A stitch in time – Synergistic impacts to platypus metapopulation extinction risk

Biological Conservation 242 (2020) 108399

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Biological Conservation journal homepage: www.elsevier.com/locate/biocon

A stitch in time – Synergistic impacts to platypus metapopulation extinction risk

T

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Gilad Binoa, , Richard T. Kingsforda, Brendan A. Wintleb a b

Centre for Ecosystem Science, School of Biological, Earth & Environmental Sciences, UNSW Sydney, NSW 2052, Australia School of Biosciences, University of Melbourne, Victoria 3010, Australia

A R T I C LE I N FO

A B S T R A C T

Keywords: Freshwater ecosystems Population viability analysis River regulation Habitat loss Species distribution model IUCN red listing RAMAS GIS

The unique platypus is currently listed as ‘Near-Threatened’ under the IUCN Red List based on observed population declines and local extinctions, though significant uncertainty exists about its current distribution and abundance. We did the first population viability analysis across its entire range, using distribution and metapopulation data and models that integrate key threatening processes. We quantified the individual and synergistic impacts of water resource development, land clearing and invasive species on population viability of the platypus. Under current climate and threats, platypus abundance and metapopulation occupancy were predicted to respectively decline by 47%–66% and 22%–32% over 50 years. This would cause extinction of local populations across about 40% of the range. Under climate change projections (2070), increased extreme drought frequencies and duration were predicted to further expose platypuses to increased local extinctions, reducing abundance and metapopulation occupancy by 51–73% and 36–56% within 50 years respectively. Predicted estimates of key threatening processes on platypus populations strongly suggested increased risk of extinction, including listing as ‘Vulnerable’, under IUCN criterion A. This adds to the increasing evidence of decline and local extinction of platypus populations. There is an urgent need to implement national conservation efforts for this unique mammal by increasing surveys, tracking trends, mitigating threats and improving management of platypus habitat in rivers.

1. Introduction Global loss of biodiversity, with rates parallel to past global mass extinction (Barnosky et al., 2011; Ceballos et al., 2017), are impacting ecosystems at local and regional scales (Rockström et al., 2009). Over a million species are currently threatened with extinction (IPBES, 2019). Given their reactive nature, conservation efforts, including monitoring, assessments, and actions are frequently focused towards the rarer species or those with narrower ranges (Gaston, 2010), at relative high cost and lower likelihood of conservation success (Lindenmayer et al., 2011; Resende et al., 2019). Although there is no doubt that endemic species and those with narrow distributions have high extinction risks (Urban, 2015), more widespread species should also be a subjected to extinction risk assessment for five reasons. First, widespread species are also declining around the world (Gaston and Fuller, 2008; Inger et al., 2015; Kamp et al., 2015). Second, they can be useful indicators of ecosystem degradation, critical for conservation (Cunningham and Olsen, 2009; Chapman et al., 2018). Third, comprehensive (i.e. multi-species) and cost effective conservation frameworks have been developed by

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considering widespread species (Maxwell and Jennings, 2005; Neeson et al., 2018). Fourth, widespread species deliver most ecosystem services (Winfree et al., 2015) in terms of structure, biomass and energy turnover (Gaston and Fuller, 2008), with small proportional declines significantly impacting on ecosystem function (Ellison et al., 2005; Gaston, 2010). Finally, many widespread species are evolutionarily distinct, requiring investment in assessment to minimise extinction risk (Isaac and Pearse, 2018). The platypus (Ornithorhynchus anatinus) is one such evolutionarily distinct species, considered widespread across the eastern Australian mainland and Tasmania (Bino et al., 2019). There is a considerable lack of knowledge about its distribution and abundance. Estimates of population sizes are difficult to obtain, given low recapture rates despite significant effort (Grant, 2004; Serena and Williams, 2012). Recent local declines and extinctions, particularly in the state of Victoria, highlight a species facing considerable risks (Lunney et al., 2008; Serena and Williams, 2010b; Woinarski et al., 2014). The species was only listed on the IUCN Red List as ‘Near Threatened’ in 2016, up from ‘Least Concern’ (Woinarski and Burbidge, 2016) but remains unlisted

Corresponding author. E-mail address: [email protected] (G. Bino).

https://doi.org/10.1016/j.biocon.2019.108399 Received 23 July 2019; Received in revised form 10 December 2019; Accepted 26 December 2019 0006-3207/ © 2020 Elsevier Ltd. All rights reserved.

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the analysis in cells containing platypus observations for three highly invasive species; the European carp (Cyprinus carpio, first Atlas record 1878), the red fox (Vulpes vulpes, first Atlas record 1770) and domestic cat (Felis catus, first Atlas record 1770) and one native freshwater mammal, the rakali (Hydromys chrysogaster, first Atlas record 1837) with similar habits to platypus. For each species, we compiled the full record and identified the last year of record for each of the 356 cells. We defined ‘loss of record continuity’ as the year after which a cell no subsequent sighting and calculated the annual proportion of cells with loss of record continuity. We analysed and compared loss of record continuity between species using the Cox proportional hazards regression model, starting from 1960 with for each of the 356 cells across the five species. We analysed data using the “coxph” function in the ‘surival’ package (Therneau, 2015) within the R environment (R Core Team, 2018). We also calculated extinction probability using the records of platypus sightings (0,1) in each of the 356 cells (50kmx50km) between 1950 and 2017, and applying a Bayesian formulation developed by Caley and Barry (2014), building on the approach by Solow (1993) within the R environment (R Development Core Team, 2018). We assumed non-constant probabilities of detection and population persistence prior to extinction, as outlined in Caley and Barry (2014). We used uninformed rates of population growth with a uniform distribution between −2.3 and 0.69 and similarly uninformative uniform rate of detection between 0.01 and 4.6. We ran a MCMC sampler with a Metropolis-Hastings step for 1 million iterations, after a “burn-in” period of 100,000 iterations without thinning of chains. To model habitat suitability of platypuses, we used the Biodiversity & Climate Change Virtual Lab and the Maximum Entropy Species Distribution Modelling approach (Phillips and Dudík, 2008). To increase model accuracy, we excluded platypus records from the Atlas databases (n = 11,830) with a spatial accuracy less precise than 10 km (n = 1992), leaving us with 9838 occurrence records (1760–2017), which we spatially aligned to the nearest stream (Stein et al., 2014). We then randomly generated an equal number of background pseudo-absences (Barbet-Massin et al., 2012). We considered eight explanatory variables (Appendix 1), biologically relevant to platypus and based on the stream and nested catchment framework for Australia (Stein et al., 2014). These included four environmental variables of contemporary climate (temperature and precipitation; 1921–1995 (Xu and Hutchinson, 2013)), two terrain variables (stream order and elevation), (Hutchinson et al., 2008), and two pre-1750 tree cover variables (Australian Government, 2006). Our rationale for including temperature was based on the species' thermal tolerance (Robinson, 1954) and for precipitation on its dependence on freshwater habitats (Bino et al., 2019). We included terrain variables, given the species' habitat preferences to mid and lower river reaches (Serena et al., 1998; Turnbull, 1998; Rohweder and Baverstock, 1999; Serena et al., 2001; Koch et al., 2006; Olsson Herrin, 2009; Macgregor et al., 2015). We also incorporated tree cover, as riparian trees provide shelter, burrows and organic matter for prey while cleared areas increase erosion and sedimentation of rivers (Rohweder, 1992; Bryant, 1993; Ellem et al., 1998; Serena et al., 2001; Milione and Harding, 2009). Predictive performance of the platypus distribution model was evaluated using the area under the receiver operating characteristic curve (AUC) and Cohen's Kappa using a ten-fold cross-validation analysis (Stockwell, 1992; Fielding and Bell, 1997; Hijmans, 2012).

under most jurisdictional legislation in Australia and nationally, except South Australia, where it is endangered (South Australia, National Parks and Wildlife Act 1972). Its distribution coincides with Australia's major threatening processes (Kingsford et al., 2009) including highly regulated and fragmented rivers (Kingsford, 2000; Grant and Fanning, 2007); other habitat degradation by agriculture, forestry, mining, and urbanisation (Grant and Temple-Smith, 2003); by-catch mortality in fishing gear (Grant and Fanning, 2007; Serena and Williams, 2010a); and predation by invasive foxes and feral dogs (Connolly et al., 1998). There is an urgent need for a national-scale risk assessment for the platypus to support understanding of its conservation status, evaluate impacts and prioritise their management to minimise extinction risk. We used population viability analysis (PVA) to quantify extinction risk and assessment of conservation status (Burgman et al., 1993). PVA also allowed assessment of the impacts of threats and benefits of conservation actions, specific to different life stages (Fox et al., 2004). It explicitly treats uncertainty, under exploratory or intervention scenarios (Chisholm and Wintle, 2007; Southwell et al., 2008), simulating temporal variation in patch (or population) occupancy, while integrating survival, fecundity and dispersal variability among patches (Akçakaya and Raphael, 1998). Incorporating metapopulation processes, including range movements and dispersal within PVA accounts for impacts of fragmentation on extinction risks (Hanski, 1998). Metapopulation models are used extensively to assess extinction risk for terrestrial mammals (Southwell et al., 2008), insects (Schtickzelle and Baguette, 2004), bird (Akçakaya et al., 2004) and plants (Lyngdoh et al., 2018). Organisms living in riverine systems present particular challenges, given the unique dendritic spatial structure of rivers, constraining population dynamics and affecting abundance, distribution and metapopulation structure (Campbell Grant et al., 2007; Labonne et al., 2008; Mari et al., 2014; Terui et al., 2018). We investigated the extinction risk of platypus across their entire distribution by collating existing knowledge of the species' distribution and life history and building the first metapopulation model across its full range using a dendritic metapopulation structure which represented their river habitat. We evaluated population viability from key threatening processes, including habitat degradation by land clearing, fragmentation by dams, competition and predation by invasive species, and historic rates of drought as well as those predicted under climate change. We assessed our results of population and distribution change using IUCN extinction risk criteria (IUCN, 2017) to assess extinction risk and identify threats, providing a focus for conservation efforts (Collar, 1996; Rodrigues et al., 2006). We also highlight key knowledge gaps and actions essential for the conservation of this globally unique species. 2. Methods 2.1. Platypus distribution We collated 11,830 platypus observations (1760–2017) from the national Atlas of Living Australia (www.ala.org.au) and atlas records held by individual states and territories (ACT Wildlife Atlas Records, 2018; BioNet Atlas of NSW Wildlife, 2018; Tasmania Natural Values Atlas, 2018; Victorian Biodiversity Atlas, 2018; WildNet Queensland Wildlife Data, 2018), the most systematic compilation of observations. We also included another 184 historical records from digitized newspaper records (Hawke et al., 2019b). We removed records with missing years of sighting and duplicates (matching coordinates and year of sighting). To include historical records of platypus observations with low resolution, we examined the occurrence and prevalence of platypus records within a 50 km × 50 km grid (n = 356 cells), a sufficient size to avoid resampling of individuals given area of occupancy for platypuses does not normally exceed 10 km (Bino et al., 2019), (Fig. 1). As accumulation of records within atlas databases is uneven across time and space, we also compared observed trends in gain and loss of distribution by replicating

2.2. Platypus densities To derive estimates of population density for the metapopulation models, we linearly scaled the modelled predicted probability of occurrence between observed maximum and minimum platypus densities (km−1). Existing estimates of platypus densities varied from 1.3–2.1 km−1 along Badger Creek in the Yarra River tributary, Victoria (Serena, 1994); 2.8 km−1 in the Shoalhaven River, New South Wales 2

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Fig. 1. a) Year of last platypus sighting, amalgamated into 50X50km cells, based on 11,830 platypus observations (1760–2017) from the Atlas of Living Australia (www.ala.org.au) and atlas records held by individual states and territories (ACT Wildlife Atlas Records, 2018; BioNet Atlas of NSW Wildlife, 2018; Tasmania Natural Values Atlas, 2018; Victorian Biodiversity Atlas, 2018; WildNet Queensland Wildlife Data, 2018) and b) probability of extinction using a Bayesian formulation, along with demarcated catchments (grey), basins (black) and the platypus' current IUCN geographic range.

(Bino et al., 2015); 3–7 km−1 in Tasmania (Koch et al., 2001); and 1.3–3.6 km−1 in Kangaroo Island, South Australia (Serena and Williams, 1997). To avoid underestimation and provide an upper measure of average platypus densities, we assumed a density of 4 km−1 in areas of high environmental suitability, where the relative likelihood of occurrence predicted by the Maxent models was P = 1.0 and scaled down as the likelihood of occurrence declined.

average land area of 1231km2 ± 985sd. 2.4. Connectivity and dispersal To quantify connectivity between platypus population units, we used the Australia Hydrologic Geo-Fabric (AHGF) stream network, based on the GEODATA Nine Second Digital Elevation Model (DEM-9S) Version 3 (Hutchinson et al., 2008). The built-in Network Analyst in ArcMap (ESRI, 2010) was the analytical framework for the river network, providing estimates of distances along the stream network and between platypus population units. We used the distance between populations along the stream network to calculate emigration potential, where annual stage-dependant dispersal rate was P = 0.25 for individuals (male juvenile P = 0.12, female juvenile P = 0.04, male adult P = 0.06, female adult P = 0.04) (Fox et al., 2004; Bino et al., 2015). We explored sensitivity of dispersal estimates by assessing variation of ± 20% in dispersal rates (Appendix 5). Adjacent population units along the river network were assigned a zero distance, recognising their probable connectivity, with equal probabilities assigned for up or downstream dispersal (Bino et al., 2019). For non-adjacent population units along the river network, emigration potential (A) was calculated using a dispersal distance function based on the assumption that average dispersal was 2 km and maximum dispersal was 18 km, based on field data (Bino et al., 2019):

2.3. Metapopulation structure There are many approaches to modelling population viability, tailored for specific needs and scales, broadly grouped to Individual Based Models and discrete population-based models (Lacy, 2019). We chose to use the RAMAS GIS (Akçakaya and Root, 2013) to construct a metapopulation dynamic model of platypus populations. Our decision was based on the capacity of RAMAS GIS to consider the spatial structure of many different populations while integrating the effects of habitat fragmentation and other threatening processes at a continental scale. Given platypus are obligate freshwater animals almost exclusively confined to rivers (Bino et al., 2019), we used river catchments as the scale for analysis. We used the HydroBASINS framework (Lehner and Grill, 2013), which divided basins into sub-basins at every location where two river branches met, each with an upstream area of at least 100 km2, continuing further with subsequent subdivisions (Verdin and Verdin, 1999). We used the seventh sub-basin level (Fig. 2), producing 775 potential areas where platypuses occur (hereafter population units), overlapping with the platypus suitability map, encompassing an average of 156 km ± 180sd (range 0.02–1442 km) of major rivers and 1105 km ± 1394sd (range 0.06–9178 km) of minor rivers, with an average land area of 2460km2 ± 2663sd. Given the computational limitations of the software we did not used the eight sub-basin level which would have produced over 6000 populations units with an

−x

⎛ e10 ⎞ A = 0.25∙ ⎜ N −x ⎟ ⎝ ∑i e10 ⎠ where x was the distance [km] between population units (N) along the stream network. Platypuses sometimes disperse overland, but no knowledge exists with regards to rates or success (Kolomyjec et al., 2009; Gongora et al., 3

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Fig. 2. Tree (tall trees > 30 m, medium trees < 20 m, low trees < 10 m) cover change since European colonisation of Australia (shaded) (Geoscience Australia, 2003a; Geoscience Australia, 2003b), dams (black circle, wall height categorised by diameter) (Geoscience Australia, 2004), platypus population units based on 7-th level HydroBASINS (Lehner and Grill, 2013), and river basins.

2.5. Life history

2012; Martin et al., 2018). Given the computational impracticality of calculating every distance between stream ends in the upper catchments, across to different catchments (i.e., over a ridge line) due to the large number of pairs, we assumed that populations with shared overland boundaries (not along the river network) were permeable to low level overland dispersal. We conservatively assumed 1% of total dispersal (P = 0.0025) was overland, calculated proportionally to each of the adjacent population units, given actual rates of overland dispersal were not clear but likely low (Kolomyjec et al., 2009; Furlan et al., 2013). We explored sensitivity of dispersal estimates by assessing variation of ± 20% in dispersal rates (Appendix 5). This low level of dispersal is only likely to be relevant when inbreeding was explicitly considered in the model.

We used a stage-structured population model with values for survival, fecundity, and the probabilities of transition from each life history stage. We assumed a four-stage population structure: females\male and juvenile\adult. Sexual maturity of female platypuses was presumed to start at two years given male platypuses do not produce functional spermatozoa until their second year when they can probably breed (Temple-Smith, 1973; Grant and Temple–Smith 1998b). One to three offspring are produced by a female during a breeding season (Burrell, 1927; Grant, 1995), although not every female breeds every year (Grant et al., 1983; Grant, 2004; Bino et al., 2015). Annual fecundity (F) was accordingly calculated as: 4

5

5

4

3

2

1

X

X

X

X X X X X

X

Mining

X

X

X

X

Fisheries

X

X

X X X

X X

Urbanisation

X

X

X

X

Invasive species

X

X

X

X X

X

X X

Climate change

Grant, T.R. and Bishop, K.A. 1998. Instream flow requirements for the platypus (Ornithorhynchus anatinus) - a review. Australian Mammalogy 20: 267–280. Grant, T.R. (2015). Family Ornithorhynchidae (Platypus). pp. 58–67 in: Wilson, D.E. and Mittermeier, R.A. eds. Handbook of the Mammals of the World. Vol. 5. Monotremes and Marsupials. Lynx Edicions. Barcelona. Bino, G., Kingsford, R.T., Archer, M., Connolly, J.H., Day, J., Dias, K., … Whittington, C. (2019) The platypus: evolutionary history, biology, and an uncertain future. Journal of Mammalogy, 100, 308–327. Grant, T.R. and Temple-Smith, P.D. 2003. Conservation of the platypus, Ornithorhynchus anatinus: threats and challenges. Aquatic Health and Management 6, 1–18. Woinarski, C.Z., Burbidge, A.A. and Harrison, P.L. 2014. The Action Plan for Australian Mammals 2012. CSIRO Publishing, Collingwood.

X

X

X X

X X

X X X X X

X X X X X

X

X

X

X

X X

X X

Reduced availability of foraging habitat Barriers to juvenile dispersal and gene flow (including overland) Reduced drought refugia Change to prey species communities (macroinvertebrates) due to: • Increased sediment run-off and sedimentation • Increased salinity • Decreased benthic heterogeneity • Pollutants and rubbish in run-off and stormwater • Removal riparian vegetation (loss of shading, litter and woody debris) • Cold water release flows Damage to burrowing banks by high flows, livestock access, construction Mortality from fish/crayfish traps, nets and fishing hooks and lines Predation by foxes, dogs and cats, including greater exposure in shallow waters and between refuge pools in reduced flows Thermoregulatory stress due to: • Cold water release • Decreased availability of temperature buffering burrows/shelters • Extreme air/water temperatures (over 30 °C thermal tolerance) Resource competition (especially salmonid fish species and possibly carp) Infectious disease

Water body Normally continuous water course, including riffles, runs, pools and lakes providing a foraging resource (predominantly benthic macroinvertebrates) Riparian margins Normally consolidated by vegetation (often overhanging) providing burrows or shelters for nesting, resting and avoidance of temperature extremes, shading of the water body and input of organic materials and woody debris to the water body

Agriculture

Water management

Effects3,4,5

Critical habitat requirements1,2,3

Table 1 Threatening and limiting processes of platypus population viability, identified through a literature review and a workshop of platypus researchers and managers (31/7/2017).

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impact to population carrying capacity. We also tested the sensitivity of models by examining a systematic reduction of carrying capacity at 20% increments (20%–80%) across all populations. We also assessed the impacts of severe natural droughts, incorporated as ‘catastrophes’ in our meta-population models. These were periods of prolonged extreme drought (CSIRO and Bureau of Meteorology, 2015), when refugia can dry up, causing loss of habitat and prey availability (Marchant and Grant, 2015), increased fragmentation and predation risk (Bino et al., 2019). We incorporated past and future climate, across the platypus's range, using the Australian Natural Resource Management (NRM) units (CSIRO and Bureau of Meteorology, 2015). Across NRM units, between 1975 and 1995, there were a median of 0.9–1.5 extreme droughts, with a median duration of 22–38 months across the platypus' range (CSIRO and Bureau of Meteorology, 2015). We calculated annual historical probabilities of these extreme droughts and explored a range of impacts in our metapopulation models of 10%, 20% and 30% on platypus mortality. We also analysed projected impacts of climate change (Representative Concentration Pathway (RCP) 2.6, 4.5, 8.5), on median frequency of extreme drought events, projected to increase in frequency (55%–320%) and duration (4%–38%) across NRM regions by 2070 (CSIRO and Bureau of Meteorology, 2015) and similarly explored a range of impacts in our metapopulation models of 10%, 20% and 30% on platypus mortality. To establish a baseline scenario, we first simulated 1000 replicates of metapopulation dynamics for 200 years to achieve an equilibrium, using RAMAS GIS 5.1 (Akçakaya and Root, 2013). We then used baseline results to simulate population dynamics and metapopulation occupancy, as a measure of extinction risk, following several scenarios of threatening processes. For each scenario, we ran 1000 replicates for 200 years. We used the same set of initial population sizes for all simulated scenarios. We evaluated impacts on populations, based on population occupancy (number of populations with platypuses) and Effective Minimum Population (EMP), a widely used metric for species' recovery and conservation management programs (McCarthy and Thompson, 2001; Clark et al., 2002), although it may not sufficiently measure long-term persistence and evolutionary potential (Trail et al., 2010). We evaluated the sensitivity of our model assumptions on metapopulation occupancy and EMP on our baseline models, following 200 years of simulation by varying the maximum growth rate (Rmax) by ± 5% and the stage matrix estimates (survival and fecundity) by ± 10%. We also examined the effect of reducing the number of females a male can mate with from three to two.

F = 1.5(average young)·0.5(proportion of females)· 0.62(females in the breeding pool) = 0.47 We assumed a polygynous mating system, where each male can mate with up to 3 females. Platypuses can live to at least 21 years in the wild, though most individuals die younger (Grant, 2004; Serena et al., 2014). We derived annual, stage-dependant, survival rates (Fox et al., 2004; Bino et al., 2015; Bino et al., 2019), with variation (sd) on vital rates assumed to be 10% for fecundities and 5% for survival (Table 2). Density dependence was assumed to be a contest and affect both survival and fecundity (Beverton and Holt, 1957). Under these assumptions, growth rate (lambda) was 1.0232.

2.6. Incorporating threats to metapopulation models We identified potential threats from the available literature and platypus experts, actively publishing on platypus conservation and ecology, producing seven major threatening processes (Table 1), with a focus on fragmentation (by dams and invasive species) and reduced carrying capacity. We also considered increased likelihood of droughts, projected by climate change, given increasing concern that waterhole refugia may be more vulnerable (Bino et al., 2019). To examine possible fragmentation by large dams (Nilsson et al., 2005), we assumed dams with a wall height > 5 m (Geoscience Australia, 2004) impeded movement of platypuses along the river network between population units. With regards to limitations to platypus overland dispersal, there is anecdotal evidence that invasive red foxes (Vulpes vulpes) and cats (Felis catus) prey on platypuses, particularly when moving overland (Grant and Temple-Smith, 2003). We collated 65,827 fox and 13,469 cat observations (1760–2017) from the national Atlas of Living Australia (www.ala.org.au) and atlas records held by individual states and territories (ACT Wildlife Atlas Records, 2018; BioNet Atlas of NSW Wildlife, 2018; Tasmania Natural Values Atlas, 2018; Victorian Biodiversity Atlas, 2018; WildNet Queensland Wildlife Data, 2018). Fox and feral cat sightings were recorded respectively in 231 sub-catchments (88%) and 335 cells (92%) and 231 sub-catchments (87%) and 335 cells (94%), where platypus records occurred, effectively the species' entire distribution. Land clearing and modification also increases predation rates, thermal exposure, erosion and sedimentation as well as forming physical barriers, further limiting overland dispersal (Bino et al., 2019). Physical degradation of platypus habitat occurs by clearing both riparian and catchment-scale vegetation, increasing bank erosion, destroying shelters and burrows for breeding, with sedimentation filling pools and reducing food availability (Table 1). To assess the impact of this habitat degradation, we used the proportion of remnant trees as the impact on population carrying capacity (Fig. 2). To derive an estimate of habitat loss and reduced carrying capacity, we compared reconstructed vegetation cover before European settlement (1788) and mapped vegetation cover in 1988 (Geoscience Australia, 2003a; Geoscience Australia, 2003b). We consolidated tree classes (tall trees > 30 m, medium trees < 20 m, low trees < 10 m) and calculated the proportion of cleared tree area in each population units, as the

3. Results Platypus atlas records were present in 356 cells (50 km × 50 km), covering 890,000 km2 (Fig. 1). Assuming a cell with a platypus record within a river catchment indicated presence throughout that catchment, there were 453 additional cells (56%) where platypuses may currently occur or have occurred, suggesting considerable gaps in knowledge of the species' distribution. Cumulative number of cells with platypus observations increased steadily from the early 1960's plateauing by 2006 (Fig. 3a). Cox proportional hazards model on the number of cells losing record continuity indicated significant differences between the species (Fig. 3b), with the highest hazard rate for the platypus, 1.33–2.4 times higher compared to other species (Appendix 5). Of the 356 cells where platypuses were recorded, 9.8% of cells had no records since 1990, similar to the native rakali (12.5%), contrasting the < 3% for the invasive species analysed (Fig. 3). By the year 2000, 19.6% of cells had lost continuity of sightings, compared to 30% for rakali and 16.7% in domestic cat, 7.1% for red fox and 6.6% for European carp (Fig. 3). After 2000, most (67%) cells where platypuses were not recorded were on western flowing rivers in the species' southern extent, west of the Great Dividing Range, predominantly the rivers of the Murray-Darling Basin. In the Murray River Catchment, extending into South Australia, 10% (11 of 163 cells) had no records

Table 2 Annual fecundity and survival rates (stage matrix, ± sd) for platypus (F-female, M-male, A-adult, J-juvenile) based on data from Fox et al. (2004), Bino et al. (2015) and Bino et al. (2019).

FJ FA MJ MA

FJ

FA

0 0.29 ± 0.01

0.47 ± 0.05 0.89 ± 0.04 0.47 ± 0.05

MJ

MA

0 0.23 ± 0.01

0 0.77 ± 0.04

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Fig. 3. a) Cumulative percentage of cells (50x50km) with platypus (cross), rakali (square), cat (triangle), fox (filled square) and carp (rhombus) records in atlas databases between 1960 and 2017 from the total 356 cells with platypus records; b) loss of record continuity (i.e., survival) curves for platypus, rakali, cat, fox and carp between 1960 and 2017 across the 356 cells (50x50km) with platypus records.

models had at least one dam within the population boundary (Fig. 2). Once integrated within the metapopulation model, fragmentation by dams projected extinction of 30 population units, a reduction of 5.9% compared to the baseline model (476 populations), and reduction of 14.7% in EMP (279,322 ± 1638SD) over the simulation (Fig. 4, Appendix 5). Almost a third of initial population units lost latitudinal connectivity with other population units. Reductions predominantly occurred in populations units in the headwaters of catchments (Fig. 4), a result of isolated small population sizes coupled with modelled environmental and demographic stochasticity. When opportunities for overland dispersal between population units were restricted, combined with fragmentation by dams, there was a predicted decrease in metapopulation occupancy by 14.2% (434 populations) and expected minimum population size by 15.1% (277,532 ± 1829sd), compared to the baseline model (Appendix 5). Fragmentation scenario predicted significant spatial fragmentation across the species' entire range, with a 50% decline in population size in almost a third (29%) of population units, extending over 39% of the area occupied by platypuses, predominantly in headwaters of catchments (Fig. 4a). Mapped 1988 vegetation cover compared to 1788, showed significant loss of tree cover has occurred where platypuses occur (Fig. 2), including an estimated loss of 40% of low trees (< 10 m), 30% of medium trees (10–30 m), and 20% of tall trees (> 30 m). Such habitat destruction was estimated to reduce carrying capacity by 26% ± 34sd,

since the 1980's, of which all seven cells in its southern mainland extent (South Australia) had no records since 1990. In the species' northern range (Queensland), 15 cells (16% of 96 cells) had no sightings after the 1990's and 31% (31%, 29 cells) after 2000. Modelled extinction probabilities closely followed the year of last sighting (YLS), with a good fit (R2 = 0.77) to a second-order polynomial model: P(extinct) = 0.0002*YLS-0.9095*YLS + 923.45. Analysis also highlighted areas with more recent loss of record continuity but with high probability of extinction (Fig. 1b). Fitted distribution model of platypus showed strong predictive performance, with an area under the receiver operating characteristic curve (AUC) of 0.93 and Cohen's Kappa of 0.73, based on a ten-fold cross-validation analysis. Precipitation of driest quarter (38%, negative association), maximum temperature of warmest month (24%, peak between 15 and 25), and maximum river segment elevation (21%, positive association) contributed most to model performance (Appendix 2). Based on this species' distribution modelling and scaling of platypus densities, the initial metapopulation model reached equilibrium (baseline), with an average of 506 populations (range 490–522), indicating metapopulation occupancy and an expected minimum population size (EMP) over the course of the 200-year simulation of 326,804 ± 1339sd (Appendix 5). Nearly half (168 cells, 47%) of all 356 cells with platypus records and 30% (153) of the 506 baseline populations of the metapopulation 7

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frequency and duration of droughts under climate change, combined with fragmentation and habitat destruction, metapopulation occupancy was estimated to decrease between 35.6% to 55.5%, a reduction between 51.6% (158,289 ± 1876SD) and 73.5% in EMP (86,696 ± 3337SD), leaving only small isolated populations in Tasmania and the east coast (Fig. 5d). Sensitivity of metapopulation occupancy and EMP to variation of ± 10% in vital rates estimates (stage matrix estimates of survival and fecundity) was low and eclipsed by the impacts of examined threatening processes (Appendix 5). EMP was moderately sensitive to variation in maximum growth rate (Rmax), with a 5% decrease in Rmax (λ = 1.045) leading to a 10.7% decrease in EMP and 6.1% in metapopulation occupancy from the baseline model. When Rmax was increased by 5% (λ = 1.155), EMP increased by 1.9% and metapopulation occupancy increased by 6.9%. The largest sensitivity was observed when the number of females a male can mate with was reduced from three to two, lowering EMP and metapopulation occupancy by 48.1% and 10.9%, respectively (Appendix 5). 4. Discussion

Fig. 4. Population size and 95%CI based on metapopulation models under scenarios: 1. Baseline (red); 2. Baseline with historic drought frequencies (‘Dr’, orange, 20% reduction in population); 3. Fragmentation (‘Frag’, green); 4. Habitat destruction (‘Hab’, jade); 5. Fragmentation and habitat destruction (blue); 5. Fragmentation, habitat destruction, and historic drought frequencies (purple); 7. Fragmentation, habitat destruction, and drought frequencies under climate change projections for 2070 (‘CC’, pink). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Our population viability analyses indicated serious concerns for the long-term future of the platypus, given increasing pressures of water resource developments, particularly construction of dams fragmenting their distribution, increased predation by invasive species during overland dispersal, land clearing degrading and fragmenting habitat, and increasing frequency of droughts (Fig. 5). Viability of many populations is compromised by synergistic effects of these threats (Grantham et al., 2017; Kingsford et al., 2017; Semlitsch et al., 2017). Our results highlight the synergistic impacts of fragmentation and reduced carrying capacity, predicting a drop in EMP between 52% to 72%, depending on drought extent and severity, over a period of about 100 years (Fig. 4), leading to local extinctions across about 40% of the distribution of platypus (Fig. 5). Our findings are supported by accumulating evidence that platypus populations are declining, with a few documented local extinctions, particularly in heavily regulated rivers experiencing prolonged droughts (Serena and Williams, 2007; Serena and Williams, 2008; Williams, 2010; Hawke et al., 2019a). Recent assessment of historic data also supports a significant shift in platypus numbers since European colonisation, suggestive up to a 90% decline in numbers beginning with the fur trade (Hawke et al., 2019b). The IUCN Red List (IUCN, 2017) is a key mechanism for assessing the conservation status of species (Rodrigues et al., 2006), currently listing platypus as ‘Near Threatened’ (Woinarski and Burbidge, 2016). Five criteria of quantitative assessment (A-D) are used to estimate extinction risk: population size (A, C, D), geographic range (B), and quantitative probability of extinction (E), with resulting categories from least concern to extinct reflected on the basis of the highest level of any one of these criteria (IUCN, 2017). Following the IUCN's framework of quantifying extinction risk to platypus, using our analyses and available data, platypus populations do not qualify under analyses of Criteria BD, given their wide distribution (Fig. 1) and estimates of total numbers exceeding 10,000 individuals. We found a reduction of 30% or greater in observed, estimated, inferred, or suspected population in the past, future or present (Fig. 4). Using IUCN Criterion A and E, assessing declines over 30 years (3 generations) and assuming a generation time of 10 years (9–12 years) (Woinarski et al., 2014), suggested the species be re-evaluated and may warrant a ‘Vulnerable’ status, particularly when considering the ongoing and further projected increase in frequencies and duration of extreme droughts (CSIRO and Bureau of Meteorology, 2015). Our assessment of changes in the distribution of the platypus is hindered by critical knowledge shortfalls, with significant areas within the species potential range without a sighting (Fig. 1). Knowledge gaps relating to changes in distribution and abundance of species presents the risk of failing to detect rapid declines and local extinctions (Powney

reducing metapopulation occupancy by 13% (426 population units) and EMP by 29.3% (230,921 ± 1246sd) from the baseline model. Tree loss was predicted to have reduced population abundance by at least 50% in 41% of populations (representing approximately 50% of area). Population declines were predicted to mostly occur along the western extent of the platypus distribution (Fig. 5b), predominantly affecting the rivers of the Murray-Darling Basin. A systematic reduction of population carrying capacity across all populations, at 20% increments (20%–80%), reduced metapopulation occupancy respectively by 4%, 10%, 19% and 32%, compared to the baseline model, while the impact on EMP was more extreme, with respective reductions of 21%, 42%, 63%, and 83% (Appendix 5). When habitat destruction was coupled with the fragmentation impacts of dams and loss of overland dispersal, metapopulation occupancy was further reduced by 30% to 353 populations and EMP by 41.8% to 190,361 ± 1601sd. This combined scenario was estimated to reduce total population abundance by half from the pre-European baseline across 67% of populations, representing 73% of the total area, leaving a scattering of more resilient, but less connected populations in areas of core suitability (Fig. 5c). Following a systematic reduction of population carrying capacity across all populations, at 20% increments (20%–80%), along with fragmentation scenario, synergistically reduced metapopulation occupancy further by 22%, 31%, 45% and 62%, with respective reductions in EMP of 36%, 56%, 74%, and 89%. These were significantly higher compared to un-fragmented populations, indicating high sensitivity of platypus to fragmentation and movement barriers. Incorporating historical severe drought frequencies, representing possible baseline scenarios, with impacts ranging from a reduction by 10% to 30% did not have a significant impact on metapopulation occupancy, decreasing number of populations respectively by 1% to 6.3%, though commensurate decreases in EMP of 8.1% (300,184 ± 1695sd) and 27.6% (236,709 ± 3529sd) resulted. The combined synergistic scenario, incorporating habitat destruction and fragmentation with historic drought frequencies (10%–30% reduction in population abundance), reduced metapopulation occupancy by 33% to 43% and EMP between 47.3% (172,158 ± 1804SD) and 60.9% (127,926 ± 3252SD), compared to the baseline. With increased 8

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Fig. 5. Predicted population size in each population unit based on 7-th level HydroBASINS (Lehner and Grill, 2013), as a proportion of baseline scenario after 200 years, under the following scenarios: (a) fragmentation (Frag, dams and predation); (b) land use change (Hab); (c) fragmentation and land use change (Hab); (d) fragmentation, land use change, and regional droughts (Dr, P = 0.1, 10% reduction in population size).

invasive species as well as that in the only other mainly amphibious native mammal, the rakali or water rat (Fig. 3, Appendix 4). Examined threatening processes (i.e., land clearing and water resource development) began > 50 years ago, both continuing to increase (Bino et al., 2016) with current land clearing rates among the highest in the developed world (Bradshaw, 2012; Evans, 2016; Simmons et al., 2018). Deleterious impacts on platypus populations likely continue, reflecting this legacy of development (i.e., extinction debt (Tilman et al., 1994)), including high sedimentation rates filling up pools, habitat degradation and fragmentation of populations (Bino et al., 2015), (Table 1). When threats were introduced into metapopulation models, most of the impact on abundance took place over a course of 50 years (Fig. 4), and continued to decline in fragmented populations. Where exactly the current condition of platypus populations lies on the sharp decline predicted by models is uncertain but likely falls at the tail end of

and Isaac, 2015). Analysis of Atlas records suggests that platypus distribution has contracted since European colonisation of Australia (Fig. 3). However, its distribution may have contracted considerably more than these estimates indicate, given the large areas without atlas records not incorporated in our continuity analysis (Fig. 1). This is likely as many of these data deficient areas coincided with major threatening processes, including some of the most regulated and disrupted rivers in Australia (Kingsford, 2000; Grant and Fanning, 2007). In addition, only 16.5% of the area occupied by platypuses coincided with protected areas. Atlas data are highly suboptimal for the purpose of monitoring trends and are replete with biases relating to the spatiotemporal distribution of effort, detectability, and lag in data digitisation and transfers to the databases (Dennis and Thomas, 2000; Snäll et al., 2011; Tulloch et al., 2013). Still, changes in platypus record continuity significantly differed to those observed in the four examined 9

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2017). This is particularly important in small streams, where platypus numbers are low and permanent drought refugia may not exist. Removal of dams would improve flow regimes but is unlikely, given human dependencies. Certainly, construction of new dams, as recently proposed by Australian governments will be detrimental to many freshwater ecosystems, affecting platypus. Developing “platypus-ways” providing safe passage from feral animals and improving connectivity by bypassing weirs and dams might be a mitigation measure but significant impediments to development remain (platypus behavior, type of structure, particularly for large dams). Maintaining healthy and connected platypus populations, between catchments, along the eastern flowing rivers of Australia and Tasmania must be a priority for the species.

it. The scale of our analysis likely increased uncertainties of population dynamics such as connectivity and dispersal between populations or the prevalence of important drought refugia. Given the computational limitations of the software, we did not use the eight sub-basin level which would have produced > 6000 populations units and substantially higher number of connections. Developing finer scale approached, including individual based models, is heavily dependent on knowledge of both life history and the accuracy of spatial data, but also requires appropriate alignment between the choice of analytical methods and desired conservation management objectives (Radchuk et al., 2016). Riverine species, with dendritic metapopulation structure as a series of watersheds and linear habitats (rather than a patch and matrix of 2dimentational metapopulations), can be particularly susceptible to fragmentation from both barriers as well as habitat destruction (Fagan, 2002; Campbell Grant, 2011). Given ongoing and projected increases in severity of droughts and other extreme weather events (CSIRO and Bureau of Meteorology, 2015), small and isolated populations will be most susceptible to local extinction without potential recolonization. Increased drying is already affecting the southeast of the continent, with runoff into the rivers of the Murray-Darling Basin declining (Chiew et al., 2009). Extended droughts will increasingly impact on stream flows, reducing the extent of critical drought refugia, forcing platypuses to move overland, where risk of predation by invasive species is high, and exacerbating competition within groups confined into decreasing numbers of remaining pools. In addition, predicted increases in ambient temperatures may also reduce thermally suitable habitat in the species' northern extent (Klamt et al., 2011).

Data availability statement Data will be made available from the Dryad Digital Repository once the manuscript is accepted for publication. CRed1iT authorship contribution statement Gilad Bino: Conceptualization, Methodology, Formal analysis, Writing - original draft, Writing - review & editing.Richard T. Kingsford: Conceptualization, Writing - review & editing.Brendan A. Wintle: Conceptualization, Writing - review & editing. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

4.1. Conservation action Conserving the platypus, an Australian icon and an evolutionarily unique animal (Isaac et al., 2007), must become a priority at all levels of government through increasing public awareness, listing on State and Federal threatened species schedules (e.g., Environment Protection and Biodiversity Conservation Act 1999), focused research and monitoring, rigorous environmental assessment and mitigation and management of the threats. Even for a presumed “safe” species such as the platypus, mitigating or even stopping threats (e.g., new dams) is likely to be more effective than waiting until extinction risk increases and possible failure (McCarthy et al., 2008). For the platypus, understanding how threatening processes affect survival, reproduction and movement remains poor, reliant primarily on qualitative data (Bino et al., 2019). Current understanding of the platypus mating system is also deficient (Grant et al., 2004; Hawkins and Battaglia, 2009; Thomas et al., 2018). Our models were highly sensitive to this assumption, with reduction of three to two mated females per male in metapopulation models significantly increasing predicted impacts of threatening processes. Given existing knowledge gaps of platypus numbers and distribution, developing cost-effective monitoring programs which integrate both systematic surveys and citizen-science initiatives are sorely needed in relation to threats, as well as improving understanding of demographics, genetics, and diseases. A national ban on enclosed cray fish traps is a first and necessary step, following recent bans in Victoria (VFA, 2018) and the Australian Capital Territory (ACT, 2019). Maintaining healthy riparian and benthic habitats is critical, dependant on land practices as well as freshwater availability. For riparian health, prevention of land clearing and restoration efforts are essential for maintaining stable banks, along with limiting cattle grazing and access (Serena et al., 2001; Lunney et al., 2004). High land clearing rates, within the range of platypus, may be degrading their habitats (Evans, 2016), particularly in Queensland where distribution, abundance and vulnerability of c platypus are poorly known. The building of dams and river management affect platypus and their prey; maintenance or restoration of natural flow regimes is critical (Gilligan and Williams, 2008; Serena and Grant,

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