The recent decline of a New Zealand endemic: how and why did populations of Archey s frog Leiopelma archeyi crash over ?

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1 BIOLOGICAL CONSERVATION Biological Conservation 120 (2004) The recent decline of a New Zealand endemic: how and why did populations of Archey s frog Leiopelma archeyi crash over ? Ben D. Bell a, *, Scott Carver a, Nicola J. Mitchell a, Shirley Pledger b a School of Biological Sciences, Victoria University of Wellington, P.O. Box 600, Wellington, New Zealand b School of Mathematical and Computing Sciences, Victoria University of Wellington, P.O. Box 600, Wellington, New Zealand Received 6 January 2004; received in revised form 9 February 2004; accepted 10 February 2004 Abstract Dramatic changes have been documented in New Zealand s vertebrate faunas since human settlement, involving major declines and extinctions, but over recent years few species have declined in numbers so rapidly as the terrestrial Archey s frog Leiopelma archeyi (Anura: Leiopelmatidae). Long-term monitoring over more than 20 years revealed a major population reduction of the species over and L. archeyi is now classified as Nationally Critical under the New Zealand threat classification system. The decline progressed northwards in the Coromandel ranges, and mostly larger (female) frogs survived. On a 100 m 2 study plot at Tapu Ridge, annual population estimates averaged 433 frogs (SE 32) over , declining by 88% to average 53 frogs (SE 8) over A mean annual survival rate of 82% for most years declined to 33% over There is mounting evidence to suggest that disease is the major agent of decline, supported by (1) the rapidity and severity of decline, (2) the progressive (south to north) nature of decline, and (3) finding frogs with chytriodiomycosis from Batrachochytrium dendrobatidis at the time of decline. Surprisingly, sympatric populations of the semi-aquatic Leiopelma hochstetteri have not declined dramatically, nor has a western population of L. archeyi at Whareorino, despite chytridiomycosis occurring in some frogs there. Sustaining and restoring populations of L. archeyi in New Zealand raises major challenges for conservation management. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: Amphibian declines; Batrachochytrium dendrobatidis; Biodiversity conservation; Demography; Leiopelma archeyi; Leiopelma hochstetteri 1. Introduction Impacts of human settlement have had major effects on New Zealand s terrestrial vertebrate populations, involving major declines and extinctions (King, 1984). Over recent years, however, few endemic vertebrates have declined in numbers so rapidly as Archey s frog Leiopelma archeyi. This species is one of three extant terrestrial Leiopelma (L. archeyi, Leiopelma hamiltoni, Leiopelma pakeka) that inhabit forests and open ridge tops, while one semi-aquatic species (Leiopelma hochstetteri) occurs in wetter habitats alongside creeks and damp watercourses, and three other species are extinct * Corresponding author. Fax: address: Ben.Bell@vuw.ac.nz (B.D. Bell). (Worthy, 1987a; Bell et al., 1998a). Historical declines are thought to be due mainly to the impact of introduced mammalian predators and/or competitors, and to loss of habitat through forest removal (Bell, 1985a; Worthy, 1987a; Newman, 1996). The genus Leiopelma is one of the two least-derived (most primitive ) living anuran genera, and as such, extant species are of high conservation value. Until recently L. archeyi was widely distributed, generally at higher altitude ( m), through much of the Coromandel Peninsula on New Zealand s North Island, with a new population being discovered in the northern King Country, 150 km SW of the Coromandel Peninsula in 1991 (Bell, 1994; Thurley and Bell, 1994; Bell et al., 1998b). In both the Coromandel Peninsula and the King Country, L. archeyi broadly occurs in /$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi: /j.biocon

2 190 B.D. Bell et al. / Biological Conservation 120 (2004) sympatry with L. hochstetteri. L. archeyi lives and breeds in cool, secluded terrestrial sites under the cover of rocks, logs or vegetation under forest or on open mist-prone ridges. It is endotrophic and exoviviparous (following the terminology of Altig and Johnston, 1989) laying 1 10 eggs, with the male undertaking parental care of eggs and the hatchlings (Archey, 1922; Bell, 1985b; Bell and Wassersug, 2003). Global declines of amphibians have been of international concern for more than a decade (Wake, 1991; Waldman and Tocher, 1998; Alford et al., 2001; Gardner, 2001; Halliday, 2001), and declines of New Zealand frogs were feared before they eventuated (Bell, 1996; Newman, 1996). In January 1995, 29 dead L. archeyi were collected by the Department of Conservation on Tokatea Ridge after a prolonged drought (R. Chappell, pers. commun.). By late 1996 a major population reduction on Tapu Ridge was detected. Concerns increased when a further population reduction of L. archeyi was recorded in 1998 on Tokatea Ridge. In 1999 Batrachochytrium dendrobatidis, a fungal pathogen, was recognised for the first time in New Zealand in Litoria raniformis (Waldman et al., 2001) and pathological investigations were initiated. In July 2001 we found a dead L. archeyi from relatively pristine forest on Te Moehau, Coromandel, infected with chytrid fungus. L. archeyi is now classified as Nationally Critical under the New Zealand threat classification system (Hitchmough, 2002). In this paper we detail evidence of the dramatic population reductions of L. archeyi in New Zealand, and we review possible reasons for these declines. 2. Materials and methods 2.1. Study areas Since the early 1970s, we have surveyed populations of L. archeyi in three study areas on the Coromandel Peninsula on the North Island of New Zealand Tapu Ridge, Tokatea Ridge and Te Moehau Mountain (Fig. 1). Periodic observations have also been made in Whareorino Forest, in the northern King Country, since the discovery of L. archeyi there in Population monitoring Unlike many anuran amphibians, Leiopelma species have only limited vocalisations, hence population monitoring based on acoustic surveys is not possible. Leiopelma are instead located by daytime searches of retreat sites (under rocks or logs or within dense vegetation), or by counting numbers of emerged individuals at night. Our most rigorous population estimates for L. archeyi were obtained from an annual survey of a 1010 m study plot on Tapu Ridge that has operated since Fig. 1. Location of study sites in the Coromandel Peninsula and at Whareorino, New Zealand (a 55 m sector of the same plot was first used in 1982). Frogs were located by day in progressive searches across the study plot. Captured frogs were weighed, measured (snout-vent and tibiofibula), and, if new, individually toe-clipped before release at the site of capture at the end of the search. Toe samples taken over were preserved in 70% ethanol and are available for further study, including retrospective assessment of chytrid fungus infection. Younger frogs were aged on body size, with reference to known lengths at metamorphosis determined from captive breeding studies, and from growth curves of known-age individuals successively recaptured on the study plot (Bell, 1978, 1994). L. archeyi cannot be sexed on external morphology, except for females attaining a greater body size than males (Bell, 1978). The sex of some females was confirmed through observation of yolky eggs through the abdominal wall (Bell, 1978, 1985b). Those adults found guarding eggs or hatchlings at nest sites are deemed to be males, as the male undertakes parental care in terrestrial Leiopelma species (Bell, 1985b). Many individuals have multiple recaptures over many years, so their ultimate body-size can be established, increasing the likelihood that their sex can be estimated from size.

3 B.D. Bell et al. / Biological Conservation 120 (2004) In addition to the study of marked frogs at Tapu, L. archeyi (and L. hochstetteri) were surveyed elsewhere in Coromandel and at Whareorino, either using measured transects or more general searches. These surveys allowed broad comparison between areas and species: the number of frogs found per unit search effort (no. frogs/ 100 sites searched) and the number found per unit search time (no. frogs/hour). Frogs were found by day under the cover of retreat sites, although after rain some L. archeyi were seen out of retreat sites on the ground or perched in low vegetation. In searches on Te Moehau, at Tokatea and in some areas of Tapu Ridge, day searches were repeated along the same transects, without the use of measured transects or grids (Bell, 1978, 1996). Elsewhere, measured transects were used (Bell, 1996; Perfect, 1996). Searches were also made at night, especially at Tapu and Te Moehau Mark-recapture analysis Population and survival estimates for the mark-recapture plot at Tapu used the Jolly-Seber model (Seber, 1973). The likelihood formulation by Schwarz and Arnason (1996) was chosen; this allows for Akaike s information criterion (AIC) comparisons with simpler models (see, e.g., Burnham and Anderson, 1998) and does not give survival estimates above one. Cruder population indices based on raw capture data were provided by the number of captures per sampling visit, and the minimum number of frogs known to be alive (following Krebs, 1998). 3. Results 3.1. Population trends of L. archeyi in the Coromandel Peninsula Population reduction on Tapu Ridge Day searches of the 100 m 2 study plot at Tapu Ridge over resulted in 980 captures of 638 individual L. archeyi and 10 L. hochstetteri. The estimated age of the oldest L. archeyi recaptured was 23 years, and the oldest L. hochstetteri 12 years. The mean snout-vent length of 26 brooding L. archeyi, assumed, and in some cases confirmed, to be male (Bell, 1978), was 28.3 mm, ranging from mm. Snoutvent lengths of females ranged from 27 to 37 mm (Bell, 1978). Despite the overlap in sizes of males and females, larger adults over 31 mm SVL were regarded as females. Initially, the number of frogs caught per visit generally increased, but a marked reduction occurred between 1994 and 1996, captures remaining low thereafter (Table 1). Trends of the minimum number alive statistic are broadly similar to those for the number of captures (Table 1). Table 1 The number of L. archeyi captures and the minimum numbers alive on the Tapu Ridge study plot, Date sampled Number of captures Minimum number alive Aug Jan Feb Feb Dec Feb Feb Feb Jun Jan Feb Dec Dec Feb Feb Feb Feb Dec Dec Dec Dec The gap represents the time of decline. Jolly-Seber estimates provide a more robust estimate of population size (Fig. 2) and also showed a major population reduction between 1994 and The mean population before the decline ( ) was 433 frogs (SE 32), dropping by 88% to a mean of 53 frogs (SE 8) over A simpler model with constant capture probabilities over time is supported (with AICc lower than for the full Jolly-Seber model by 19.6), which indicates why the numbers of captures and the minimum number alive are acting as indices for the population size in this particular study. Means before and after the decline were (69.0, 12.0) for the number of captures and (100.5, 19.0) for the minimum number alive, representing population reductions of 82.6% and 81.1%, respectively. There was no support for a model with constant annual survival rates (AICc 5.9 higher than for full Jolly-Seber). A major decline and recovery in annual survival rates was observed (Fig. 3). The mean annual survival rate is 0.82 (SE 0.05) for and , but reduced to 0.33 (SE 0.08) over Lower survival is also indicated for The lower rate for the last sampling period is assumed to have the negative bias usual in final estimates of the Jolly-Seber model, while standard errors could not be computed for the last two survival estimates (Fig. 3). Indices of frog numbers elsewhere on Tapu Ridge were obtained from searches (by B.D.B.) over The percentage of sites with L. archeyi averaged 12.7% (range %) in three general searches at

4 192 B.D. Bell et al. / Biological Conservation 120 (2004) Nhat Aug-1983 Jan-1984 Feb-1985 Feb-1986 Dec-1986 Feb-1988 Feb-1989 Feb-1990 Jun-1991 Jan-1993 Feb-1994 Dec-1994 Dec-1996 Feb-1997 Feb-1998 Feb-1999 Feb-2000 Dec-2000 Dec-2001 Dec-2002 Dec-2003 Sampling dates Fig. 2. Jolly-Seber population estimates of population size (Nhat) of L. archeyi on the Tapu Ridge study plot, Error bars ¼ 1 SE Annual survival rate Aug-1983 Jan-1984 Feb-1985 Feb-1986 Dec-1986 Feb-1988 Feb-1989 Feb-1990 Jun-1991 Jan-1993 Feb-1994 Dec-1994 Dec-1996 Feb-1997 Feb-1998 Feb-1999 Feb-2000 Dec-2000 Dec-2001 Dec-2002 Dec-2003 Sampling visits Fig. 3. Annual survival estimates (Phi) of L. archeyi on the Tapu Ridge study plot Error bar ¼ 1 SE. Following convention, initial dates are given for intervals over which survival rates are calculated. Standard errors could not be computed for the last two estimates.

5 B.D. Bell et al. / Biological Conservation 120 (2004) Table 2 Comparison of 1983 and 1998 transect searches for L. archeyi in a relatively undisturbed area of native forest on Tapu Ridge Dec-1983 Feb-1998 % Decline No. L. archeyi found % No. L. archeyi/h % No. L. archeyi/100 sites % Tapu over , but only 1.7% (range %) in two searches over a significant population reduction of 87.0% (generalised linear model with binomial responses, v 2 ¼ 79:6751, p < 0:001, df ¼ 1). Searches along a 252 m transect in December 1983 and February 1998, in an otherwise undisturbed area adjacent to the mark-recapture plot, revealed that a significant reduction of 76 78% had occurred (v 2 ¼ 14:163, p < 0:001, df ¼ 1; Table 2). The mean number of L. archeyi found by Perfect (1996) on 10 monthly transect counts on Tapu Ridge over January October 1995 was 87.4 frogs (SE 8.66, range ), but a repeat count in February 1997 revealed only 15 frogs a mean reduction of 83% Population reduction on Tokatea Ridge While L. archeyi had become scarce on Tapu Ridge by December 1996, an equivalent decline was not evident on Tokatea Ridge in February 1997, but numbers had crashed by November 1998 (Table 3). More general searches for L. archeyi at Tokatea confirm the decline registered on the main transect. There is evidence to suggest that L. archeyi in the central Coromandel ranges between Tapu and Tokatea are also scarcer than formerly. In a two-hour search in 1993, R. Thorpe (pers. commun.) found six frogs at Manaia, but an eight hour search in the same area in 1999 revealed no frogs Population reduction on Te Moehau In suitable areas on Te Moehau L. archeyi was formerly abundant (Stephenson and Stephenson, 1957; Bell, 1978). Search indices over the period September 1973 to October 2001 show that a marked decline occurred there also, but was not evident until L. archeyi was readily located by Ongohi hut in April 2001, but by July the species was extremely difficult to find, as well as subsequently (Fig. 4). One of two dead L. archeyi we found near Ongohi hut in July provided the first case of chytridiomycosis in Leiopelma. Only four live L. archeyi were found there in both July and October 2001, while no L. archeyi were found in a three hour search near Te Hope hut in October 2001, despite favourably wet weather Change of size distribution of L. archeyi after the decline Comparison of size distributions of L. archeyi before ( ) and after ( ) the decline on Tapu Ridge shows that proportionately more large frogs (>30 mm snout-vent length) were caught after the decline (Mann Whitney U test, z ¼ 2:7775, p ¼ 0:003, n ¼ 13). These would be mostly females (Bell, 1978, 1994). Not only did the frogs size distribution change at Tapu after the decline (Fig. 5), but their relative condition (weight for given length) was significantly greater. The mean condition index (100 (log weight/log snoutvent length)) of frogs greater than 20 mm snout-vent length was lower (24.7) in , before the decline, than afterwards (32.8; Mann Whitney U test, p < 0:001, n ¼ 237). This difference in part reflects the greater proportion of larger, gravid females captured after the decline, but may also indicate a better overall condition of frogs at lower density, as found in L. pakeka following translocation on Maud Island (Bell et al., 2004). To check this, weights and lengths of larger frogs with snout-vent lengths greater than 31.0 mm (females) were compared. Their condition indices before (33.6) and after (38.3) the decline were still significantly different (Mann Whitney U test, p < 0:001, n ¼ 94), suggesting that surviving female frogs of similar size were indeed in better condition. Several juveniles (<20 mm snout-vent length) were caught after the decline, providing evidence of continued breeding (also a male was found on an egg cluster 5 m from the plot in December 2001). Most surviving L. archeyi found at Tokatea after the decline Table 3 Leiopelmatid frogs located along the transect on Tokatea Ridge There was one observer over , two observers over Nov-1995 Feb-1997 Nov-1998 Dec-2000 Dec-2003 L. archeyi/100 sites L. hochstetteri/100 sites L. archeyi/h L. hochstetteri/h Sites searched Search time (min) No. L. archeyi No. L. hochstetteri

6 194 B.D. Bell et al. / Biological Conservation 120 (2004) Fig. 4. Capture rate of L. archeyi on Te Moehau (frogs h 1 ) over BDB, surveys by B.D. Bell (west slopes and below summit); DOC, surveys by Department of Conservation on east slopes at m; VUW, surveys by Victoria University of Wellington (N.J.M., S.C.) near Ongohi and Te Hope huts. Fig. 5. L. archeyi size distribution on the Tapu Ridge study plot before ( ) and after ( ) the population decline. (n ¼ 6) also were larger frogs in the female size range (mean snout-vent 33.3 mm, range mm), as at Tapu (Fig. 5). A young L. archeyi found at Tokatea in December 2003 (snout-vent length 17.1 mm) provides evidence of continued breeding there Population trends in L. hochstetteri Unlike L. archeyi, no major declines of L. hochstetteri are evident. The mean number of L hochstetteri found by Perfect (1996) on 10 monthly transect counts on

7 B.D. Bell et al. / Biological Conservation 120 (2004) Tapu Ridge over January October 1995 was 39.2 frogs (SE 2.98, range 30 55), but a repeat count in February 1997 revealed 22 frogs, which was below the minimum count for Along the Tokatea Ridge transect L. hochstetteri remained common (Table 3). Five counts by B.D.B. along the upper reaches of Driving Creek, west of Tokatea Ridge, revealed varying numbers of L. hochstetteri over thirty years ( ), successive search indices (frogs h 1 ) being: 12.0 (February 1972); 5.6 (December 1972); 12.5 (September 1973); 7.8 (November 1995); 6.7 (February 2002). L. hochstetteri remained common during the period of marked L. archeyi decline on Te Moehau in 2001, search indices being 3.6 and 4.6 frogs h 1 at Ongohi Hut in July and October 2001, and 1.9 frogs h 1 at Te Hope Hut in October In conclusion, from available survey data there is no evidence of a decline of L. hochstetteri in Coromandel as seen in L. archeyi, although more monitoring of the species is needed to provide data equivalent to those available for L. archeyi. 4. Discussion Since human settlement, all extant species of Leiopelma have suffered range reductions in New Zealand, with three species going extinct (Worthy, 1987a; Bell, 1994). It is recognised that these past declines or extinctions are likely to have resulted particularly from the impact of introduced mammals, and also from habitat loss (Bell, 1985a, 1994; Newman, 1996). On the other hand, faunal surveys over recent decades resulted in extensions of known ranges of both L. archeyi and L. hochstetteri in the North Island, including the discovery of both species in Whareorino forest in the northern King Country (Bell, 1994; Thurley and Bell, 1994; Newman, 1996). It should be noted, however, that their ranges were far more extensive in the Late Holocene (Worthy, 1987b). In 1996, at a time of increasing worldwide concern for declining amphibian populations (Vial and Saylor, 1993; Carey and Bryant, 1995; Laurance et al., 1996), it was seen as important for trends in New Zealand s amphibian populations to be adequately monitored for early identification of potential problems (Bell, 1996; Newman, 1996). Previously, there had been only anecdotal reports of recent frog declines in New Zealand, and these were of introduced Litoria species (Bishop, 1999) Value of long-term monitoring In order to elucidate real declines from stochastic fluctuations, Gardner (2001) notes that a long time series is highly desirable, although few studies are longer than five years, and even fewer are more than 10 (Alford and Richards, 1999; Houlahan et al., 2000; Marsh, 2001; Young et al., 2001). Populations of terrestrial-breeding amphibians fluctuate less than their aquatic-breeding counterparts (Marsh, 2001), thus our Tapu dataset spanning two decades provides unequivocal evidence of a population decline. Had this study not been carried out, the decline may well have been overlooked, or at least not identified for some time. The decline was so substantial that less sensitive search indices also revealed it Progressive northward decline in Coromandel The decline of L. archeyi at Tapu Ridge is placed between December 1994 and December 1996 from mark-recapture data (Table 1, Fig. 2). Additional evidence, however, suggests that L. archeyi remained abundant through 1995: substantial numbers (n ¼ 91) were located on 1080-monitoring transects as late as October 1995 (Perfect, 1996). Even by mid-1996 the species was still comparatively common, for members of the Native Frog Recovery Group had no difficulty in finding frogs then (D.G. Newman, pers. commun.). By mid-november 1996, however, only one frog was found after well over 100 sites were searched (K. Corbett, pers. commun.). That scarcity was confirmed on the study plot the following month (Table 1), while a more general search in early January 1997 again revealed very few frogs (A. Styche, pers. commun.). Although dead L. archeyi were found at Tokatea in 1995, the major decline there occurred between February 1997 and November 1998 (Table 3). On Te Moehau, the onset of the decline in the Department of Conservation survey area at m altitude appears to have been by January 2001, although by July numbers had decreased further (Fig. 4). While the years of decline of L. archeyi are only estimated reliably for Tapu, Tokatea and Te Moehau, they indicate that the decline progressed northwards at an average rate of about 12 km per year or 1 km per month What caused the decline? Numerous factors may have contributed to declines of L. archeyi on the Coromandel Peninsula, including (1) human disturbance, (2) habitat loss, (3) chemicals such as biocides, (4) mammalian predation, (5) climatic factors, and (6) disease. Each of these potential factors is discussed below in light of the available evidence. We do not consider effects of potential increases in ambient ultraviolet-b (UV-b) radiation (cf. Adams et al., 2001), as L. archeyi eggs are brooded in cryptic locations and adults spend daylight hours in retreats Human disturbance In December 1996, when a decline had only been recorded on the 100 m 2 study plot on Tapu Ridge, a

8 196 B.D. Bell et al. / Biological Conservation 120 (2004) local disturbance event was a possibility. Conceivably frogs might have been deliberately and illegally collected from the site. Indeed, many rocks had been disturbed there early in 1997, presumably in a search for frogs, but not before the decline was first noted in December. Our annual day searches at the site would also have had some impact, since retreat sites can be drier as a result of lifting rocks (Bell, 1996). It is very unlikely, however, that such activity would cause the sudden and major decline in Further, we are aware that frogs are likely to have experienced initial handling stress through our individual marking regime. However, survival rates were relatively high over most of the study period (when most frogs were marked), showing that marking had minimal impact on future survival, and was not a factor in their sudden decline. Moreover, surveys elsewhere in the Tapu area in 1997 and 1998 confirmed that the decline was widespread, so human disturbance can be discounted as a major agent of recent decline Habitat loss More general habitat loss within the range of L. archeyi in Coromandel did not occur to any extent during the period of decline. Indeed, the species has been resilient to major habitat changes in the area since European settlement, such as logging and gold mining operations, although such activity is likely to deplete numbers (Bell, 1985a). Habitat loss can therefore also be discounted as a major agent of recent decline Chemicals There is no evidence that chemicals, such as pollutants or agrochemicals, had an impact on L. archeyi. However, the decline at Tapu Ridge did occur the year after a sodium monofluoroacetate (1080) poison drop, so it is important to assess whether 1080 was a factor in the decline (the study plot was within the 1080 drop zone). Fortunately, Tapu Ridge was the focus of a study to specifically monitor the short-term impact of 1080 on native frogs in 1995, so we have information on its likely effect. Substantial numbers (n ¼ 91) of L. archeyi were still found on survey transects in October 1995, four months after the 1080 operation (Perfect, 1996). A re-survey of the transect lines in February 1997 showed that the decline was not confined to areas where 1080 had been used, expected if the toxin had an effect, but also occurred in a control area where 1080 had not been used. This provided evidence that 1080 was not a direct agent of recent decline. The decline at Tokatea is further evidence, as it was again in an area in which 1080 had not been used. The literature suggests that L. archeyi may not be very susceptible to 1080, as high LD 50 doses have been calculated for a range of amphibians, suggesting that they are highly resistant (Hudson et al., 1984; McIlroy et al., 1985; Perfect, 1996) Mammalian predation Coromandel Leiopelma populations have coexisted with introduced mammalian predators for many decades, and no novel mammalian predators entered the study areas during the study period. Unlike L. archeyi at Whareorino forest (Thurley and Bell, 1994; T. Thurley, pers. commun.), there has been no direct evidence of rat predation on Tapu Ridge. Larger frogs might be expected to be at greater risk to rat predation than smaller frogs, as they may emerge more often and may be less able to occupy retreat sites inaccessible to predators: the rat-predated L. archeyi found at Whareorino in were all adults (Thurley and Bell, 1994). Survivors found at Tapu and Tokatea tended to be larger individuals, however, suggesting that predation was not a prime agent of decline there. Side effects of 1080 poisoning, if any, are hard to predict. The 1080 operation was aimed at reducing numbers of introduced brushtail possums Trichosurus vulpecula, but it would also have reduced numbers of potential predators (e.g., ship rat Rattus rattus, stoat Mustela erminea), as well as invertebrates (Atkinson et al., 1995). Whether 1080 poisoning led to prey-switching in surviving predators is not known. Now that populations of L. archeyi are reduced in the Coromandel Peninsula, the impact of mammalian predation on them may become more significant there Climate change While climatic factors may contribute to population change and local distribution, weather conditions in the Coromandel Peninsula over were not particularly exceptional (Bishop, 1999). In January 1995, 29 dead L. archeyi were collected by the Department of Conservation on a 50 m stretch of the summit track at their type locality on Tokatea Ridge (R. Chappell, pers. commun.). This followed a thunderstorm, then sunshine, after a prolonged drought. The dead frogs were mainly in the adult size range. It is conceivable that heavy rainfall initiated movement of relatively weakened and dehydrated individuals to the exposed track, or had swept them there, and a sudden clearance to sunny weather might have exposed them to fatally warm conditions. Alternatively, other factors, such as disease, may have predisposed them to such mortality, but subsequent surveys confirmed that good numbers of L. archeyi were still to be found in apparently good condition at Tokatea in 1995 and The co-occurrence of a disease outbreak and a climatic anomaly remains a conceivable explanation for this event, but in general there is little evidence to suggest that climate has been the main causal factor in declines of L. archeyi in the Coromandel Peninsula Disease To date the identification of chytrid fungus has provided the most convincing relationship with the decline

9 B.D. Bell et al. / Biological Conservation 120 (2004) of L. archeyi in the Coromandel region. Pathological chytrid fungus Batrachochytrium dendrobatidis (phylum Chytridiomycota), described by Longcore et al. (1999), was first recognised in New Zealand in the introduced hylid frog Litoria raniformis in Christchurch in (Waldman et al., 2001). Chytrid fungus was found in L. archeyi at Te Moehau, Tapu and Whareorino in , being first recorded in a dead L. archeyi from Te Moehau in July The progressive northward declines of L. archeyi populations in Coromandel ( ) would support the notion of a spreading pathogen, with an average rate of about 12 km per year. If the causal factor is chytrid fungus, this suggests the pathogen was in Coromandel by late 1996, when the first decline occurred at Tapu, even though chytridiomycosis was not identified in New Zealand until (Waldman et al., 2001) and not at Tapu until Reports across New Zealand suggest that populations of introduced frogs (Litoria spp.) crashed over (Bishop, 1999). In the Coromandel region, declines of Litoria aurea were reported over (P. Thomson, in litt.). While dead L. archeyi infected with chytrid fungus have been found at Whareorino, no overall decline has occurred there, and the reasons for this are obscure Conclusion disease the most likely agent of decline On a global scale, declining amphibian populations cannot be attributed to a single cause for it appears that multiple, interacting causes are involved. We have considered various causal agents for the declines of L. archeyi in New Zealand, and several of these factors may have interacted to effect those declines. There is mounting evidence, however, that disease has been the major agent of decline, either directly, or indirectly through the frogs becoming susceptible as a result of other factors (e.g., Pounds, 2001). The disease argument is supported by (1) the rapidity and severity of declines, (2) the progressive (south to north) nature of the outbreaks, and (3) evidence of chytriodiomycosis infection in dead or sick frogs at the time of decline. In Australia, montane creek-dwelling species tend to have been most impacted by recent declines (Laurance et al., 1996; Berger et al., 1998), so we might have expected the semi-aquatic L. hochstetteri to be more affected in New Zealand. This was not the case - instead the terrestrial L. archeyi declined and was found to have chytridiomycosis. While chytrid fungus is associated with the frog s decline, it is not necessarily the main causal agent. We do not yet know enough of the pathology and epidemiology of this or other possible amphibian pathogens, nor of other factors that may have predisposed frogs to infection. Further, the mechanism of spread is uncertain, and those studying these frogs are well aware of the need to follow meticulous hygiene protocols, to prevent our spreading the pathogen (Bell, 2002) Future scenarios for Leiopelma species Leiopelma archeyi had sufficient resilience to survive severe habitat disturbance in Coromandel in the past, including gold mining, kauri logging, deforestation and introduced mammalian predators. However, it is a K- selected species with low clutch size, slow maturity and long lifespan. Theoretical population models (Southwood et al., 1974) indicate that there is a low population threshold for K-selected species below which extinction is likely, and a decline of around 80 90% could exceed such a threshold. Several scenarios for the future of Leiopelma species in New Zealand can be envisaged. The most optimistic scenario is that L. archeyi will persist and slowly recover from its decline and that other Leiopelma species will not be seriously affected, nor the Whareorino L. archeyi population. A pessimistic scenario is that L. archeyi will not recover and is edging towards extinction, and that the closely related L. hamiltoni and L. pakeka may also be at high risk. An intermediate scenario is that populations of L. archeyi will not recover to their former state, having become locally extinct in parts of their range, but will survive in lower numbers elsewhere, with other Leiopelma species not declining. As we understand so little of the pathology and epidemiology of any disease that might be affecting L. archeyi, it is hard to make definite recommendations for management to ensure protection against disease, although prudent preventative measures and contingencies need to be further developed. New Zealand has justifiably earned international respect for its success in conservation management of threatened endemic fauna such as endemic birds, where agents of decline can often be more readily tackled (Bell and Merton, 2002), but the appearance of a contagious disease in a native frog brings new and difficult challenges. Even if populations of L. archeyi persist, increased conservation management is now needed, such as habitat protection and predator control, supplemented with captive management. It is to be hoped that this archaic and attractive frog will survive despite the major population collapse it has recently experienced in its former Coromandel stronghold. Acknowledgements Kim McConkey kindly offered constructive comments on a draft of this paper. We thank all those who have assisted in the frog studies reported here, especially Ann Bell, Paul Bell, Oliver Berry, Roman Biek, Phil Bishop, Gill Brackenbury, Finn Buchanan, Rob Chappell, Mike Cogswell, Keith Corbett, Alison Cree, Kelly Hare, Kim McConkey, Leigh Marshall, Don Newman, Richard Norman, Alison Perfect, Chandra Ramarao,

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