CSIRO PUBLISHING
Australian Journal of Botany, 2017, 65, 38–57 http://dx.doi.org/10.1071/BT16148
A genetic, demographic and habitat evaluation of an endangered ephemeral species Xerothamnella herbacea from Australia’s Brigalow belt Alison Shapcott A,B, Robert W. Lamont A, Gabriel Conroy A, Heather E. James A and Yoko Shimizu-Kimura A A
Genecology Research Centre Faculty Science Health Education Engineering, University Sunshine Coast, Maroochydore DC, Qld 4558, Australia. B Corresponding author. Email
[email protected]
Abstract. Little remains of the Brigalow (Acacia harpophylla F.Muell. ex Benth.) woodlands of Australia, primarily due to land clearing for grazing and agriculture. Many threatened species in this region are poorly studied, and the life history traits of some herbaceous species such as ephemeral shoot systems, mean that conservation assessments are difficult. Recent gas pipeline developments have led to an increased need to understand the ecology and genetics of such taxa, in order to advise offset and translocation activities. Xerothamnella herbacea R.Baker is an endangered ephemeral herbaceous species from the Brigalow Belt region, which dies back during prolonged dry conditions. The aim of this study was to map the extent of potentially suitable habitat of this species, including determination of population extent within existing protected area estate. The species population sizes, reproductive activity and evidence of clonal spread, as well as the levels of genetic diversity and inbreeding, across the species range were also assessed to provide guidance for potential translocation and offsetting programs. The genetic results were related to the species suitable habitat distribution to test whether historic or recent habitat fragmentation most explains genetic patterns in this species. Most of the populations of this species were found to be small with less than 100 plants. The species appears not to be limited by its reproductive output, suggesting other factors may limit its abundance. The species populations have moderate to low genetic diversity suggesting the species is genetically viable in the medium term but are inbred which may be partially due to vegetative spread. Geographic proximity does not predict genetic similarity of populations and diversity is not correlated with population size. The results indicate potential translocation or offsetting programs need to account for genetic relationships in their planning. Resprouting ability has potentially assisted the species to slow the pace of genetic diversity loss due to anthropogenic fragmentation. Additional keywords: Acanthaceae, clonality, ephemeral species, genetic diversity, inbreeding, species distribution modelling, translocations. Received 15 July 2015, accepted 28 November 2016, published online 23 December 2016
Introduction Land use change has been identified as the major driver for rapid change in terrestrial ecosystems (Sala et al. 2000; Tscharntke et al. 2012). The subcoastal regions of South East Queensland Australia, have been extensively modified due to clearing primarily for cattle grazing (Accad and Neldner 2015). Of the once widespread woodland communities known as Brigalow and dominated by Acacia harpophylla F.Muell. ex Benth. in this region, only 10 percent now remain (Peeters and Butler 2014). Brigalow is defined by 16 different Regional Ecosystem (RE) types, all of which are classified as endangered (Queensland Vegetation Management Act 1999; Accad and Neldner 2015). Several herbaceous species listed as endangered or vulnerable are associated with Brigalow vegetation types, Journal compilation CSIRO 2017
but most are poorly known (Peeters and Butler 2014). The expansion of the coal seam gas industry transportation pipelines through this region has further impacted Brigalow communities, although these activities have also resulted in a rapid expansion of vegetation surveys as part of environmental impact assessments. This in turn has greatly increased knowledge of the distribution of many species but has also lead to an increased need to develop restoration and translocation methodologies for a suite of poorly known species (Shapcott et al. 2015). Success of translocations for threatened species will depend on knowledge of species’ habitat distribution, biology and ecology, genetic diversity and population dynamics (Godefroid et al. 2011; Weeks et al. 2011; Shapcott et al. 2015). Thus there is an urgent need to increase knowledge www.publish.csiro.au/journals/ajb
Xerothamnella herbacea
of these poorly known threatened species to minimise the impact of land use change. One poorly known species that was identified during gas pipeline surveys was Xerothamnella herbacea R.Baker (Acanthaceae), an endangered perennial herb endemic to South East Queensland (Environment Protection and Biodiversity Conservation Act 1999 and Nature Conservation Act 1992). At the time of commencement of the present study, X. herbacea was known from only four regions, with only two or three locations recorded in each: north-east of Chinchilla, east of Goondiwindi, and north-east of Theodore and recently it was found south- west of Theodore (Boobook 2012) where it was impacted by the Santos GLNG pipeline. Previous field observations suggested that the species may vegetatively spread to form clumps and suggest that it is found associated with moist depressions, and that it may die back during drier times of the year, hence making it easily missed in surveys (Boobook 2012). Flowers are small, whitish pink to mauve to 6.5 mm long (Barker 1986), the pollinators are unknown but are expected to be insects. The fruit was expected to be similar to its congener Xerothamnella parvifolia C.White, which has a 7–9 mm long capsule which splits revealing one or two seeds in each of the halves (Barker 1986). Acanthaceae typically have ballistic seed release that facilitates local dispersal (Morley and Toelken 1983; Balkwill and Balkwill 1998). However, some members in this family are known to have distinctive hairs on the seeds, which are sticky when wet, facilitating long distance dispersal by animals (Morley and Toelken 1983). In some Acanthaceae genera, species have highly restricted distributions often associated with specific soil types (Balkwill and Balkwill 1998). Soil moisture is limiting and rainfall is sporadic in the Brigalow Belt region (Tunstall and Connor 1981; Cowie et al. 2007). Many arid and rangeland herbaceous flora are ephemeral in the landscape, potentially responding to moisture (Silcock and Fensham 2013; Silcock et al. 2014). Previous preliminary field observations suggested X. herbacea populations may die back and it was unknown if regeneration is primarily from seed or resprouting from dormant adult plants (Boobook 2012). However, many herbaceous and grassland species are thought to be dispersal limited (Vanden Broeck et al. 2015). These factors combined have implications for the species landscape distribution and connectivity of populations over time, which highlights the importance of understanding its potential habitat distribution and genetic diversity. Planning knowledge of the location extent and past connectivity of populations is crucial for conservation and translocation, particularly to reduce the potential for outbreeding depression (Godefroid et al. 2011; Weeks et al. 2011). Species distribution models (SDM) can be relatively accurate for modelling spatio-temporal habitat distribution of species with few documented populations (Pearson et al. 2007; Franklin 2013). Geographic projections of species distribution models are a cost effective approach that can be used to target areas for searching for additional populations, or identification of suitable areas for reintroduction (Pfab and Witkowski 1997; Powell et al. 2005). Species distribution models have also been used to assist with interpreting the patterns of genetic differentiation and diversity in endangered species particularly in fragmented landscapes (Shapcott et al. 2012; Thode et al. 2014). For poorly known
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species such as X. herbacea that occur in highly fragmented landscapes, quantification of how much of the species potential range may have been already cleared or degraded, as well how much remains and is protected, is important for conservation and recovery planning, particularly where there is the threat of future development activities in the region. Habitat fragmentation may alter plant reproductive processes by reducing the size of plant and pollinator populations and altering the spatial arrangement of populations leading to declines in outcrossing and reproductive output (Coates et al. 2007; Zhang et al. 2012; Menz et al. 2015). Plant populations that are too small or isolated to receive pollinator services experience the Allee effect where there is a disproportionate decline in reproduction with a decline in population size (Lamont et al. 1993; Ghazoul 2005). Thus demographic estimates for X. herbacea are important to gain some appreciation of the relative threats to the species and for designing recovery and or translocation programs that mimic natural population demographic processes. Flowering of X. herbacea congener, X. parvifolia (Vulnerable), is reported to be opportunistic depending on rainfall (Barker 1986). If X. herbacea reproduction is also linked to rainfall events it is unlikely that reproduction would be synchronous across the landscape except at a local scale, reducing the potential for pollinators to move between populations and hence reducing gene flow potential. Thus, gaining some estimates of population size and reproductive activity are important for assessing both the short-term population viability threats to X. herbacea, as well as longer-term threats particularly for potential recovery and translocation planning. Many plant species are potentially locally adapted over a range of geographic scales (McKay et al. 2005). Thus, if translocated plants are added to existing populations as part of an offset program there is the potential for the dilution of localised adaptations via genetic swamping, as well as other negative consequences such as outbreeding depression (Weeks et al. 2011). As there was no information of genetics of this or related species, local managers were interested in gaining genetic knowledge of X. herbacea so that any potential recovery or translocation actions could be appropriately designed. Clonal growth is common in herbaceous woodland species and is seen as an adaptation to patchy environments and reducing the risk of loss of genetic diversity in disturbed environments (Whigham and Chapa 1999). Whilst X. herbacea has been observed to spread vegetatively it is unknown if there is extensive clonal growth in this species that may impact on the genetic diversity or reproductive success of populations, which could be an important consideration for conservation assessments and potential offsetting, translocation or reintroduction programs. Before this study, little was known about X. herbacea reproductive ecology demographics or genetics that would enable assessment to be made regarding its long-term viability and the potential impacts of proposed developments on the local population and species as a whole. Surveys associated with gas pipeline development found new populations well to the north of previous records, making it difficult to predict where the species may be encountered or how well it may be conserved within the protected area estate. Therefore the aim of this study was to develop species distribution models (SDM) for X. herbacea and to map the extent of potentially suitable habitat of this species,
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comparing this with the distribution of specific Brigalow vegetation types that the species has previously been associated with, and to assess proportion of its populations and potential suitable habitat occurring within the existing protected area estate. Given the lack of knowledge about the species abundance and viability, the study also aimed to determine the species population sizes and reproductive activity at the time of sampling across its known distribution and test for evidence of clonal spread. In order to assess long-term species and population viability, the study also aimed to estimate the levels of genetic diversity within and among populations and levels of inbreeding across the species range, which would also enable guidance for potential translocation and offsetting programs, and to relate the genetic patterns observed to the species suitable habitat distribution to test whether historic or recent habitat fragmentation most explains genetic patterns in this species. Materials and methods Species distribution modelling Xerothamnella herbacea R.Baker occurrence data was compiled from historical presence database (Queensland Herbrecs database) field survey records from this study, as well as Boobook (http://www.boobook.biz/, accessed 20 January 2014) and Santos GNLG (http://www.santosglng.com/ , accessed 21 January 2014) survey records. The presence records of X. herbacea were classified into (1) the historical known distribution of X. herbacea (any presence information dated before 2000), and (2) updated, latest currently known distribution of X. herbacea (any presence information reported since 2000), and visualised in order to assess changes in distribution of the species since the 1990s. The latest presence information obtained from a field survey conducted in June and July 2014 as part of this study was added to this analysis. To avoid model oversampling, any duplicated species presence points within a 100 100 m grid area were omitted. A total of 37 presence points were thus used as X. herbacea presence data in this study. It should be noted that these 37 georeferenced presence points do not necessarily translate to separate populations on the ground but indicate the recorded geographic distribution of the species from a variety of sources. The modelling was confined to the south-east Queensland region utilising the available mapping layers for this region. We selected 24 variables as the potential predictors, which included 19 climatic variables and five environmental variables such as elevation, slope, aspect, land zone, and geology. Nineteen bioclimatic surface layers (BIOCLIM) were derived from ANUCLIM ver. 6.1 (Xu and Hutchinson 2013) at 250 250 m grid resolution. A 25 25 m grid resolution elevation dataset (digital elevation model; DEM) was used to generate slope and aspect layers. We used the current regional ecosystem (RE) dataset layer (2013) to derive land zone information, and a Queensland geology dataset containing dominant rock substrate information. All bioclimatic and environmental datasets were re-sampled to a 100 100 m grid resolution before modelling analysis. Prior to modelling analysis, A 100 100 m grid resolution DEM was used to re-sample all bioclimatic and environmental datasets in ArcGIS ver. 10.2 (Esri).
A. Shapcott et al.
We chose MAXENT (Phillips et al. 2006) to model the habitat distribution of X. herbacea. It has been successfully applied to a wide range of ecological modelling applications, and has been found to be a robust approach for modelling species distributions under both current and future environments (Phillips et al. 2006; Kearney et al. 2010; Hill et al. 2012; Nazeri et al. 2012). In order to test multicollinearity, we conducted cross-correlation analysis on all parameter variables using Spearman’s rank correlation analysis in SPSS ver. 21 (SPSS Inc.), with a threshold of R >0.80 used to indicate a significant relationship. For significantly correlated pairs of variables, the variable that made the least or no contribution to the model performance and prediction was omitted according to the MAXENT jack knife test results. The final model was run at a spatial resolution of 100 100 m with 5-fold cross validation. The program was run with 500 iterations and the logistic output format, which represents the probability of occurrence of the target species within the range of 0 to 1.0 for each grid cell in the model (Phillips and Dudik 2008). Model performance was evaluated by the area under the curve (AUC) in receiver operating characteristic analysis (ROC) of the cross validated model output. An AUC score of 1.0 indicates a statistically valid, perfect model fitting, while an AUC value of 0.6 indicate good predictions; 0.2–0.6 indicates fair predictions; and values 0.75) and only 4.1 percent of the area of medium suitability (20 981.5 km2; P = 0.29–0.75: Fig. 1). The species potential suitable habitat map concurs with records indicating that X. herbacea is found in broad geographic clusters but also indicates significant differences in extent among these (Fig. 1). The newly discovered northern populations are located within the largest area of suitable habitat for this species particularly north-east of Theodore, and the extent of this suitable habitat suggests there may yet be considerable areas where populations could yet be discovered (Fig. 1). There is a more southern significant area of suitable habitat in the Chinchilla region where some of the extant populations have been recorded (Fig. 1). The most southern cluster of populations in the Goondiwindi region is at the southern end of the species limits where there is little potentially suitable habitat (Fig. 1). The projection maps indicate considerable fine scale habitat preferences within the area of extent indicating potential for populations to be naturally scattered within the landscape with relatively few larger areas of continuous suitable habitat (Fig. 1). Although most known populations were located within the larger areas of suitable habitat, the presence of populations within some of these very small scattered areas of suitable habitat indicates the potential for the species to occur in small stepping stone populations that could facilitate gene flow. X. herbacea suitable habitat was found to occur in seven RE types associated with Brigalow five of which are endangered and specifically associated with A. harpophylla, 22% of the area being RE type 11.9.5 (Table 2). Although the pre-clearing distribution of these combined Brigalow (RE) vegetation types
was already quite restricted, they now only exist as tiny fragments scattered across the study area (Fig. 2). Previous species descriptions identified the species as endemic to Brigalow however, our analysis of the current presence records indicated that the majority (65%) of highly suitable species habitat was found where other RE types had been mapped (Table 2). It can also be seen that considerable areas of potentially suitable habitat for this species do not coincide with any of these Brigalow vegetation types based on the preclearing data (Figs 1, 2). The results suggest that this species is not strongly associated with RE type and that the habitat model is a better estimate of potential distribution than RE mapping alone (Figs 1, 2). Although ~15 percent (3347.3 km2) of the area identified as potentially suitable habitat X. herbacea is currently located within the protected area estate, only seven of the recorded presence sites are currently conserved within protected areas (Fig. 3). The largest areas of potentially suitable habitat in the protected area estate were within state forest (Barakula SF 529.5 Ha; 15.82%: Belington Hut SF 491.5 Ha; 14.68%). The national parks with the largest areas were Carnarvon NP (8.64%) and Expedition NP (8.10%) where three known populations are located. Population size and extent We found evidence of population flush and decline in response to rainfall events and availability of moisture as at least two recently reported populations that were identified after regional rainfall (Boobook 2012) were not relocated upon visiting. One appeared to have declined due to dry conditions, and the other due to a combination of habitat damage due to cattle grazing and dry conditions. Our study confirms the presence of twelve extant populations of X. herbacea at the time of study with an
Table 2. A list of Regional Ecosystem (RE) types which were identified to accommodate currently known Xerothamnella herbacea populations based on the vegetation regional ecosystem (RE) dataset of Queensland and the Regional Ecosystem Description Database (REDD) ver. 8.1 (Queensland Herbarium 2014) Area abundance of each RE type within the species’ high quality habitat is given in km2 and percentage in parentheses. Area abundance of other RE types within the species’ high quality habitat is also given (other RE types and non-remnant) Dominant RE type
RE description
Biodiversity status
Area cover km2 (%)
11.9.5
Acacia harpophylla and/or Casuarina cristata open forest on fine-grained sedimentary rocks. In 2013, 10 000 ha and >30% of the pre-clearing area remained Corymbia citriodora woodland on coarse-grained sedimentary rocks Acacia harpophylla–Eucalyptus cambageana woodland to open forest on finegrained sedimentary rocks. In 2013, 0.05) correlated with patch size (Rho = 0.505) or density (Rho = 0.088). Some of the differences may be due to variation among regions in the timing of reproduction as while the Lonesome populations were predominantly in flower at the time of sampling, fewer plants ( 0.05; Rho 0.05; Rho
