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Australian Mammalogy, 2018, 40, 47–57 http://dx.doi.org/10.1071/AM16059

Using repeat citizen science surveys of koalas to assess their population trend in the north-west of New South Wales: scale matters Martin Predavec A,D, Daniel Lunney A,B, Ian Shannon A, John Lemon C, Indrie Sonawane A and Mathew Crowther B A

Science Division, Office of Environment and Heritage NSW, PO Box 1967, Hurstville, NSW 2220, Australia. School of Life and Environmental Sciences, University of Sydney, NSW 2006, Australia. C JML Environmental Consultants Pty Ltd, 9127 Kamilaroi Highway, Gunnedah, NSW 2380, Australia. D Corresponding author. Email: [email protected] B

Abstract. Scale matters when assessing population trends. Whereas traditional field-based ecological surveys are generally restricted to small temporal and spatial scales, community (citizen science) surveys allow wider consideration of population trends. We used repeat community surveys (completed in 2006 and 2015) to assess population change in koalas (Phascolarctos cinereus) across an area of 36 900 km2 in the north-west of New South Wales. In both community surveys we asked respondents to record the location of their koala sightings as well as those of eight other common species. We further asked respondents about their perceptions of population change. Through three different measures (likelihood of koala occurrence, number of koalas observed per respondent, and the perception of population change), we found that koala numbers were declining across the region during the study period. The timing and broad and consistent geographic spread of the decline suggests that broad-scale environmental factors, such as weather, are important drivers of this change. This information will allow managers to place conservation efforts into an appropriate spatial context. While such information sourced from the community can provide critical information on threatened species, including the koala, this study highlights the limits of such information. Additional keywords: community wisdom, population cycles, population decline, Phascolarctos cinereus, refuges. Received 30 November 2016, accepted 17 March 2017, published online 19 May 2017

Introduction Scale matters when assessing population trends. There is much focus on temporal scale, such as the IUCN criteria for a population decline over three generations (IUCN 2012), but spatial scale is also important (Lomolino and Channell 1995). The broad spatial and long-term temporal assessment of population trends allows questions of environmental drivers to be addressed and can better embed conservation actions on the ground within the appropriate context, as has been shown for koalas (Phascolarctos cinereus) (Knott et al. 1998; Lunney et al. 2010, 2016b, 2016c; Lunney and Moon 2012; Predavec et al. 2016). We use community (citizen science) surveys to determine the population trends of koalas within the north-west slopes and plains of New South Wales (NSW). Whereas traditional ecological survey and research tends to operate over small spatial and temporal scales (Fig. 1), citizen science presents opportunities to look at longer temporal scales (Lunney et al. 2016b; Predavec et al. 2016) and broader spatial scales (Predavec et al. 2016). Citizen science is a maturing scientific tool in which members of the community (citizens) are included in Journal compilation Australian Mammal Society 2018

the scientific process, often with a focus on data collection (Silvertown 2009; Tulloch et al. 2013). Citizen science projects work well for studies of koalas because of the broad community interest in the species, its instantly recognisable form, the fact that sightings tend to be well remembered and members of the public will likely have an opinion on the species (Predavec et al. 2016). Data collection on koala populations using citizen scientists has to date included citizen scientists directly observing koalas during a survey (Sequeira et al. 2014), recording past observations of koalas on maps (Reed et al. 1990; Lunney et al. 2009, 2016b), and combining the collective perceptions of citizens regarding population change (Predavec et al. 2016). It is the latter two methods that best allow koala citizen science projects to cover broad geographic areas as well as long timeframes (Fig. 1) and these form the core of the current study. The sustained narrative surrounding the koala populations of NSW is one of decline since the first state-wide koala survey in 1986–87 (Reed et al. 1990; Reed and Lunney 1990). It is seen in many studies that have looked at koala populations over multiple generations (Lunney et al. 2009; McAlpine et al. 2015; www.publish.csiro.au/journals/am

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Adams-Hosking et al. 2016; Predavec et al. 2016). Further, this led to the listing of the koala as Vulnerable in NSW in 1992 under the NSW Endangered Fauna (Interim Protection) Act 1991, a status it maintained under the NSW Threatened Species Conservation Act 1995 as well as the 2012 listing under the Federal Environment Protection and Biodiversity Conservation Act 1999. In the state-wide listings and studies, two populations have stood out against the general pattern of decline. The koalas of Gunnedah were shown in a 2006 community survey to be increasing, the only local government area that showed an increase (Lunney et al. 2009; Predavec et al. 2016). Nearby, the Pilliga population was shown in the 1990s to be large (Kavanagh and Barrott 2001) and the population in the region (including Gunnedah) was considered to be stable (Predavec 2002). More recent studies point to the koala populations in both the Gunnedah region and the Pilliga forests as declining (Lunney et al. 2012, 2016a). Following a significant drought and heatwave in 2009, the koalas of Gunnedah and the surrounding Liverpool Plains, suffered a 25% decline in numbers (Lunney et al. 2012). In the Pilliga forests, repeat field surveys in 2013 of surveys initially carried out in the 1990s showed an 80% decline in the distribution and activity of koalas (Lunney et al. 2016a). This study identified that while koalas were present in the Pilliga forests in riparian habitats, past disturbance of these habitats mean that they no longer function as refugial habitats and that the Pilliga population is vulnerable to extinction (Lunney et al. 2016a). To explore further the decline of koalas in the region, we used the citizen science method of community survey of koalas. By using methods similar to a state-wide community survey carried out in 2006 (Lunney et al. 2009) we could compare the results and look at how the population of koalas has changed between pre-2004 and 2015 across the broad geographic range of the north-west slopes and plains of NSW.

Methods Study area The study area consists of 36 900 km2 on the north-west slopes and plains of NSW (Fig. 2), an area that equates to 5% of the State. This area encompasses the Liverpool Plains surrounding Gunnedah, the Pilliga forests to the west of Gunnedah and Warrumbungle National Park, three specific areas of interest in the region in relation to koala populations. The Liverpool Plains are among Australia’s prime agricultural landscapes where the conservation of biodiversity occurs largely on private land (Crowther et al. 2009; Lunney et al. 2012). The Pilliga forests (535 000 ha), near Coonabarabran, Baradine and Narrabri, have a long and continuing history of timber harvesting dating back more than a century. The semiarid climate and unsuitability of the soils for agriculture combined to protect the Pilliga forests (a mixture of cypress pines and eucalypts) from land clearing for agriculture, such that this area is now the single largest remaining tract of native forest and woodland in NSW west of the Great Dividing Range. The size of the study area reflects an area that we regard as containing a functioning koala population (i.e. gene flow across the extent) over the longer term. The study area also incorporates local areas of interest, such as the Liverpool Plains and the Pilliga forests. 2006 Citizen Science Survey As part of a 2006 state-wide, map-based survey of 10 wildlife species, we sent out 213 685 survey forms by mail across rural NSW (Lunney et al. 2009). The form included a questionnaire asking whether the species occurred in their local area and whether respondents thought that populations had increased, decreased, or stayed the same in number. The survey form included an A2 colour map on which respondents could mark sightings of animals, with respondents asked to identify sightings made between 2004 and 2006 and before 2004. Each respondent was given a unique identifier.

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2015 Citizen Science Survey of the north-west region The 2015 survey was web-based and addressed the location of koalas and 15 other species observed by members of the public both before and after January 2013 as well as their perceptions of population trends. Species included koala, galah, echidna, cat, fox, flying-fox, emu, kangaroo (as a group), wild dog/dingo, quoll, wombat, brushtail possum, ring-tail possum, deer (as a group), platypus, and eastern rosella. Letters were sent to 31 000 postal points within the region (the study area plus a 10-km buffer) asking community members to complete the survey. Media were contacted regarding the survey and promoted participation. Participants were asked questions about occurrence and population trends for each of the 16 taxa. For the koala they were asked also about health (sightings of individuals with visible signs of chlamydiosis) and reproduction (sightings of individuals with back young). Participants were asked to record the location of species observed by dropping markers onto two maps: one for sightings between 2006 and the end of 2012 and the other between 2013 and 2015. The map interface was based on Google Maps (maps.google.com) and participants could zoom in and out to allow accurate placement of markers. The survey remained open from October 2014 to March 2015, with reminders posted in the media during this period. As in the 2006 survey, each respondent was given a unique identifier. Data analysis Nine of the species, including the koala, were surveyed in both the 2006 and 2015 surveys and formed the basis of the analyses. Because of the structure of the two surveys, we could split the overall study into four periods: pre-2004, 2004–06, 2006–12, and 2013–15.

Sufficient information To determine whether sufficient data were collected, we looked at the spatial spread of the data across the study area (Area of Occupancy) in relation to the survey effort. For the koala separately, and the other eight species as a group, we assigned each record to a 10 km 10 km grid spread across the study area. We then plotted the cumulative number of unique grid cells in which a record fell against the cumulative number of records, giving a measure of the Area of Occupancy against survey effort. The curve was smoothed by randomising the order of record entry 100 times and averaging the results. An accumulation function (Clench 1979) was fitted to the curve using non-linear least-squares. The slope at the point of the last record was calculated using the first-order derivative of the Clench function. A steep curve at the point of the last record, taken to be a value greater than a 5% slope, indicated that we were still collecting new survey locations to the end of the survey. In contrast, a curve that flattened (slope less than 5%) indicated that no or little new information was being added with additional records. The curves and slopes were calculated for koalas and other species for the two surveys as a whole and the four periods separately. Comparison of the koala population spatially and temporally Across the study area as a whole and for each of the four periods we compared the proportion of the total sightings for each species, giving a measure of the relative abundance (Predavec et al. 2015). We investigated the distribution of records across the eight species and four periods using a Chi-square contingency table. As a second independent measure, we calculated the average number of sightings per unique respondent in each of the four periods and for each of the eight species and compared the distribution using a Chi-square contingency test.

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To investigate the spatial pattern of change we divided the study area into a 20 km 20 km grid and mapped all species sightings across the cell grid using ArcGIS 10.1. For a comparison of time we used only data from 2004–06 and 2013–15 (i.e. a single period from each of the two community surveys). For each 20 km 20 km cell we calculated the confidence in the data following the species accumulation curve method of Graham et al. (2015). Whereas for the entire study area the accumulation curve of the Area of Occupancy versus the number of records can be used to assess the sufficiency of data, for smaller spatial areas this is not appropriate. For each cell, we determined a smoothed species accumulation curve created by plotting the cumulative number of species against the number of records and with the curve smoothed by randomising the order of record entry 100 times and averaging the results. This followed the methods of Graham et al. (2015) and is described above in the section determining sufficient information. All calculations were completed in R (R Development Core Team 2016) using code developed by Graham et al. (2015). If data from an individual cell resulted in a slope at the point of the last record of greater than 5% then they were combined with data from an adjacent cell, creating a larger cell, and the species accumulation curve, Clench function and final slope were recalculated. This process was

repeated until all cells, now covering a range of sizes, each met the criteria of having a slope at the point of the last record of less than 5%. This process was completed for data from the two surveys in parallel so that the spatial distribution of the cells matched. For each cell we calculated the proportion of records that were koalas (Predavec et al. 2015) from the two periods. The comparison between the two periods was made using a paired t-test. Perceptions of population change Finally, we looked at the respondent’s perception of change in the koala populations. People’s perception of change in fauna populations can give a reliable indication of the direction of population change (Predavec et al. 2016). Respondents in both surveys were asked if the koala population in their local area was increasing, decreasing or staying the same. The distribution of responses in each of the three categories in the 2015 survey was compared with an expected distribution based on the 2006 responses using a Chi-square test. In the 2015 survey respondents were also asked whether koalas occur in their local area (yes; previously but not now; never been here) and when they last saw a koala (within the last week; month; year; 10 years; before 10 years; or never seen one). The spatial distribution of

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the responses was mapped on the basis of the postcodes of the areas in which the respondent lived (this was the only spatial extent that we could assign individual respondents to regarding the general questions). Results Data and data sufficiency In the 2006 survey we received 16 526 completed responses across NSW, with respondents reporting 4909 koala sightings. Within the study area we received 479 responses, comprising 2073 sightings of the nine species common between the two surveys, including 813 koala sightings. In 2015, 413 individuals responded to the survey and provided usable map-based data across the study area. This resulted in 7239 sightings in total, 2218 mapped sightings across the nine common species and 619 sighting of koalas (Fig. 3). The area accumulation curves for the koala and other species as a group showed levelling off (slope less than 5%) in both surveys (Fig. 4), indicating that additional survey effort would 2006 Survey All 2006 survey

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not provide significantly more information. In the 2006 survey this pattern held for the period 2004–06 when considered in isolation, but did not hold for the pre-2004 period. In the 2015 survey the pattern was almost significant in the period 2013–15, but again was not significant in the earlier period (2006–13) (Fig. 4). The overall pattern is consistent, with fewer records being obtained in both surveys for the earlier period compared with the current period, which is consistent with respondents forgetting that they had seen animals further back in time. Lunney et al. (2016b) have shown that community survey data, such as these, usually fit a negative exponential curve known as a forgetting curve (Ebbinghaus 1885; Averell and Heathcote 2011): that is, people remember recent events better than they do older events. Change in measures of koala abundance During the four consecutive periods covered by the two community surveys, the proportion of the total number of animals recorded that were koalas has declined (Fig. 5). Seven 2015 Survey All 2015 survey

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of the eight other species showed little change, or an increase, over the same period (Fig. 5). A contingency table analysis comparing the nine species and the four periods suggests a significant difference (c2 = 291, P < 0.05), with 40% of the variation attributed to the koala. Comparing the number of animals recorded per respondent in the four periods (Fig. 6) showed that for seven of the species there was an increase from the earlier periods to the later period. The koala and wombat showed a decline from 2006–12 to 2013–15. A decline in a more recent period is even more pronounced when the forgetting curve (where people are more likely to remember recent events than older events) is considered (Lunney et al. 2016b). This pattern is again consistent with a decline in koalas. A contingency table analysis of the four periods and the nine species showed a significant result (c2 = 120, P < 0.001), with the koala contributing most towards the overall Chi-square value, with the number observed per respondent in 2013–15 being lower than expected under a null hypothesis of no change. The decline in koalas across the study area, as measured by the proportion of records that were of koalas, was not spatially consistent (Fig. 7), with different areas (cells) contributing to a mix of decreases, no change and increases across the study area. On average, there was a decrease of five percentage points in the proportion of records that were koalas (25% in 2006

versus 20% in 2015), representing a 20% decline. The paired t-test was significant (t = 2.4, d.f. = 24, P = 0.05), showing an overall decline in koalas across the study area. Community perception of the koala population The community’s perception of population change is consistent with a decline in koalas. Comparing the percentage of responses in each of the two survey periods as to the population of koalas increasing, staying the same or decreasing (Table 1), showed a decrease in the percentage of respondents who thought the population was increasing and a corresponding increase in the percentage who thought the population was stable or decreasing. The distribution of responses in the three categories comparing 2015 with 2006 is dependent on year (c2 = 6.2, P < 0.05) (Table 1). Although in 2015 a larger percentage of respondents Table 1. Number and percentage of respondents in the two surveys who thought the koala population was increasing, decreasing or staying the same

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thought local koala populations were increasing when compared with decreasing, given the time between the two surveys and the time lag in people’s recognition of change (Predavec et al. 2016) it is the change in the percentages between the two surveys that is consistent with a decline in koalas. In the 2015 survey, the average responses to the three koala population questions varied spatially (Fig. 8). For a large proportion of the study area, respondents indicated that koalas once occurred in the local area, but not now (Fig. 8a). This does not necessarily indicate local extinction, but may be a case that animals are seen less frequently. It was only in areas surrounding Gunnedah that koalas were seen frequently (i.e. within the last week or month). Across much of the study area, koalas were last seen over a year before the survey and in many cases more than 10 years prior (Fig. 8b). For a large proportion of the study area, respondents thought the koala population was decreasing or staying the same. It is important to recognise that a population staying the same does not necessarily imply a healthy population, but can represent a population that was close to undetectable to start with and has not changed. Discussion The patterns seen in comparing the results of the two citizen science surveys, eight years apart, are largely ones of decline. This is seen in the proportion of koalas, the number of koalas per respondent and in the community’s perception of population

change. The value of such combined ‘community wisdom’ in determining population change in koalas is detailed in Predavec et al. (2016). This overall pattern of decline is consistent with field-based local studies of koala populations within the study area. Repeat surveys of koalas within the Pilliga forests between the 1990s and 2013 reported an overall decline in both the distribution and activity levels of koalas (Lunney et al. 2016a). The study suggested that the extreme weather events caused koala populations to contract into riparian refuges, but that historical damage to riparian habitats have reduced their value as refuges. In Gunnedah, there was a significant decline following heatwaves during the drought in 2009. This extreme weather event saw above-average temperatures in the region and, importantly, the high temperatures occurred over strings of successive days rather than simply on isolated days. The weather event saw an estimated 25% of the koala population of the Gunnedah region die and an increase in the expression of symptoms of Chlamydia infection (Lunney et al. 2012). The environmental impact statement for a quarry expansion at Mary Mount, ~20 km west of Gunnedah, showed a high population of koalas on the mine site and surrounding properties, with 18 koalas seen in a single night in 2013 (Niche Environment and Heritage 2014). Repeat surveys of the site in 2016 found only three koalas (D. Lunney, unpubl. data). These site-based local studies all identify a similar pattern of population decline, although the timing of the decline is not necessarily consistent across the studies. The current comparison

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of citizen science surveys supports the impression that koalas across the broad region are declining. Comparison with studies further afield indicate that the patterns of decline detailed in this study occurred over a large geographic area. A study of drought-driven changes in koala

numbers in south-west Queensland (Seabrook et al. 2011) found an 80% decline in koala numbers over the period 1995 to 2009. This comparison is particularly relevant given that the study took place in a semiarid landscape setting like the present study. The broad geographic scale of the decline suggests that there



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(a) Do koalas occur in your local area? No data Never been here Previously, but not now Yes

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Fig. 8. The spatial distribution of responses to the three koala population questions in the 2015 survey. The spatial units are postcodes and the data are averaged across all responses.

is a broad-action environmental factor at play, such as weather conditions. Not all declines in the region might be attributed to the same feature. The decline of koalas in Warrumbungle National Park can be partly attributed to the severe fire that occurred in January 2013 (Barlass 2013), but a major decline in the koala population

in the national park can also be attributed to the Millennium drought (Sue Brookhouse, NSW NPWS, pers. comm.). However, the cause of the regional decline may be a contributing factor to how the Warrumbungle National Park koala population responded to the fire and, importantly, how it might recover after fire. Lunney et al. (2016a) have reasoned that disturbance

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of riparian refuges within the Pilliga forests was a contributing factor to the decline of koalas, with the impact of the overall decline in koalas affected by the loss of refuge habitat. This project compared two community surveys spanning the period pre-2004 to 2015, which is 2–3 koala generations. What is not clear is whether the decline we have recorded is part of a broad overall decline or the decline phase of a boom and bust cycle. Koalas certainly have been at low densities in the region in the past and have increased. There is no long-term ecological history for the region, and this study identifies the need for such a study. However, there are perceptions of long-term trends and studies that point to a stable or increasing population before the recent declines described here. The 2006 state-wide community survey highlighted the Gunnedah region as the only area of NSW with an increasing koala population (Lunney et al. 2009). Even in the 2015 survey, a large proportion of the residents thought the population was increasing (Table 1). A similar result was found in the studies informing the Gunnedah Koala Strategy, with current occupancy rates of available habitat being ~50% compared with ~15% estimated through historical koala records (Gunnedah Shire Council 2015). Within the Pilliga Forests, the high population estimate in the 1990s was thought to have followed a population increase, and the 1990s population was thought to be at the highest level in over 70 years (van Kempen 1997; Kavanagh and Barrott 2001). In the Warrumbungle National Park, south of the Pilliga forests, koalas were at sufficiently low numbers in the 1960s that they were thought extinct in the Warrumbungle National Park (Fox 1996). Plans were proposed to recolonise the national park with koalas translocated from Victoria and progressed to the point of a plantation of manna gums (Eucalyptus viminalis) being planted in the park. Koalas were discovered in the park soon after the planting and the translocation plans were abandoned (Fox 1996). Until the 2013 fires within the park, koalas were considered to be abundant in the late 1990s, although numbers had declined markedly in the years preceding the 2013 fire, most likely from the Millennium drought. These studies allow the conclusion to be drawn that the regional koala population can expand and contract and the geographic extent over which this occurs identifies weather or climate as an important driver of these changes. Such fluctuations may be part of a natural population cycle, but human-induced climate change is likely to result in greater extremes, which will have an impact on the koala populations (e.g. Gunnedah). The low point of the cycle makes the koalas particularly vulnerable as is seen in the Warrumbungle fires and in disturbance of the riparian refuges in the Pilliga forests (Lunney et al. 2016a). Value of community surveys Community surveys are useful for obtaining data over large geographic areas (in this case, 36 900 km2) and, if designed carefully, over a relatively long period. The combination of spatial records with community perception is particularly powerful in that it provides two methods by which the population trends can be determined. However, community surveys are limited by people in the community (density) and their willingness to complete the surveys. Data are also biased

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towards roads or other public spaces, as can be seen in Fig. 3, with the concentrations of records around urban centres such as Gunnedah and along roads. The biases can be partly overcome by keeping the survey methods consistent among surveys (i.e. keeping the biases consistent) and using measures, such as koalas observed per respondent, that are largely independent of survey effort. This is particularly the case when different survey methods are used in surveys, as was the case in this study. While the first survey was paper-based, and the second survey was web-based, the impact of this change on the results is unknown. We assume this impact is small, but recommend using consistent survey tools where possible. It is also important to include measures of confidence in citizen science data analysis, which is the central feature of this paper, and not be lured to a conclusion by the initial spread of survey results, as seen in Fig. 3. The current study is in an area with a low human population density (31 000 residences over 36 900 km2) and this is likely at the border of which such studies can work. Even in this study the impact of the human population can be seen: the further west in the study area, where the human population density is lower, the more general are the conclusions that can be drawn. This should not devalue such studies, but rather highlights elements that must be considered in their design. The knowledge of the community about koalas and their populations has provided important information regarding population changes. This information is critical to the conservation of koalas, given the scale (temporal and spatial) at which we can access this information. Acknowledgements We thank residents of the study area who participated in the survey. Without their participation, we would not have a project. This project has been assisted by the New South Wales Government through its Environmental Trust. Mike Fleming and Liz Tasker of OEH provided support for the survey, particularly in areas surrounding Warrumbungle National Park.

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