Ibis (2018)
doi: 10.1111/ibi.12617
Short communication
Control of invasive predators improves breeding success of an endangered alpine passerine KERRY A. WESTON,1* COLIN F. J. O’DONNELL,1 2 PAUL VAN DAM-BATES & JOANNE M. MONKS3 1 Department of Conservation, Biodiversity Group, Christchurch Mail Centre, Private Bag 4715, Christchurch, 8140, New Zealand 2 Ecofish Research Ltd, Suite F – 450 8th Street, Courtenay, BC, V9N 1N, Canada 3 Department of Conservation, Biodiversity Group, PO Box 5244, Dunedin, 9058, New Zealand
Birds living in alpine environments are becoming increasingly impacted by human-induced threats. We investigated the impacts of introduced mammalian predators on an endangered alpine species, the New Zealand Rockwren Xenicus gilviventris, and assessed whether predator control improved its breeding success. Nest monitoring revealed that the primary cause of nest failure was predation by invasive mammals, primarily Stoats Mustela erminea and House Mice Mus musculus. Daily survival rates (DSR) decreased with nest age, and nests were at their most vulnerable to predators just prior to fledging. DSR, egg-hatching and fledgling rates were all improved by predator trapping, demonstrating the significant impacts that even low numbers of invasive predators can have on sensitive alpine and upland species.
Keywords: Acanthisittidae, elevation, nest survival, predation, Rockwren. Assessing the impacts of global change on alpine species is problematic, despite these being among the most vulnerable groups (Chamberlain et al. 2012, Brambilla et al. 2017). This is especially true for endangered species already at low densities, occupying challenging and inaccessible high-altitude habitats. For these species, even *Corresponding author. Email:
[email protected] Twitter: @gilviventris
© 2018 British Ornithologists’ Union
basic ecological information critical for identifying threats and developing effective conservation measures often remains lacking. In the Northern Hemisphere, major perceived threats to alpine birds are pastoral land abandonment, urbanization, leisure activities, forestry and the increasing threat of climate change (Sekercioglu et al. 2008, Scridel 2014, Ferrarini et al. 2017). Synergistic interactions among climate change and other drivers of global change represent one of the largest areas of uncertainty in projections of change to alpine ecosystems (Sala et al. 2000). For example, increasing temperatures may also drive elevational range expansion of a wider suite of invasive species (Chen et al. 2011, Christie et al. 2017). This in turn may have negative consequences for high-altitude biodiversity not previously exposed to the threat of invasive species (Pauchard et al. 2016). Predation by invasive mammals is a primary cause of ongoing decline and extinction of birds on oceanic islands globally (Blackburn et al. 2004). In alpine habitats, invasive predators are emerging as an important, although poorly understood, threat to biodiversity (Wilson et al. 2006, Smith et al. 2007, O’Donnell et al. 2017). The New Zealand Rockwren Xenicus gilviventris (hereafter Rockwren), is a small (14–20 g) alpine specialist, only found above the climatic tree line. Juveniles establish territories and form breeding pairs within the same season that they fledge, and commence nesting the following spring (Michelsen-Heath 1989). Generally, Rockwrens are socially monogamous across seasons (Michelsen-Heath 1989). The Rockwren is one of only two remaining members of an ancient endemic lineage of primarily ground-dwelling passerines (Acanthisittidae; Barker et al. 2002, Ericson et al. 2002, Higgins et al. 2006). The group once included at least eight species, although six have become extinct, largely attributed to the destruction of forest habitat and the introduction of mammalian predators (Tennyson & Martinson 2006, Worthy et al. 2010). It was long assumed that Rockwrens were buffered against the threats faced by their forest-dwelling conspecifics, given that their alpine habitat had undergone relatively minor modification (Heath, 1986, McGlone 1989). Recently, however, a range-wide decline of this species has been recognized (Michelsen-Heath & Gaze 2007) and their conservation status has been changed from Vulnerable to Endangered (Robertson et al. 2013, Birdlife International 2017). It has been suggested that introduced mammalian predators are responsible for the recent decline of Rockwrens (Michelsen-Heath & Gaze 2007). This is based on evidence of introduced Stoats Mustela erminea and House Mice Mus musculus preying upon Rockwren eggs and nestlings (Michelsen-Heath 1989) and the increasing recognition that invasive predators are widespread within the New Zealand alpine zones (O’Donnell et al. 2017). Despite the assumption that invasive predators
2
K. A. Weston et al.
are responsible for the decline of this species, the extent and effect of predation on Rockwrens has not been investigated. Conservation efforts aimed at recovering Rockwren populations are in their infancy and to date have focused on the perceived threat from invasive predators, involving localized trapping of mammalian predators by volunteer groups (Stocker et al. 2006), attempted translocations to predator-free offshore islands (Willans & Weston 2005) and, most recently, aerial poisoning of potential predators (Elliott & Kemp 2016). The objective of this study was to investigate the influence of invasive predators on the breeding ecology of Rockwrens by: (1) identifying predators visiting Rockwren nests and their predation rates and (2) investigating whether kill-trapping of invasive mammalian predators increases Rockwren breeding success. METHODS Study sites Breeding success of Rockwrens was monitored in three study areas. The Haast Range study site (c. 400 ha, 1100–1500 m a.s.l.) in Mount Aspiring National Park (44.09°S, 168.79°E; Fig. S1) is primarily snow tussock Chionochloa spp. grassland interdispersed with patches of subalpine scrub, rocky bluff systems, scree slopes and boulder fields. The Homer-Gertrude Cirque site (c. 200 ha, 850–1200 m a.s.l.; 44.76°S, 168.00°E) in northern Fiordland National Park is composed of extensive boulder fields and prostrate herbs, with large areas of subalpine scrub and snow tussock. The Lake Roe site (c. 500 ha, 900–1100 m a.s.l.; 45.70°S, 167.14°E) in southern Fiordland National Park encompasses extensive snow tussock grasslands interdispersed with patches of subalpine scrub, rocky bluff systems, scree slopes and boulder fields. Monitoring Rockwren nests Nest monitoring occurred over five breeding seasons, 2012–17 (Table 1). Field teams commenced searching the study areas for nests at the beginning of the breeding season in October each year. Territory mapping (Bibby et al. 2000) was undertaken to aid in identifying
breeding pairs and potential nest-sites. Attempts were made to ensure all birds were colour-banded at the beginning of each breeding season, but with further birds banded opportunistically throughout (including fledglings as they became available). The locations of all colour-banded and unbanded birds were recorded as encountered using GPS units (Garmin GPSMAP 64s or 62s). Field teams (usually two people per team) searched the study areas for nests on a weekly basis, commencing at the beginning of the breeding season in October each year. Nest activity (incubating, feeding nestlings, fledged, failed) was recorded during visits at least once every 4 days using binoculars from a distance to minimize disturbance. For nests that could be accessed safely, the number of eggs and nestlings were recorded at each visit. Continuous 24 h recording and motion-triggered camera set-ups were also used at a subset of nests (38 of 146 nests, 26%) to monitor nesting behaviours and outcomes, and to identify predators (for details of equipment, see Little et al. 2017). Cameras were not set up until eggs had been laid to reduce the risk of nest abandonment. A nest was considered successful if at least one chick fledged. If the nest was no longer active and close to the estimated fledging date, fledging was only confirmed if either the fledging event was captured on nest cameras or the parents and at least one fledgling could be located. Predator trapping We used a BACI (before-after control-impact) design with two replicates and a non-treatment site. This design is less optimal than switching treatments, but it was adapted due to conservation concerns, i.e. it was inappropriate to cease predator control once initiated due to the risk of population extinction. Predator trapping occurred in the Homer-Gertrude Cirque and Haast Range after one and two seasons of non-treatment, respectively. The Lake Roe site was not trapped (Table 1). Traps used were DOC150 and DOC200 models, which are designed to target mustelids and Rats Rattus spp. humanely (Poutu & Warburton 2005). At Homer-Gertrude Cirque, predator trapping was established in the 2013–14 season by local conservation
Table 1. Schedule of treatment (predator trapping) and non-treatment of Rockwren study sites and number of nests monitored with a known outcome (n) in the South Island of New Zealand, 2012–17. Year
Haast Range
n
Homer-Gertrude
n
Lake Roe
n
2012–13 2013–14 2014–15 2015–16 2016–17
– Non-treatment Non-treatment Treatment Treatment
–
Non-treatment Treatment Treatment Treatment Treatment
20 – 8 16 20
– – Non-treatment Non-treatment Non-treatment
– –
© 2018 British Ornithologists’ Union
9 11 8 22
9 4 13
Invasive predator impacts on alpine rock wren
volunteer groups. The network consisted of 37 kill traps (c. 200 m apart and covering c. 200 ha of habitat). In the Haast Range, a predator trapping network was established in September 2015, consisting of 89 kill traps spaced 200 m apart and covering c. 400 ha of habitat. The number of traps remained constant among years. Traps in both areas were checked and re-baited monthly with hen’s eggs, fresh rabbit or dehydrated rabbit, between October and May each year.
3
best model were considered important in explaining variation in the data. To estimate the probability of overall nest survival, the product of the DSRs for the duration of nesting (44 days) was calculated using the estimates from the top performing model. Standard errors (se) were based on 1000 simulations from a multivariate normal distribution (Cooch & White 2017).
RESULTS Breeding success analysis The mean number of eggs laid, eggs hatched and nestlings fledged (se) was calculated for each nest that could be accessed at the egg stage. Hatching and fledging rates were compared between nests in trapped and non-trapped sites. The proportion of eggs hatching (conditional on the number of eggs) and the proportion of hatched eggs fledging were both modelled as a binomial response in a logistic mixed effect regression with a fixed effect of trap (presence or absence of traps at the site in a given year), and a random effect of nest to account for within-nest variability (re-nests were assigned a different number to first attempts), using R 3.2.5 (package lme4; Bates et al. 2015, R Core Team 2016). Apparent nesting success, defined as the percentage of nests that produce at least one young, is biased depending on when in the nesting cycle a nest is located; that is, the longer a nest is monitored, the more likely it is that a nest failure will be observed (Mayfield 1961). To correct for this bias, we used the nest survival model developed for program MARK (White & Burnham 1999, Rotella 2006), using the package RMark (Laake 2013) in R 3.2.5 (R Core Team, 2016). Maximum likelihood estimates of daily survival rate (DSR) of the nest were calculated across the whole nesting period, which for Rockwrens was defined as an incubation phase of 20 days, followed by a 24-day nestling phase (Michelsen-Heath 1989). The impact of predator control (trapping) on DSR was assessed against site, year, elevation above the treeline (metres), the number of days a nest was active (‘nest age’) and the time within the breeding season that a nest was initiated (‘time’). Linear and quadratic relationships between DSR, and both time and nest age, were explored. We also examined the interaction between trapping and each covariate to investigate whether the effect of trapping differed among sites, years and with elevation, time or nest age. Model selection was performed using Akaike’s information criterion corrected for small sample size (AICc) (Akaike 1973, Burnham & Anderson 2002). The best (most parsimonious) model was used to evaluate the change in DSR with predator control, and other models within the top model set (DAICc < 2) were considered when interpreting results. All covariates included in the
Nesting began in early October (austral spring), with the last nests fledging by mid-February. In total, 146 nests were located, all above the treeline. An almost completely enclosed, spherical or elliptical-shaped nest was built inside an excavated cavity, with a single entrance hole at or towards one end. Nest building was conducted by both sexes. Nests were most commonly built within cracks, or vegetated ledges on rock faces and large free-standing boulders (see Fig. S2 for images of typical nesting habitat). Nests were distributed along an elevational gradient of approximately 500 m. The contents of 31 nests were accessible during incubation across all sites. Mean clutch size was 3.97 0.11 se (range two to five eggs). Both male and female Rockwrens incubated eggs during the day. A regular pattern of incubation was established several days after the last egg was laid, with each parent alternating in attendance for periods averaging 35 min (21 pairs, 34.52 1.30 min, range = 10–62 min). Video monitoring showed that only the female incubated eggs during the night. The mean number of eggs hatched per nest was 1.81 0.30 (range 0–4, n = 31). Both male and female Rockwrens fed and brooded young. As for incubation, only females brooded at night. Time spent brooding young decreased as the nestlings grew and demands for food increased. During the final week of the nestling phase, large food items were being delivered to the nest every 3–4 min (13 pairs, 3.7 0.4 min) during daylight hours. Nestlings became increasingly noisy and could be seen at the nest entrance in the days prior to fledging. Broods of nestlings fledged synchronously, calling frequently. Overall, 0.97 0.28 chicks (range 0–4, n = 30) fledged per nest. Re-nesting of the same pair was observed both after failed nesting attempts (14 of 140 nests, 10%) and after successful nesting attempts (7 of 140 nests, 5%). One pair commenced building of their second nest while still feeding nestlings in their first nest.
Causes of nest failure Of the 146 nests monitored, the outcome (success or fail) was confirmed for 140 nests. In total, 46% of nests (n = 65) were successful. Predation was the most common cause of nest failure, with evidence of predation
© 2018 British Ornithologists’ Union
4
K. A. Weston et al.
recorded at 48% of failed nests (n = 36). Evidence included camera footage, damage to nests, the presence of remains, bite/gnaw marks, faeces and fur. Most confirmed predation events were by mustelids (17 of 36 nests; 47%) and, to a lesser extent, House Mice (4 of 36 nests, 11%). Mustelid predation was the primary cause of nest failure when predator control was not in place; in contrast, no mustelid predation events were confirmed when predator control was established. Stoats were the only mustelids identified to species and were captured on cameras at all three sites (n = 15 nests). They characteristically removed the entire nest contents (eggs, nestlings and brooding adults) and left nest entrances enlarged. Mice gnawed and cracked open eggs in the nest, leaving behind broken eggshell, and preyed upon nestlings, leaving gnaw marks and fatal wounds. Rat (spp. unknown) faeces were found in one nest which also contained two dead chicks and part of a head. Possum Trichosurus vulpecula gnaw marks were identified on the eggs from one nest. Nest abandonments were the most common known cause of nest failure when predator control was in place (Table S1). At least three of these abandonments appear to have been weather-related, occurring during periods of heavy snow. On one occasion, during a snowstorm which lasted several days, a nest became completely buried by snow. The birds continued to burrow through the snow to the nest, although they subsequently abandoned its three chicks nearing fledging. The cause of failure was unknown for 26 nests. Invasive mammal control and breeding success Thirty-three Stoats were trapped within the treatment areas during the study period (Haast Range = 16; Homer-Gertrude Cirque = 17). Stoat captures were generally low, but highest during the Rockwren chick brooding phase (Fig. S3). Ten rats Rattus spp. and one House Mouse were also caught during the study period. Of the 31 nests monitored from egg-laying to completion, the proportion of eggs hatched per nest was higher with predator trapping (0.56 0.10, n = 18) than with no predator management (0.32 0.09, n = 13), although this was not significant based on the logistic mixed effect regression (b = 1.98 1.18, P = 0.09). Given the number hatched, the proportion of chicks that fledged per nest was significantly higher when predators were controlled (0.69 0.12, n = 12) than with no predator control (0.14 0.14, n = 7; b = 18.43 5.94, P = 0.002). Only one of 13 nests fledged chicks when there was no predator trapping. There were sufficient data from 133 Rockwren nests to estimate DSRs. The best fitting model of daily survival was traps + nest age + site (Table S2). Based on this best model, DSR was substantially improved by trapping,
© 2018 British Ornithologists’ Union
decreased with nest age and differed among sites (Table 2, i.e. 95% confidence intervals do not overlap zero; Fig. 1). The next best model, equally supported, included year instead of site (DAICc = 0.47), suggesting that the environmental factors influencing both temporal and spatial variation are important. Models containing elevation, a quadratic relationship of nest age and time, and interactive effects had little support. Overall Rockwren nest survival rates ranged from 2% to 28% at sites without predator control and from 47% to 67% where predator control was in place (Table S3). The evidence for the impact of predation on Rockwrens is strong, despite design limitations (i.e. the inability to switch treatments). DISCUSSION Although Rockwrens appeared well-adapted to breeding in the extreme alpine conditions, the primary cause of nest failures was predation by invasive mammals. Breeding success of Rockwrens was improved substantially by predator trapping at both sites where it was implemented, even with low numbers of predators being trapped across the landscape. This indicates that relatively low numbers of predators can have a significant impact on the breeding success of sensitive alpine species. Removal of invasive predators has been shown to improve the breeding success of a diversity of threatened lowland bird species (Smith et al. 2010). We identified Stoats as the primary predator of Rockwrens. The widespread impacts of invasive Stoats on birds within other ecosystems is well known, although rarely studied in an alpine environment (King & Powell 2007, Innes et al. 2010, O’Donnell et al. 2017). Following Stoats, House Mice were the next most common nest predator. Mouse predation on nesting passerines is rare, although introduced House Mice on offshore islands are significant predators of seabirds (Wanless et al. 2007, Jones & Ryan 2009). Wanless et al. (2007) suggested that in ecosystems where Mouse populations are released from the ecological effects of other Table 2. Beta estimates for the effects of predator trapping, nest age and site on daily nest survival rates of Rockwrens at Haast Range, Mount Aspiring National Park; Homer-Gertrude Cirque, Fiordland National Park; and Lake Roe, Fiordland National Park, New Zealand, 2012–17. Estimates are given on the logit scale, where Lake Roe is the reference habitat (i.e. estimate = 0). The 95% confidence limits are shown.
Intercept Trapping Nest age Haast Homer-Gertrude
Estimate
se
4.173 1.791 0.026 0.590 1.240
0.411 0.300 0.013 0.347 0.356
LCL
UCL
3.366 1.203 0.051 1.270 1.940
4.979 2.380 0.002 0.091 0.544
Invasive predator impacts on alpine rock wren
5
Figure 1. Daily survival rates of Rockwren Xenicus gilviventris nests at Haast Range, Mount Aspiring National Park (n = 49); Homer-Gertrude Cirque, Fiordland National Park (n = 58); and Lake Roe, Fiordland National Park (n = 26), New Zealand, 2012–17. Estimates are from the model including predator traps, nest age and site. Shaded bands show 95% confidence intervals.
predators and competitors, they may become predatory. There is some evidence that House Mice reach high densities in alpine habitats, particularly in years when snow tussocks are mast seeding (Wilson & Lee 2010). It is likely that Stoat populations also increase following mast years in response to the increased abundance of mice above the treeline, although evidence for this relationship in alpine ecosystems is currently lacking (O’Donnell et al. 2017). Although rats are among the most common predators of New Zealand forest birds (Innes et al. 2010), rat predation was only recorded once at a Rockwren nest. Rats are relatively uncommon at higher elevations in New Zealand, probably attributable to a climatic preference for warmer, lower elevation habitats (Christie et al. 2017, O’Donnell et al. 2017). However, global warming may result in range shifts in rats to higher elevations (Christie et al. 2017). The energetic advantages of cavity-roosting and nesting, especially in harsh climatic conditions, are well recognized (Cooper 1999, Rhodes et al. 2009). However, this same adaptation also makes cavity nesters with relatively shallow excavations particularly vulnerable to
predation by introduced mammals (Innes et al. 2010, Yoon et al. 2016). The length of the nesting period of Rockwren (44 days; Michelsen-Heath 1989) is unusually long for a small passerine and also increases vulnerability to predation (Martin 1995). Rockwrens evolved in the absence of mammalian predators and, consequently, a prolonged nesting period may not be unexpected given the absence of this selective pressure until only recently (Reme^s & Martin 2002). Daily nest survival rates decreased with nest age, with nests at their most vulnerable to predators just prior to fledging. This trend is as expected in altricial species, where the adults make more feeding visits to the nest as nestlings grow, increasing conspicuousness to potential predators (Dinsmore et al. 2002). Rockwren nestlings also provide more auditory cues to predators as they develop. All small mustelids have acute senses of sight, hearing and smell, although they often hunt more by hearing than by sight (King & Powell 2007). Relatively higher mustelid trap catch during the Rockwren chick brooding phase (mid-December to February) coincides with end of the Stoat breeding season in New Zealand and the time that the young Stoats start
© 2018 British Ornithologists’ Union
6
K. A. Weston et al.
venturing from their dens (King & Powell 2007). With higher numbers of Stoats across the landscape, the threat to alpine species at this time is considerable. Nest survival was higher at Lake Roe than at other sites during non-treatment years. It may be that in this southern Fiordland site there are fewer predators because of the harsher environment and fewer masting events (which drive periodic predator irruptions; Wilson & Lee 2010). It is in these mountains that the last populations of several predator-vulnerable endangered species persisted on mainland New Zealand (Mills et al. 1984, Elliott et al. 2001), and where Rockwren numbers still appear highest (Michelsen-Heath & Gaze 2007). At present, techniques for monitoring Stoats in the alpine zone are under development (Smith & Weston 2017); consequently predator abundance data do not currently exist directly to test this hypothesis. Predator control involved only ground-based trapping, targeting mustelids and rats. The logistics of trapping at the landscape scale across alpine habitats are challenging. Novel predator control techniques that can safely be applied at scale above the treeline are urgently required. Whether predator control to sustain populations of Rockwrens and other sensitive alpine fauna is required year-round, and on an annual basis, also needs to be considered. We thank everyone who helped with field data collection; Kathrin Affeld for data management; Haast and Te Anau Department of Conservation staff for assistance with logistics; those involved in the community trapping programme at Homer-Gertrude Cirque, Fiordland; the Australasian Bird Fair for funding predator traps on the Haast Range; Jim Briskie for useful advice on an earlier draft; and Dan Chamberlain and Davide Scridel for their helpful comments and recommendations while reviewing the manuscript.
REFERENCES Akaike, H. 1973. Information theory and an extension of the maximum likelihood principle. Second International Symposium on Information Theory: 267–281. Barker, F.K., Barrowclough, G.F. & Groth, J.G. 2002. A phylogenetic hypothesis for passerine birds: taxonomic and biogeographic implications of an analysis of nuclear DNA sequence data. Proc. R. Soc. Lond. B 269: 295–308. €chler, M., Bolker, B.M. & Walker, S.C. 2015. Bates, D., Ma Fitting linear mixed-effects models using lme4. J. Stat. Softw., 67: 1–48. Bibby, C., Burgess, N., Hill, D. & Mustoe, S. 2000. Bird Census Techniques. London: Academic Press. Birdlife International. 2017. Xenicus gilviventris. (Amended version published in 2016.) The IUCN Red List of Threatened Species 2017: e.T22698585A111474204 (accessed 13 June 2017). Blackburn, T.M., Cassey, P., Duncan, R.P., Evans, K.L. & Gaston, K.J. 2004. Avian extinction and mammalian introductions on oceanic islands. Science 305: 1955–1958.
© 2018 British Ornithologists’ Union
Brambilla, M., Cortesi, M., Capelli, F., Chamberlain, D., Pedrini, P. & Rubolini, D. 2017. Foraging habitat selection by Alpine White-winged Snowfinches Montifringilla nivalis during the nestling rearing period. J. Ornithol. 158: 277– 286. Burnham, K.P. & Anderson, D.R. 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. New York, NY: Springer. Chamberlain, D.A.N., Arlettaz, R., Caprio, E., Maggini, R., Pedrini, P., Rolando, A. & Zbinden, N. 2012. The altitudinal frontier in avian climate impact research. Ibis 154: 205–209. € ller, R., Roy, D.B. & Thomas, Chen, I.C., Hill, J.K., Ohlemu C.D. 2011. Rapid range shifts of species associated with high levels of climate warming. Science 333: 1024–1026. Christie, J.E., Wilson, P.R., Taylor, R.H. & Elliott, G. 2017. How elevation affects ship rat (Rattus rattus) capture patterns, Mt Misery, New Zealand. N. Z. J. Ecol. 41: 113– 119. Cooch, E. & White, G. 2017. The ‘Delta method’. In Cooch, E. & White, G. (eds) A Gentle Introduction, 2nd edn, Program Mark. Analysis of Data from Marked Individuals: 1– 44. Available at: http://www.phidot.org/software/mark/docs/b ook/pdf/app_2.pdf (accessed 10 May 2017). Cooper, S.J. 1999. The thermal and energetic significance of cavity roosting in Mountain Chickadees and Juniper Titmice. Condor 101: 863–866. Dinsmore, S.J., White, G.C. & Knopf, F.L. 2002. Advanced techniques for modeling avian nest survival. Ecology 83: 3476–3488. Elliott, G. & Kemp, J. 2016. Large-scale pest control in New Zealand beech forests. Ecol. Manag. Restor. 17: 200–209. Elliott, G.P., Merton, D.V. & Jansen, P.W. 2001. Intensive management of a critically endangered species: the kakapo. Biol. Cons. 99: 121–133. Ericson, P.G.P., Christidis, L., Cooper, A., Irestedt, M., Jackson, J., Johansson, U.S. & Norman, J.A. 2002. A Gondwanan origin of passerine birds supported by DNA sequences of the endemic New Zealand wrens. Proc. R. Soc. Lond. B 269: 235–241. Ferrarini, A., Alatalo, J.M. & Gustin, M. 2017. Climate change will seriously impact bird species dwelling above the treeline: a prospective study for the Italian Alps. Sci. Total Environ. 590–591: 686–694. Heath. 1986. Rock Wrens in the Southern Alps of New Zealand. In Barlow, B.A. (ed.) Flora and Fauna of Alpine Australasia: Ages and Origins: 277–289. Melbourne, Vic.: CSIRO. Higgins, P., Peter, J. & Cowling, S. (eds). 2006. Handbook of Australian, New Zealand and Antarctic Birds. Volume 7: Boatbill to Starlings. Melbourne, Vic.: Oxford University Press. Innes, J., Kelly, D., Overton, J.M. & Gillies, C. 2010. Predation and other factors currently limiting New Zealand forest birds. N. Z. J. Ecol. 34: 86–114. Jones, M.G.W. & Ryan, P.G. 2009. Evidence of mouse attacks on albatross chicks on sub-Antarctic Marion Island. Antarct. Sci. 22: 39–42. King, C.M. & Powell, R.A. 2007. The Natural History of Weasels and Stoats: Ecology, Behavior, and Management. New York, NY: Oxford University Press.
Invasive predator impacts on alpine rock wren
Laake, J.L. 2013. RMark: An R Interface for Analysis of Capture-Recapture Data with MARK. Alaska Fish. Sci. Cent, NOAA, Natl. Mar. Fish. Serv., 7600 Sand Point Way NE, Seattle WA 98115: AFSC Processed Rep 2013-01: 25. Little, L., King, C.M. & O’Donnell, C.F.J. 2017. Behaviour of stoats (Mustela erminea) raiding the nests of rock wrens (Xenicus gilviventris) in alpine New Zealand. Notornis 64: 124–135. Martin, T.E. 1995. Avian life history evolution in relation to nest sites, nest predation, and food. Ecol. Monogr. 65: 101–127. Mayfield, H. 1961. Nesting success calculated from exposure. Wilson Bull. 73: 255–261. McGlone, M.S. 1989. The Polynesian settlement of New Zealand in relation to environmental and biotic changes. N. Z. J. Ecol. 12: 115–129. Michelsen-Heath, S. 1989. The breeding biology of the Rock Wren, Xenicus gilviventris, in the Murchison Mountains, Fiordland National Park, New Zealand. MSc thesis, University of Otago, Dunedin. Michelsen-Heath, S. & Gaze, P. 2007. Changes in abundance and distribution of the Rock Wren (Xenicus gilviventris) in the South Island, New Zealand. Notornis 54: 71–78. Mills, J.A., Lavers, R.B. & Lee, W.G. 1984. The takahe – a relict of the Pleistocene grassland avifauna of New Zealand. N. Z. J. Ecol. 7: 57–70. O’Donnell, C.F.J., Weston, K.A. & Monks, J.M. 2017. Impacts of introduced mammalian predators on New Zealand’s alpine fauna. N. Z. J. Ecol. 41: 1–22. Pauchard, A., Milbau, A., Albihn, A., Alexander, J., Burgess, T., Daehler, C., Englund, G., Essl, F., Eveng ard, B., Greenwood, G.B., Haider, S., Lenoir, J., McDougall, ~ ez, M.A., Olofsson, J., Pellissier, L., K., Muths, E., Nun Rabitsch, W., Rew, L.J., Robertson, M., Sanders, N. & Kueffer, C. 2016. Non-native and native organisms moving into high elevation and high latitude ecosystems in an era of climate change: new challenges for ecology and conservation. Biol. Invasions 18: 345–353. Poutu, N. & Warburton, B. 2005. Effectiveness of the DOC 150, 200, and 250 Traps for Killing Stoats, Ferrets, Norway Rats, Ship Rats, and Hedgehogs; 12. Lincoln: Landcare Research. R Core Team. 2016. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. ^ , V. & Martin, T.E. 2002. Environmental influences on Remes the evolution of growth and developmental rates in passerines. Evolution 56: 2505–2518. Rhodes, B., O’Donnell, C. & Jamieson, I. 2009. Microclimate of natural cavity nests and its implications for a threatened secondary-cavity-nesting passerine of New Zealand, the South Island Saddleback. Condor 111: 462–469. Robertson, H., Dowding, J., Elliott, G., Hitchmough, R., Miskelly, C., O’Donnell, C., Powlesland, R., Sagar, P., Scofield, P. & Taylor, G. 2013. Conservation status of New Zealand birds, 2012. In New Zealand Threat Classification Series 4. Wellington: Department of Conservation. Rotella, J.J. 2006. Nest survival. In Cooch, E. & White, G. (eds) Program MARK: A Gentle Introduction. Available pdf format at: http://www.phidot.org/software/mark/docs/book/ (accessed 26 February 2017).
7
Sala, O.E., Chapin Iii, F.S., Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L.F., Jackson, R.B., Kinzig, A., Leemans, R., Lodge, D.M., Mooney, H.A., Oesterheld, M., Poff, N.L., Sykes, M.T., Walker, B.H., Walker, M. & Wall, D.H. 2000. Global biodiversity scenarios for the year 2100. Science 287: 1770–1774. Scridel, D. 2014. Ecology and conservation of birds in upland and alpine habitats: a report on the BOU’s Annual Conference held at the University of Leicester, 1–3 April 2014. Ibis 156: 896–900. Sekercioglu, C.H., Schneider, S.H., Fay, J.P. & Loarie, S.R. 2008. Climate change, elevational range shifts, and bird extinctions. Conserv. Biol. 22: 140–150. Smith, D.H.V. & Weston, K.A. 2017. Capturing the cryptic: a comparison of detection methods for stoats (Mustela erminea) in alpine habitats. Wildl. Res. 44: 418–426. Smith, D.H.V., Wilson, D.J., Moller, H., Murphy, E.C. & van Heezik, Y. 2007. Selection of alpine grasslands over beech forest by Stoats (Mustela erminea) in montane southern New Zealand. N. Z. J. Ecol. 31: 88–97. Smith, R.K., Pullin, A.S., Stewart, G.B. & Sutherland, W.J. 2010. Effectiveness of predator removal for enhancing bird populations. Conserv. Biol. 24: 820–829. Stocker, R., Garret, M. & Petyt, C. 2006. A Five-Year Study of Rock Wren in Henderson Basin, Kahurangi National Park. Nelson: Department of Conservation. Tennyson, A.J.D. & Martinson, P. 2006. Extinct Birds of New Zealand. Wellington: Te Papa Press. Wanless, R.M., Angel, A., Cuthbert, R.J., Hilton, G.M. & Ryan, P.G. 2007. Can predation by invasive mice drive seabird extinctions? Biol. Let. 3: 241–244. White, G.C. & Burnham, K.P. 1999. Program MARK: survival estimation from populations of marked animals. Bird Study 46: S120–S139. Willans, M. & Weston, K.A. 2005. Translocation of Rock Wren Xenicus gilviventris from Murchison Mountains to Anchor Island, Dusky Sound, Fiordland. Te Anau: Department of Conservation. Wilson, D.J. & Lee, W.G. 2010. Primary and secondary resource pulses in an alpine ecosystem: snow tussock grass (Chionochloa spp.) flowering and House Mouse (Mus musculus) populations in New Zealand. Wildl. Res. 37: 89– 103. Wilson, D.J., McElrea, G.J., McElrea, L.M., Heyward, R.P., Peach, R.M.E. & Thomson, C. 2006. Potential conservation impacts of high-altitude small mammals: a field study and literature review. In DOC Research & Development Series 248. Wellington: Department of Conservation. Worthy, T.H., Hand, S.J., Nguyen, J.M.T., Tennyson, A.J.D., Worthy, J.P., Scofield, R.P., Boles, W.E. & Archer, M. 2010. Biogeographical and phylogenetic implications of an early Miocene Wren (Aves: Passeriformes: Acanthisittidae) from New Zealand. J. Vertebr. Paleontol. 30: 479–498. Yoon, J., Kim, B.-S., Joo, E.-J. & Park, S.-R. 2016. Nest predation risk influences a cavity-nesting passerine during the post-hatching care period. Sci. Rep. 6: 31989. Received 26 November 2017; revision accepted 15 May 2018. Associate Editor: Zhijun Ma.
© 2018 British Ornithologists’ Union
8
K. A. Weston et al.
SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article: Table S1. Causes of failures of 75 Rockwren Xenicus gilviventris nests at Haast Range, Mount Aspiring National Park; Homer-Gertrude Cirque, Fiordland National Park; and Lake Roe, Fiordland National Park, New Zealand, 2012–17. Table S2. Models used to explain variation in daily nest survival rates of Rockwrens Xenicus gilviventris at Haast Range, Mount Aspiring National Park; HomerGertrude Cirque, Fiordland National Park; and Lake Roe, Fiordland National Park, New Zealand, 2012–17. Table S3. Overall nest survival rates for Rockwrens Xenicus gilviventris at Haast Range, Mount Aspiring
© 2018 British Ornithologists’ Union
National Park; Homer-Gertrude Cirque, Fiordland National Park; and Lake Roe, Fiordland National Park, New Zealand, 2012–17. Figure S1. Rockwren Xenicus gilviventris breeding ecology study sites in the South Island of New Zealand, 2012–17. Figure S2. Typical New Zealand Rockwren Xenicus gilviventris nesting habitat at (a) Homer-Gertrude Cirque, Fiordland National Park, (b) Haast Range, Mt Aspiring National Park, and (c) Lake Roe, Fiordland National Park. Figure S3. Breeding phenology of Rockwrens Xenicus gilviventris in relation to mustelid trap catch.
