birds Tropical Australia cleared increasing increasing Woinarski, 2009 Fauna assemblages…Northern Territory… woodland Rankmore Butterflies Tropical Papua New cultivated clear = Bowman, 1990 Slash-and-burn agriculture in the wet rainforest Guinea regrowth Woinarski coastal lowlands of Papua… Butterflies Tropical Cameroon cultivated regrowth = unusual: reg complementary est. rich: Bobo, 2006 From forest to farmland: butterfly… (frugivorous) Forest remnant highest unusual Waltert (reg. high, clear low) Butterflies Tropical Brazil cultivated increasing inverse reg=rem complementary diversity: Barlow, 2007 …plantation forests for fruit-feeding (frugivorous) rainforest reg=rem, Overal butterflies… est. rich: increasing Centipedes Tropical Australia cleared increasing Dawes 2009 Impacts…termites and soil water open forest storage…Australian savanna Dung beetles Tropical Brazil cultivated clear = clear = regrowth complementary Gardner, 2008 …plantation forests for neotropical dung rainforest regrowth Hernandez beetles Dung beetles Tropical Indonesia cultivated clear = clear = regrowth (clear=reg) est. rich Shahabuddin, 2005 Changes of dung beetle…agroforestry Rainforest regrowth (Jack1): Schultze systems...Sulawesi clear=reg Earthworms Tropical Australia cleared increasing Dawes 2009 Impacts…termites and soil water open forest storage…Australian savanna Flies Subtropical Australia cleared null Green, 1998 …fauna of Wivenhoe Park forest Catterall Flies (fruit Tropical Brazil cultivated null clear = regrowth Barlow, 2007 Quantifying the biodiversity value of flies) rainforest Gardner tropical… Flies Tropical Brazil cultivated null complementary Barlow, 2007 Quantifying the biodiversity value of (scavenger rainforest Gardner tropical… flies) Hemiptera Subtropical Australia cleared null Green, 1998 …fauna of Wivenhoe Park forest Catterall

Page 23 of 31

Taxon Biome Country Disturbance Richness Abundance Composition Other First two Year Key title phrase model model model models authors Hymenoptera Subtropical Australia cleared null Green, 1998 …fauna of Wivenhoe Park (excl. ants) forest Catterall Hymenoptera Tropical Brazil cultivated null clear = regrowth Barlow, 2007 Quantifying the biodiversity value of (Orchid bees) rainforest Gardner tropical… Invertebrates Subtropical Australia cleared clear = (clear=reg) Green, 1998 …fauna of Wivenhoe Park forest regrowth Catterall Invertebrates Tropical Australia cleared regrowth = increasing Dawes 2009 Impacts…termites and soil water open forest remnant storage…Australian savanna Isopods Tropical Australia cleared increasing Dawes 2009 Impacts…termites and soil water (slaters) open forest storage…Australian savanna Isoptera Subtropical Australia cleared (clear=reg) Green, 1998 …fauna of Wivenhoe Park forest Catterall Isoptera Tropical Australia cleared increasing Dawes 2009 Impacts…termites and soil water (termites) open forest storage…Australian savanna Subtropical Australia cleared (increase) Green, 1998 …fauna of Wivenhoe Park forest Catterall Mammals Temperate USA cleared cleared = (complementary) Lomolino, 2000 Assembly and disassembly… mammal… rainforest regrowth Perault rain forest Mammals Tropical Australia cleared null null Woinarski, 2009 Fauna assemblages…Northern Territory… woodland Rankmore Mammals Tropical Brazil cultivated regrowth = complementary Barlow, 2007 Quantifying the biodiversity value of (large) rainforest remnant Gardner tropical… Mammals Tropical Brazil cultivated null clear = regrowth Barlow, 2007 Quantifying the biodiversity value of (small) rainforest Gardner tropical… Mites Subtropical Australia cleared null Catteral, 2004 …reforestation: perspectives, design rainforest Kanowski issues...Australian… Mites Tropical Australia cleared null clear = regrowth Catteral, 2004 …reforestation: perspectives, design issues rainforest Kanowski ...Australian… Moths Tropical Brazil cultivated inverse clear complementary Barlow, 2007 Quantifying the biodiversity value of rainforest = reg Gardner tropical… Nematodes Tropical Cameroon cleared regrowth = regrowth = Bloemers, 1997 …effects of forest disturbance…tropical (soil) Forest remnant remnant Hodda soil nematodes

Orthoptera Tropical Brazil cultivated null complementary Barlow, 2007 Quantifying the biodiversity value of (grasshoppers) rainforest Gardner tropical…

Page 24 of 31

Taxon Biome Country Disturbance Richness Abundance Composition Other First two Year Key title phrase model model model models authors Orthoptera Subtropical Australia cleared (clear=reg) Green, 1998 …fauna of Wivenhoe Park (grasshoppers, forest Catterall crickets) Orthoptera Subtropical Australia cleared (inverse reg=rem) Catteral, 2004 …reforestation: perspectives, design issues (grasshoppers, rainforest Kanowski ...Australian… crickets) Orthoptera Tropical Australia cleared (inverse reg=rem) Catteral, 2004 …reforestation: perspectives, design issues (grasshoppers, rainforest Kanowski ...Australian… crickets) Spiders Subtropical Australia cleared null Green, 1998 …fauna of Wivenhoe Park forest Catterall Spiders Temperate USA cleared increasing McIver, 1992 Litter spider succession… western forest Parsons coniferous Spiders Tropical Australia cleared regrowth = Dawes 2014 Impacts…termites and soil water open forest remnant storage…Australian savanna Spiders Tropical Brazil cultivated clear = (null?/ inverse complementary Lo-Man- 2008 …plantation forests for Neotropical epigeic (epigeic) rainforest regrowth reg = rem?) Hung, arachnids Gardner 1 Parentheses indicate trends inferred from graphs where formal tests for significant differences were not reported. Question marks indicate substantial uncertainty in the inferred model.

Page 25 of 31

Appendix B : Reptile species surveyed and known from the study site.

Thermal Number Rarity at Species 1 Family Habit 2 Habitats 5 source 3 surveyed study site 4 Ctenotus robustus Scincidae T, F H 96 very common All Heteronotia binoei Gekkonidae T T 70 very common All foliorum Scincidae T H 67 very common All Eremiascincus richardsonii Scincidae T, F T 51 very common All boulengeri Scincidae T, SA H 46 very common All steindachneri Gekkonidae T T 32 very common All williamsi Gekkonidae A T 12 very common re, ME, ra, MA Varanus gouldii Varanidae T, F H 3 very common ra, re burnsi T, A H 39 very common re, ME, ra, MA Ctenotus ingrami Scincidae T H 33 very common re, ME, ra, MA Diplodactylus vittatus Gekkonidae T T 22 very common re, ME, ra, MA Rhynchoedura ornata 6 Gekkonidae T T 19 very common All timida Scincidae F T 27 common c, re, ME, ra Ctenotus allotropis Scincidae T H 19 common c, re, ME, MA Egernia striolata Scincidae A H/T 17 common re, ME, ra, MA Amphibolurus nobbi 7 Agamidae SA H 14 common re, ME, ra, MA Parasuta dwyeri T, F T 9 common c, re, ME, MA Pseudechis australis Elapidae T, F H/T 3 common ra, MA Oedura monilis Gekkonidae A T 3 common ra Pogona barbata Agamidae T, SA H 2 common c, ra Cryptoblepharus spp. 8 Scincidae SA H 9 uncommon re, ME, ra Lerista punctatovittata Scincidae F T 8 uncommon re, ME, ra, MA Lialis burtonis Pygopodidae T T/H 5 uncommon re, ME, MA Vermicella annulata Elapidae F T 4 uncommon re, ME, ra Varanus tristis Varanidae A H 3 uncommon ME, MA Pseudonaja aspidorhyncha Elapidae T H/T 3 uncommon ME, MA australis Elapidae F T 2 uncommon re, ra Pygopus schraderi Pygopodidae T T 2 uncommon MA Pseudonaja textilis Elapidae T H/T 3 uncommon MA Furina diadema Elapidae T T 2 uncommon re, ra Ramphotyphlops spp. 9 Typhlopidae F T 3 rare re, MA greyii Scincidae T H 3 rare c Demansia psammophis Elapidae T H 1 rare re Paradelma orientalis Pygopodidae T, SA T 1 rare ME Not trapped (inferred reason) 10 Varanus varius (large) Varanidae A,T H - common - Suta suta (uncommon) Elapidae T, F T - uncommon - Acanthophis antarcticus Elapidae T T - uncommon - (uncommon, sedentary) Hoplocephalus bitorquatus Elapidae T, A T - uncommon - (uncommon) Gehyra dubia (rare) Gekkonidae A T - rare -

Page 26 of 31

Thermal Number Rarity at Species 1 Family Habit 2 Habitats 5 source 3 surveyed study site 4 Gehyra variegata (rare) Gekkonidae A T - rare - Ramphotyphlops ligatus Typhlopidae F T - rare - (rare) Tiliqua scincoides (rare) Scincidae T H - rare - Aspidites ramsayi (large, Pythonidae T, F T/H - rare - rare) Morelia spilota mcdowelli Pythonidae A, T T - rare - (large, rare) punctulatus A H - rare - (rare) Egernia rugosa (rare, Scincidae F, T H - rare - clumped distribution) Oedura marmorata (rare) Gekkonidae A T - rare - 1Species classification follows Wilson and Swan (2010). 2Habit = terrestrial (T), fossorial (F), arboreal (A), or semi-arboreal (SA) from Wilson and Knowles (1988) and Cogger (2000). 3H = Heliothermic, T = Thigmothermic 4Rarity was assessed using the quartile method of Gaston (1994) based on both road transect and trapping records at the study site from 2010-2012. 5Cleared (c), regrowth Eucalyptus (re), remnant Eucalyptus (ME), regrowth Acacia (ra), remnant Acacia (MA). 6Rhynchoedura ornata has recently been split into five species. The species found at the study site is likely to be Rhynochoedura ormsbyi (Pepper et al. 2011). 7Amphibolurus nobbi is now generally accepted as nobbi (Edwards and Melville 2011). 8Due to difficulties in field differentiation, the superficially similar Cryptoblepharus metallicus, C. pulcher and C. pannosus were grouped as Cryptoblepharus spp . 9The superficially similar blindsnakes Ramphotyphlops affinis and R. weidii were recorded as Ramphotyphlops spp . 10 The survey methods used in this study restricted captures of large, uncommon, and highly clumped reptile species.

References: Cogger, H.G., 2000. Reptiles & Amphibians of Australia. Reed New Holland, Sydney, Australia.

Edwards, D.L., Melville, J., 2011. Extensive phylogeographic and morphological diversity in Diporiphora nobbi (Agamidae) leads to a taxonomic review and a new species description. Journal of 45, 530-546.

Gaston, K.J., 1994. Rarity. Chapman and Hall, London.

Pepper, M., Doughty, P., Hutchinson, M.N., Keogh, J.S., 2011. Ancient drainages divide cryptic species in Australia's arid zone: morphological and multi-gene evidence for four new species of Beaked Geckos ( Rhynchoedura ). Molecular Phylogenetics and Evolution 61, 810-822.

Wilson, S., Swan, G., 2010. A Complete Guide to Reptiles of Australia, 3rd edn. New Holland Publishers Pty Ltd, Sydney.

Wilson, S.K., Knowles, D.G., 1988. Australia's Reptiles: A photographic reference to the terrestrial reptiles of Australia. Collins Publishers Australia, Sydney.

Page 27 of 31

Appendix C : Key structural features in regrowth and remnant Eucalyptus populnea - and Acacia catenulata -dominated woodlands at the study site. Structures are: a) canopy cover; b) fallen stems (woody debris); c) number of standing hollows; d) leaf litter cover; and e) shrub cover. Scores are the mean and standard errors for each habitat category with stars (*) indicating significant pairwise differences between regrowth and remnant for each woodland type.

Page 28 of 31

Appendix D : The proportion (%) of juvenile and adult individuals of each reptile species detected in each habitat type

Regrowth Remnant Remnant Acacia Remnant Acacia Cleared Eucalyptus Eucalyptus Regrowth Acacia (simple) (complex) Adult Juvenile Adult Juvenile Adult Juvenile Adult Juvenile Adult Juvenile Adult Juvenile Amphibolurus burnsi 0 0 0 10 1 9 1 21 4 43 0 57 Amphibolurus nobbi 0 0 2 5 1 3 4 13 0 0 0 4 Brachyurophis australis 0 0 1 0 0 0 1 0 0 0 0 0 Cryptoblepharus 0 0 1 0 0 3 0 0 2 13 5 0 Ctenotus allotropis 20 0 1 0 4 0 0 0 6 0 2 0 Ctenotus ingrami 0 0 2 10 1 0 12 13 13 4 11 4 Ctenotus robustus 47 79 12 31 0 9 4 0 0 17 4 0 Demansia psammophis 0 0 0 3 0 0 0 0 0 0 0 0 Diplodactylus vittatus 0 0 2 0 2 0 4 4 11 0 12 4 Egernia striolata 0 0 2 0 3 3 0 4 4 4 7 13 Eremiascincus richardsonii 4 0 3 5 15 21 14 29 4 9 2 0 Furina diadema 0 0 1 0 0 0 1 0 0 0 0 0 Heteronotia bynoei 0 2 13 8 14 3 23 0 23 0 14 0 Lerista punctatovittata 0 0 1 0 1 0 3 0 0 0 7 0 4 2 12 3 5 0 0 0 0 0 5 0 Lialis burtonis 0 0 2 0 1 0 0 0 0 0 2 0 Lucasium steindachneri 12 0 7 5 8 0 3 4 11 0 2 0 0 5 25 13 15 26 5 0 2 0 0 4 4 2 0 0 0 0 0 0 0 0 0 0 Morethia boulengeri 4 2 3 5 18 15 3 4 6 4 14 0 Oedura monilis 0 0 0 0 0 0 4 0 0 0 0 0 Paradelma orientalis 0 0 0 0 1 0 0 0 0 0 0 0 Parasuta dwyeri 0 2 0 3 0 6 0 0 4 0 2 9

Page 29 of 31

Regrowth Remnant Regrowth Remnant Acacia Remnant Acacia Cleared Eucalyptus Eucalyptus Acacia (simple) (complex) Adult Juvenile Adult Juvenile Adult Juvenile Adult Juvenile Adult Juvenile Adult Juvenile Pogona barbata 0 2 0 0 0 0 0 0 0 0 0 4 Pseudechis australis 0 0 0 0 0 0 1 0 0 0 4 0 Pseudonaja aspidorhyncha 0 0 0 0 1 0 0 0 4 0 0 0 Pseudonaja textilis 0 0 0 0 0 0 0 0 0 4 4 0 Pygopus schraderi 0 0 0 0 0 0 0 0 0 0 4 0 Ramphotyphlops 0 0 0 0 0 0 0 0 0 0 0 0 Rhynchoedura ornata 6 2 6 0 4 0 4 0 2 0 0 0 Strophurus williamsi 0 0 2 0 0 3 10 0 2 0 2 0 Varanus gouldii 0 0 1 0 0 0 0 8 0 0 0 0 Varanus tristis 0 0 0 0 1 0 0 0 0 0 0 0 Vermicella annulata 0 0 1 0 2 0 1 0 0 0 0 0 Total count: 51 42 122 39 93 34 73 24 47 23 57 23

Page 30 of 31

Page 31 of 31