Effects of rat poisoning operations on abundance and diet of mustelids in New Zealand podocarp forests

New Zealand Journal of Zoology ISSN: 31-4223 (Print) 1175-8821 (Online) Journal homepage: https://www.tandfonline.com/loi/tnzz2 Effects of rat poisoning operations on abundance and diet of mustelids in New Zealand podocarp forests Elaine C. Murphy, B. Kay Clapperton, Philip M. F. Bradfield & Hazel J. Speed To cite this article: Elaine C. Murphy, B. Kay Clapperton, Philip M. F. Bradfield & Hazel J. Speed (1998) Effects of rat poisoning operations on abundance and diet of mustelids in New Zealand podocarp forests, New Zealand Journal of Zoology, 25:4, 315-328, DOI: 1./314223.1998.9518161 To link to this article: https://doi.org/1./314223.1998.9518161 Published online: 3 Mar 21. Submit your article to this journal Article views: 69 Citing articles: 25 View citing articles Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalinformation?journalcode=tnzz2

New Zealand Journal of Zoology, 1998, Vol. 25: 315-328 31-4223/254-315 $7./ The Royal Society of New Zealand 1998 315 Effects of rat-poisoning operations on abundance and diet of mustelids in New Zealand podocarp forests ELAINE C. MURPHY Department of Conservation Private Bag 68-98 Newton Auckland, New Zealand B. KAY CLAPPERTON 49 Margaret Avenue Havelock North, New Zealand PHILIP M. F. BRADFIELD Department of Conservation Te Kuiti Field Centre P.O. Box 38 Te Kuiti, New Zealand HAZEL J. SPEED Department of Conservation Pureora Forest Park RD7 Te Kuiti, New Zealand Abstract This study aimed to quantify the changes in numbers and diet of stoats, weasels and ferrets following rat and possum poison operations in two podocarp-hardwood forests between 1989 and 1995. Poison operations were classified according to their success in reducing rat numbers, and if they used an acute toxin () or an anticoagulant (brodifacoum or pindone). Stoat catch rates followed the same seasonal patterns as rat footprint tracking rates, and stoat catch rates were positively correlated with rat catch rates. Rat numbers in spring had no significant relationship with the number of juvenile stoats caught in summer. Stoat catch rates did not vary significantly with poison-operation type over a six month period, but all three successful anticoagulant operations resulted in lower stoat catch rates than did Z983 Received 9 January 1998; accepted 22 June 1998 unsuccessful operations. Brodifacoum in bait stations may have lowered stoat numbers by secondary poisoning for the first 2-3 months, but thereafter there was no apparent effect. The sex ratio of stoats caught varied significantly amongst the poison operations. The fewest females were caught following anticoagulant operations. Stoat stomachs and intestines contained mostly rats, and some birds and mice. Weasels ate mostly mice, while ferrets predominantly ate lagomorphs and invertebrates. Male and female stoats ate similar proportions of rats, but females ate more mice. Both sexes, but particularly females, ate fewer birds in autumn and winter than in spring and summer. Stoats shifted between eating rats and birds, depending upon the abundance of rats. Thus successful rat-poisoning operations resulted in higher bird consumption than unsuccessful ones. Combining the numerical and functional responses of stoats into a 'bird predation index' showed that stoats are likely to have the greatest effect on birds after successful poison operations. Diet shifts could not be demonstrated in weasels or ferrets because sample sizes were too small for quantitative assessments. The risk of increased predation pressure on birds from diet-shifting by stoats must be balanced against the predation pressure on birds and other ecological impacts of rats and possums from different poison operations. Keywords diet; functional response; mustelid; Mustela erminea; Mustela furo; Mustela nivalis; numerical response; poison; rat; stoat INTRODUCTION Native fauna in New Zealand forests are at risk from predation by introduced mammals, especially the ship rat (Rattus rattus), and the stoat (Mustela erminea) (Innes & Hay 1991; King et al. 1996; O'Donnell et al. 1996). Large-scale poisoning by aerial application or bait stations is used routinely to control rats and another pest species, the Australian brushtail possum (Trichosurus vulpecula)

316 New Zealand Journal of Zoology, 1998, Vol. 25 (Henderson et al. 1994; Innes et al. 1995). The main predators of rodents (rats and mice Mus musculus) in New Zealand forests are stoats, feral cats (Felis catus), and, to a lesser extent, weasels (Mustela nivalis) and ferrets (Mustela furo) (Innes 199; Murphy & Pickard 199). The impacts of poisoning on these rodent predators must be determined before a full assessment can be made of the costs and benefits of controlling rats. If non-target mustelid populations are reduced by rat control, then integrated pest management systems will benefit by the reduced effort needed to target those species directly. Because mustelids are unlikely to sample cereal-based baits (Richardson 1995; E. B. Spurr pers. comm.), they are not at risk from direct poisoning in rodent/possum operations. A numerical response by predators to reductions in rodent abundance due to poisoning could be either due to food shortages, inducing a reduction in the predators' reproductive output, increased emigration, decreased immigration and death from starvation, or to secondary poisoning from their consuming toxic rodent carcases (Hegdal et al. 1981; Alterio et al. 1997), or both. Secondary poisoning is more likely to follow the application of slow-acting anticoagulants than application of acute toxins such as because of live prey containing high toxicant content surviving for longer in the former case (Godfrey 1985). Predators can, however, die from eating -poisoned carcases (Hegdal et al. 1981; Gillies 1997; Murphy et al. in press). If mustelid populations are not reduced by rodent poison operations, then any benefits to the species under protection gained from reduced predation by rodents may be offset by increased predation by the rodent predators themselves. Mustelids demonstrate diet switching as a functional response to changes in the abundance of their primary prey (Erlinge 1975; Dunn 1977; Tapper 1979; Jarvinen 1985). The effects of both numerical and functional responses of predators need to be assessed together to determine the overall effect on all their prey. King (1983) produced a 'bird predation index' by multiplying the catch rate of stoats by the percentage of birds in their diet. She found that in New Zealand beech forests (Nothofagus spp.), the negative correlation between the percentages of bird and mouse consumption did not offset the effects of high stoat densities produced as an indirect response to mast years (King 1983). The highest bird predation indices were recorded in summers of high mouse abundance. Korpimaki et al. (1991) used a similar index (termed 'vole kill rate') to show that weasels (but not stoats) may cause the observed declines in microtine rodent population densities. Functional and numerical responses of mustelids have been demonstrated following poisoning operations. Ferrets increased their consumption of lizards, invertebrates and birds after poisoning of their main prey, the rabbit (Oryctolagus cuniculus) (Pierce 1987; Norbury & Heyward 1996). Ferret densities have also been shown to decline six to twelve months following poisoning (Norbury & McGlinchy 1996). Pierce (1987) suggested that stoats may become more abundant in areas where ferret and cat densities have been reduced. This could increase the predator pressure on wetland birds, because stoats are likely to prey more on birds and less on rabbits than the larger two predators. Little is known of the population dynamics and diet of mustelids in podocarp-hardwood forests in New Zealand, or the impact of rodent and possum control operations on mustelid populations. Preliminary findings by Murphy & Bradfield (1992) suggest that stoat abundance over a six month period was unaffected by an aerial -poison operation for possums and rats, and that stoats preyed more on birds when rat numbers were drastically reduced. Here we aim to describe the numerical and functional responses of mustelids following rat- and possum-poisoning operations, so that we can gain a fuller understanding of the broader ecological impacts of these operations. We quantify the changes in numbers of stoats, weasels and ferrets, and the structure of stoat populations in relation to rodent abundance in two podocarp-hardwood forests in the North Island of New Zealand, following different poisoning operations targeting rats and possums. We also describe the diets of all three mustelid species and determine whether or not stoats switch to other prey when rats are reduced. We compare the effects of the various poison operations on stoat diet changes. METHODS Study sites The study was undertaken in two podocarp-hardwood forests in the North Island, New Zealand. Both sites - Mapara Wildlife Management Reserve, King Country (38 33'S, 175 17'E) and Kaharoa Forest, Bay of Plenty (38 5'S, 176 18'E) - had previously been logged for podocarps and are dominated by a tawa (Beilschmiedia tawa) canopy. Both have a diverse understorey, interspersed with old, grassed logging tracks. The forests are managed as habitat

Murphy et al. Effects of rat-poisoning on mustelids 317 for the endangered wattlebird, North Island kokako (Callaeas cinerea wilsoni) (Saunders 199; Innes et al. 1995). Poison operations The study sites were poisoned with either or one of two anticoagulants - brodifacoum orpindone (Animal Pest Management Services, Wellington, N.Z.). Details of the poison operations at both sites are summarised in Table 1. In 1989-9 no widespread poisoning was done at Mapara, but bait stations containing 'Talon 5 WB' (brodifacoum; ICI Crop Care, Nelson, N.Z.) were placed within the territories of 1 kokako in one region of the reserve. These had a negligible effect on rat densities over the rest of the reserve (Innes et al. 1995). Aerial operations at both sites used cereal-based pollard baits. At Kaharoa non-toxic pre-feed baits were distributed three weeks before the poison drops in 199. In 1993-94 and 1994-95 at Mapara, 'Talon Possum Bait' (brodifacoum, ICI Crop Care, Nelson, N.Z.) was placed in 473 bait stations set roughly 2 m apart across the 1432 ha reserve. In 1994-95 bait station spacing was increased to 1 m in 5 ha of the reserve. The stations were filled five times in 1993-94 and four times in 1994-95. The fifth bait renewal for 1993-94 was in mid-january 1994, and some baits remained available to rats for 1-3 months after this (P. Thomson pers. comm.). All baits were removed in April 1995. Monitoring Rat and mustelid numbers in the Mapara Reserve were estimated from kill-trapping rates between October 1989 and April 1995. Mark 4 Fenn traps (FHT Works, Worcester, England) were set in tunnels along a 24 km trapline situated along the main ridge-lines and within valleys and along grassy tracks throughout the reserve. In the first 6-month trapping period (15 October 1989-21 April 199), 13 traps were used. Between 3 September 199 and 27 April 1995, 142 traps were operated continuously. The traps were unbaited except for the first four weeks of trapping in 1989, when sardine or rabbit liver bait was used. Traps were usually checked twice, but sometimes only once, weekly. Fenn traps have been shown to be an effective method of monitoring ship rat abundance (King & Moller 1997). Rodent abundance was also monitored at Mapara by recording footprints in tunnels with ink pads (King & Edgar 1977). These were used from September 1991 to March 1995. In the Kaharoa Conservation Area, 71 Fenn traps were set throughout the 381 ha block of forest from 23 October 199 to 29 March 1991, from 3 November 1991 to 5 July 1992, and from 31 August 1992 to 6 May 1993. In 199-91 the traps were baited with 'beef and gravy' flavoured catfood. In 1991-92 and 1992-93 half the traps were baited with hen eggs and the other half were unbaited. The poison operations were defined post hoc as "unsuccessful" if more than.5 rats were caught per 1 trap nights (TN) during November and December, or "successful" if rat catch/1tn was less than.5. The Nov-Dec period was chosen because it immediately followed the poison operation, and thus showed the lowest rat numbers. The.5 rat catch' 1TN was an arbitrary figure, but the operations fell clearly into two groups either side of this figure. Successful operations were subdivided depending upon the type of toxin used into '' and 'anticoagulant' (Table 1). Age and diet assessment Trapped mustelids were collected and frozen until autopsy. Males were categorised as adults or juveniles (<1 year old) based on the size of testes or weight of their baculum (Grue & King 1984). The contents of the stomach and intestines of each animal were sieved (.5 mm) and stored in 7% ethanol. Mammalian remains were identified where possible as rat, mouse, lagomorph (probably mostly often rabbit, but possibly some hare, Lepus europaeus) or possum from bones, teeth or hair scale patterns (Day 1966). Birds, lizards and invertebrates were recorded but not further identified. Diet results are presented as percentage of guts containing each prey type. In addition, the percentage of each prey by weight was calculated by expressing the number of prey items of a certain type as a proportion of the total number of items, and weighting these proportions by the estimated weight of the prey when consumed (King & Moody 1982b). The diet data include those reported by Murphy & Bradfield (1992). Statistical tests Non-parametric Kruskal-Wallis (H statistic) and Mann-Whitney (U statistic) tests were used to compare the effects of the poison-operation types on stoat numbers and diet. Correlations were statistically assessed using Spearman rank correlation (r s ). Differences in diet between species and between sexes were tested using Chi-square tests.

318 New Zealand Journal of Zoology, 1998, Vol. 25 RESULTS Mustelid population dynamics In total 26 stoats, 112 weasels and 9 ferrets were trapped at Mapara between October 1989 and September 1995. At Kaharoa, 39 stoats, 7 weasels, and 2 ferrets were trapped between October 199 and May 1993. Stoat capture rates were highest in summer (December-February) or autumn (March-May) of each year, except at Kaharoa in 1992-93. In that trapping period most stoats were caught in spring (September-November), the majority before the poison drop in October. Weasels were most frequently caught in autumn or winter (May-August) and ferrets were caught only in summer and autumn. At Kaharoa only 7 weasels were caught, all between December 1991 and October 1992. Stoat captures at Mapara generally followed the same seasonal patterns as the abundance of rats as demonstrated by tunnel tracking rates (Fig. la). Seasonal captures of stoats were significantly correlated with rat tracking rates (r s =.77, n=13, P <.5), but not with mouse tracking rates (r s =.28). Rat tracking and rat trapping indices were positively correlated (r s =.88, n=13, P <.1). Neither weasel nor ferret captures rates showed significant correspondence to either mouse or rat tracking rates (Fig. lb). The mouse index differed from the rat index in that it was low in summer 1992-93 and high in summer 1993-94. The highest catch rates for all three mustelid species were recorded in autumn 1994, even though rat catch rates in Fenn traps were low that year (16 cf 137, 213 and 217 in the three preceding autumns). Stoat numbers at Mapara and Kaharoa during October-March were positively correlated with rat numbers caught in Fenn traps during the same period (r s =.63, n=9, P<.5, one-tailed test). The relationship was logarithmic (Fig. 2). Effects of poisoning on stoat numbers Stoat catch rates (per 1TN) in October-March did not vary significantly amongst the poison-operation types (H=2.4, n=9, P>.1). All three successful anticoagulant operations resulted in lower stoat catch rates than unsuccessful operations, but the catch rates after successful operations varied greatly (Fig. 2). Numbers of stoats caught at Mapara following the two brodifacoum operations of 1993-94 and 1994-95 were low in the first three months and rose Table 1 Details of the poison operations carried out between 1989 and 1994 at Mapara, and in 199 to 1992 at Kaharoa, including an index of success of the operations based upon the numbers of rats caught in Fenn traps per 1 trap nights in November and December following each poison operation. "Unsuccessful" = more than.5 rats/1tn; "Successful" = less than.5 rats/1tn. Further details of the operations up to 1992-93 are given by Innes et al. (1995). Period Operation date Method Toxin (cone.) Rate No. rats caught No. rats per 1TN Poison operation type Mapara 89-9 9-91 91-92 92-93 93-94 94-95 Kaharoa 9-91 91-92 92-93 Oct-Apr Sep Oct Oct Sep-Apr Aug-Apr Oct Oct Oct bait station aerial aerial aerial bait stations bait stations aerial aerial aerial brodifacoum (5 ppm) (.8%) (.8%) (.8%) brodifacoum (2 ppm) brodifacoum (2 ppm) (.15%) pindone (5 ppm) (.13%) - 8 kg ha-' 8 kg ha-' 8 kg ha-' - - 18 kg ha" 1 1 kg ha" 1 6 kg ha- 1 89 4 64 74 17 7 1 4 1 1.42.5.74.85.2.8.4.18.2 Unsuccessful Successful Unsuccessful Unsuccessful Successful Successful Successful Successful Successful

Murphy et al. Effects of rat-poisoning on mustelids 319 Fig. 1 Seasonal changes in (a) number of stoats kill-trapped ( ) and percentage of tracking tunnels that recorded rat footprints ( ) and (b) numbers of weasels ( ) and ferrets (A) kill-trapped and percentage of tunnels recording mice footprints ( ) at Mapara Reserve, between Spring 1992 and Autumn 1995. 1992 1992 1993 Fig. 2 Relationship between catch rates of rats and stoats in Fenn traps in October-March of each poison operation at Mapara Reserve and at Kaharoa Forest; A Unsuccessful; Successful ; Successful Anticoagulant. The fitted line is logarithmic: y=.281n(x)+.125, with its corresponding correlation index (r 2 ). Rat data exclude captures in October prior to that year's poison operation..14.12 z.1 5.8 ^.6 2.4.2..2.4.6.8 1 r 2 =.47 1.2 1.2 Rats(n/1TN) sharply in January (Table 2). The unsuccessful ratpoisoning year of 1989-9 and the successful operation year of 199-91 also both produced low stoat catch rates, but only for October and November. Catch rates at Kaharoa in all three years did not exceed 5 stoats in any month. Similar numbers of male and female stoats were caught in October-December during years when control operations had little effect on rat numbers. Males dominated the trapping data after successful operations, and no females at all were caught after all three successful anticoagulant operations (Fig. 3a). These differences amongst poison-operation types were statistically significant (H=5.84, n=9. P <.5). During January-March of each following year, males still dominated in the anticoagulant treatments, but there was less of a difference amongst the treatments (H=5.35, n=8, P >.5).

32 New Zealand Journal of Zoology, 1998, Vol. 25 % Male 1 8 6 4 2 (a) The proportion of male stoats that were juveniles in the two time periods are shown in Fig. 3b. No juveniles were caught during successful anticoagulant poison operations in October-December, but the differences between the operations were not statistically significant in either October-December (H=2.9, n=9, P >.1) or in January-March (H=.2, n=8, P >.1). Rat numbers in October and November had no obvious effect on the production of juvenile stoats in the following summer (r s =.4, n=7, P >.1). O luvenil * 1 8 6 4 2 (b) Unsuccessful D Successful Oct-Dec Jan-Mar Fig. 3 Mean percentages of (a) stoats that were males and (b) male stoats that were juveniles caught in Fenn traps in Mapara Reserve and Kaharoa Forest from October to December and from January to March, classified according to poison operation type. Error bars represent+se. n=3 for each operation type, except for Successful in Jan- Mar, where n=2. Mustelid diet Details of the diet of stoats, weasels and ferrets at Mapara and Kaharoa are given in Tables 3-5. Overall, rats were the main component of stoat diet, followed by birds, mice and lagomorphs. The guts of 22% of the stoats were empty. Mice accounted for the majority of weasel diet both by frequency of occurrence (72%) and by weight (64%). Ferrets ate more lagomorphs than any other prey by weight (5%). They also ate large numbers of invertebrates, but these accounted for only 8% of the diet by weight. The guts of 35% of the weasels and 66% of the ferrets were empty. Prey items appeared in different proportions in the different mustelid species. Stoats ate significantly more rats and lagomorphs, and fewer mice than weasels (% 2 =61.8, d.f.=2, P <.1). Table 2 Numbers of stoats Fenn-trapped in Mapara Reserve from October 1989 to April 1995. Numbers in brackets are numbers of females/males caught. One male in October 1991 and one male in October 1992 were caught before the operations were done. 1989-9 199-91 1991-92 1992-93 1993-94 1994-95 Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep 2(1/1) 1 (1/) 7(3/4) 7(3/4) 4(1/3) 1 (/1) 1 (/1) 1 (/1) 2 (/2) 4(1/3) 1(3/7) 9 (4/5) 9* (6/2) 9(6/3) 5 (3/2) 1 (I/O) 1 (/1) 3 (/3) 1 (/1) 3(1/2) 2 (2/) 4 (4/) 3* (2/) 3(2/1) 7(1/6) 8 (3/5) 4(2/2) 7(6/1) 1 (1/) 8* (/7) 3 (/3) 5(1/4) 5* (1/3) 6(4/2) 5(1/4) 4* (1/2) 9 (4/5) 4 (4/) 3(2/1) 3* (1/1) 4 (/4) 2 (/2) 2(/2) 5 (3/2) 3 (/3) 11 (3/8) 4(1/3) 7 (2/5) 9 (3/6) 5 (2/3) 3(1/2) 5(1/4) 1 (/1) 3 (/2) 7 (4/3) 1 /1) 7 (2/5) 6* (1/4) * Includes one stoat of unknown sex

Murphy et al. Effects of rat-poisoning on mustelids 321 Table 3 Percentage frequency of occurrence and percentage composition by weight of the prey in the guts of stoats collected during and following poison operations at Mapara, between October 1989 and April 1995 and at Kaharoa between October 199 and May 1993. The guts of 57 more stoats were empty. n Rat Mouse Lagomorph Possum Birds Lizards Invertebrates Unidentified % Frequency of occurrence % by Weight Mapara Kaharoa Mapara Kaharoa 175 41.1 17.7 13.7 1.1 16.6.6 6.3 7.4 27 37. 3.7 3.7 51.8 3.7 7.4 175 5.3 1.8 16.7 1.4 1.1.2 1.1 9.1 27 48.4 4.8 4.8 33.9.7 9.7 Table 4 Percentage frequency of occurrence of the prey in the guts of weasels collected between October and March during or following the various poison-operation types at Mapara from 1989 to 1995 and at Kaharoa from 1991 to 1993. Numbers of weasels containing prey are given in parentheses. The guts of 35 more weasels were empty. Rat Mouse Bird Lizard Invertebrate Unidentified Unsuccessful (17) 12 47 29 18 61 18 (1) 1 Anticoagulant (1) 7 3 1 3 Table 5 Percentage frequency of occurrence of the prey in the guts of ferrets collected between October and March during or following the various poison-operation types at Mapara from 1989 to 1995 and at Kaharoa from 1991 to 1993. Number of ferrets containing prey are given in parentheses. The guts of 5 more ferrets were empty. Rat Mouse Lagomorph Bird Invertebrate Unidentified Unsuccessful (5) 6 4 (6) 17 83 : One of these prey was identified as rodent. Anticoagulant (1) 2 1 3 1 3* Male and female stoats ate similar proportions of rats (x 2 =1.14, d.f.= l, P>.25). These dietary patterns were similar in October March and April-September (Fig. 4). Males ate fewer mice than females, especially in April-September (% 2 =4.68, d.f.=l, P <.5). Males and females ate similar numbers of birds in October-March, but females reduced bird consumption significantly more than males did in April-September (% 2 =12.7, d.f.=l,/ ) <.1), when rat and mouse consumption increased in both sexes. The frequency of occurrence of rats in the diet of stoats in October-March was positively correlated with rat numbers caught during that period (r s =.91, n=8, P <.25) (Fig. 5a). The occurrence of birds showed a corresponding negative correlation (r s^.76, n=8, P <.25) (Fig. 5b). The occurrence of mice was not correlated with rat numbers (Fig 5c). Effects of poisoning on mustelid diet Stoat diet during October-March varied depending on the success of the poison operation conducted (Fig. 6). Successful and anticoagulant operations affected stoat diets in similar ways. Bird consumption was significantly higher in the six months after successful operations of either type than after unsuccessful ones (Mann-Whitney test: U=15, n=3,5, P =.5). Rat consumption was significantly reduced during October-March by successful poison operations (U=15, n=3,5, P =.5). The frequency of occurrence of mice in the diet of stoats did not vary depending upon the success of the poison operation (U=7.5, n=3,5, P >.1). Lagomorph and invertebrate components of stoat diet were not affected by the poison operations. The proportion of stoats with empty guts was higher in the six months following successful poison operations (mean=54%) than after unsuccessful operations (14%), or successful anticoagulant operations (18.9%) but the differences amongst the poison-operation types were not significant (H=5.35, n=9,.1>p>.5). Weasels ate rats during October-March only in 1989-9, one of the unsuccessful operations (Table 4), when November-December rat numbers were highest (Table 1). They ate the highest proportions of mice after successful poison operations, but sample sizes were too small for statistical comparisons. During the anticoagulant-operation years, 23 weasels were caught between April and September. Mice were present in 83% of their guts, rats in 4%, and invertebrates in 9%. Mice also dominated the gut contents of the nine weasels caught in April-September of the -operation years. Consumption of

322 New Zealand Journal of Zoology, 1998, Vol. 25 o 35 3 25 2 15 1 5 Male n=61 m Female n=52 Fig. 4 Percentage frequency of occurrence of prey items in the diet of male and female stoats killtrapped (a) from October to March and (b) from April to September at Mapara Reserve between 1989 and 1995 and at Kaharoa Forest between 1991 and 1993, data from the two sites combined. n=number of captured stoats with identifiable gut contents. 7 6 5 4 3 2 1 Malen=57 e Female n=39 Bird Rat Mouse Lagomorph Invertebrate lagomorphs by ferrets may have been reduced by successful poison operations (Table 5). Invertebrates replaced lagomorphs as the major component offerret diet directly after successful operations, while 4% of the ferrets' diet was rodents during anticoagulant operations. Predation indices Bird predation indices (combining the numerical and functional responses) for stoats in October-March varied significantly amongst the poison-operation types (H=6.25, n=8, P =.2). Successful operations produced higher BPIs than Talon or Pindone operations (Table 6). In April-September, the successful and unsuccessful years for which data are available still had higher BPIs than the one available Talon year. DISCUSSION Population dynamics Stoats dominated the mustelid trapping data in both forests. This is a typical pattern in New Zealand forests, although relatively more weasels were caught during this study than in other mustelid trapping programmes (King & Moody 1982a; King 199; King et al. 1996). This may be because of the diversity of habitats within the study area. Weasels may have been under-represented in our trapping because they avoid stoat-scented traps (Erlinge & Sandell 1988). Co-existence of the three mustelid species is possible because of their dietary differences. Separation within different habitats in the forest may also be a way by which the mustelid species partition the resources (Erlinge & Sandell 1988; King et al. 1996). At Mapara, 4% of successful traps caught all three species of mustelids in any one year (P. Bradfield, unpubl. data). The majority of weasels were caught in fern-dominated areas which could contain permanent populations of mice. Ferrets were caught mainly near the reserve margin or along grassy tracks. The peak of stoat captures in summer and autumn resulted from the presence in the population of juveniles from December until March. This pattern is similar to those reported from other New Zealand forest types (King & McMillan 1982; Dilks et al. 1996). Males are normally caught more frequently than females, irrespective of trapping system or stoat density (King & McMillan 1982). Close seasonal relationships and summer correlations between stoat and rat densities in the podocarp forest at Mapara also occur in New Zealand beech forests between stoats and mice (King 1983), and between stoats and microtine rodents in northern Europe (Korpimaki et al. 1991). Such relationships have also been observed between weasels and field voles (Microtus agrestis) (Erlinge

Murphy et al. Effects of rat-poisoning on mustelids 323 8 7 6 5 4 3 2 1 4 35 3 25 2 15 1 =.9..2.4.6.8 1. 1.2 1.4..2.4.6.8 1. 1.2 1.4 5 o to)...2 u 1 > _ i 1.4.6.8 1. 1.2 1. Rats (n/1tn) Fig. 5 Relationship between the catch rate of rats and the frequency of occurrence of (a) rats, (b) birds, and (c) mice in the diet of stoats kill-trapped from October to March at Mapara Reserve between 1989 and 1995 and at Kaharoa Forest between 1991 and 1993, combined. The fitted lines are linear: y=52.6x-.8 and y=-51.5x+61.4 for (a) and (b), respectively. 1974), but with a time lag between the cycles of prey and predator (Tapper 1979; Korpimaki et al. 1991). These predator-prey relationships suggest that any manipulation (e.g., reduction by poisoning) of their main prey will produce a numerical response in mustelids, especially stoats. u u Numerical responses following poison operations Stoats did not show a consistent strong numerical response to the drastic reductions in rat numbers caused by the poison operations. However, the poison operation in Kaharoa in 199, which used the highest concentration of toxin application rate, produced the greatest reduction in stoat numbers as well as the greatest reduction in rat numbers. The unsuccessful poisoning operations may still have provided enough opportunities for secondary poisoning of stoats to have made it difficult to demonstrate a difference between the unsuccessful and successful operations. This is indicated by the low stoat catch rates recorded in October and November of 1989-9. Brodifacoum-killed rat carcases and rats surviving following a poisoning operation can contain high concentrations of the poison (Alterio et al. 1997; Murphy et al. 1998), and even in unsuccessful operations, some rats would have been poisoned. The differences in stoat numbers amongst the poison operation types may also have been underestimated by our sampling technique. Stoat trapability has been shown to increase when rodents are scarce, so there may not be a linear relationship between stoat density and prey density as measured by trap catch rates (Alterio, Moller & Brown unpubl. data). Although limited food supplies can reduce reproductive output in stoats (Erlinge 1983), the slight reduction in stoat numbers during or after poisoning observed in the present study is unlikely to have been caused by reduced reproduction. October to November is the "critical period" determining the success of stoat reproduction (King 1981). We found no relationship between rat numbers at that time and the numbers of juvenile stoats in the following summer. While some stoats may have died of hunger following -poison operations, this is not likely to have been a major mortality factor for anticoagulant-poison operations, as illustrated by the lack of change in the percentage of empty stoat guts compared with stoats trapped after unsuccessful operations. Stoats from this study were assayed for brodifacoum residues, and 77% contained detectable levels of the toxin in their livers (Murphy et al. 1998). This suggests that secondary poisoning may be an important mortality factor. There are two possible reasons for the rise in stoat numbers at Mapara from January. First, most juvenile stoats become independent in January (King & McMillan 1982) so at that time those animals bred in the reserve, plus those invading from outside, will

324 New Zealand Journal of Zoology, 1998, Vol. 25 Bird Rat Mouse Unsuccessful (n=3) Successful (n=3) M uccessful Anticoagulant (n=3) Lagomorph Invertebrate Fig. 6 Mean percentage frequency of occurrence of the major prey items in the diet of stoats killtrapped between October and March at Mapara Reserve between 1989 and 1995 and at Kaharoa Forest between 199 and 1993, classified according to poison operation type. Error bars represent +SE. be recruited into the population. Secondly, rodent numbers are kept low by the on-going poisoning in bait stations. This means that the prevalence of the 'vehicle' for transfer of toxin to stoats is reduced. This may be partly offset by the accumulation of brodifacoum in the stoats producing lethal doses (Murphy et al. 1998). The trend to catch the lowest proportion of females both during and after Talon and Pindone operations compared with operations suggests that anticoagulant poisons and may affect stoat population structure differently. This is supported by the finding that a higher proportion of females than males contained brodifacoum residues (Murphy et al. 1998), perhaps partly because of dietary differences between the sexes. While males and females ate similar proportions of rats, females ate more mice, especially later in the year, when the anticoagulant poisons would still have been present in the rodent population (Murphy et al. 1998). While possum carcases may be another source of secondary poisoning, only two stoats had consumed possum, and both were males. The fact that Talon was presented in bait stations over an eight month period, whilst the was given in a single aerial operation, may be another reason why the poisons had different effects. No information is available on the responses of male and female stoats to bait stations. Different rates of immigration between male and female stoats (Alterio & Moller unpubl. data) may partly explain the overall differences between the sexes in catch rates after the poison operations, but it does not explain the differences amongst the poison-operation types in the sex ratios of stoats caught. Too few weasels and ferrets were caught to quantify the effects of reduced rodent densities on their populations. The coinciding peaks in catch rates of all three mustelid species in autumn of the same year suggests that there was no major change in dominance in the predator guild, as suggested by Pierce (1987). There was an indication that weasels increased in abundance in the autumn and winter after a Talon operation, but it is not possible to say whether this was an effect from the poison operation per se. Table 6 Bird predation indices (stoats/ 1TN x % frequency occurrence of birds in stoat diet) during October-March and April-September of each poison operation at Mapara between 1989 and 1995 and at Kaharoa between 1991 and 1993. Site Mapara Kaharoa Operation 1989-9 199-91 1991-92 1992-93 1993-94 1994-95 1991-92 1992-93 * Successful poison operation Poison None * Talon* Talon* Pindone* * Bird predation index Oct-Mar Apr-Sep.77 7.18.6.54 1.63 4.19 4.41 6.58 _.84.96.96.5 - -

Murphy et al. Effects of rat-poisoning on mustelids 325 Functional responses following poisoning The functional response of stoats to reductions in rat abundance in New Zealand podocarp forests suggested by Murphy & Bradfield (1992) has been confirmed in the present study. Although sample sizes are small, the use of non-parametric statistics leads to conservative conclusions. At both Mapara and Kaharoa, when rats were successfully poisoned, stoats switched in summer from eating rats to birds. There was no consistent effect on consumption of other prey groups. Lagomorph consumption did not rise when rodents were scarce as in beech forest (Murphy & Dowding 1995). We found the same correlation between rat numbers and frequency of occurrence of rats in stoat diet as King (1983) found with mice in beech forest. While neither King (1983) nor Murphy & Dowding (1995) found any variation in consumption of birds with mouse abundance in beech forests, we found in podocarp forests that birds were eaten more frequently when rats, the main rodent prey, were scarce. Our results support the conclusions of Korpimaki et al. (1991) that stoats are "semi-generalist" predators, that are not likely to cause declines in rodent densities. The poisoning operations in this study targeted both rats and possums. Alterio & Moller (in press) and Brown et al. (in press) found that eating possum carcases could be an important source of poisoning for stoats in South Island podocarp and beech forests, respectively, but that is unlikely to be the case in this study. Possums densities were very low at Mapara throughout the study (Bradfield & Flux 1996), and this was reflected in the low level of occurrence of possum in the diet of stoats. Possum did not occur in the gut samples of any of the stoats from Kaharoa. The role of mice as an alternative prey for stoats is less clear. Mouse consumption was not consistently higher in successful - or anticoagulantpoison operation years, but we did not have indices of mouse abundance for every year. Mice were eaten mostly in autumn and early winter (unpubl. data) when bird consumption was low, as in beech forests (King 1983). They may form a buffer, reducing the impact on birds of diet switching by stoats after poison operations. Alternatively, the availability of mice in autumn and winter may allow stoat populations to survive even when their main rodent prey, the rat, has been eliminated and birds are scarce. Both hypotheses need to be investigated. Neither weasels nor ferrets consumed enough rats for the poison operations to have a major impact on their diets, but weasels did eat rats when they were abundant. Weasels may face more competition from stoats for mice when rat numbers are drastically reduced, but this did not result in diet shifting by weasels. The possible reduction in the proportion of lagomorphs in the diet of ferrets suggests that rabbit and/or hare densities may also be affected by the poison operations. Both these species are likely to consume poison baits spilled from bait stations (Alterio 1996). Implications for predator control Combining the numerical and functional responses of stoats to the reduction of rat numbers as a 'bird predation index' gives an overall view of the impact of the various poison operations on bird predation by stoats. It indicates that Talon and Pindone operations result in less bird predation pressure from stoats than successful operations. Anticoagulants may have an additional advantage over acute toxins. They may be an effective means of targeting female stoats, which are harder to control by trapping (Buskirk & Lindstedt 1989; Dilks et al. 1996). Virtually all New Zealand forest birds breed in spring and summer (Heather & Robertson 1996) and some poisoning operations are timed to reduce rat numbers during this period. Our finding that secondary poisoning by brodifacoum reduces stoat numbers for 2-3 months (October-December) means that species which finish breeding by the end of December will benefit from reduced stoat predation. The increase in stoat numbers from January onwards will have a negative effect on species that have extended breeding periods (e.g., kiwi (Apteryx spp), kereru (Hemiphaga novaeseelandiae), and kaka (Nestor meridionalis)). The effect on stoats is only one aspect of the success of a pest-poisoning operation. To determine the overall impact on the protected species, we need to determine whether rats or mustelids pose more of a risk to each protected species. For this we need accurate assessments of rat and mustelid densities before and after poisoning, and of the biomass of the particular prey consumed by the two groups (rats and their predators) at varying times of the year and before and after poisoning. Poisoning may also have more complex effects on the forest community. This is demonstrated in this study by the potential impact on lagomorphs and alternative prey of ferrets. Other species are also at risk either directly from poison bait consumption or by secondary poisoning (Godfrey 1985; Spurr 1994; Eason & Spurr 1995).

326 New Zealand Journal of Zoology, 1998, Vol. 25 To be able to make a full cost-benefit assessment of a poison regime we need to know its impact on the primary target species, on additional pests and non-target species and, ultimately, on the species being protected. The present study has provided some indication of the consequences of rat poisoning for mustelids, and leads us closer to effective integrated pest management in New Zealand forests. ACKNOWLEDGEMENTS We are grateful to Department of Conservation staff from Te Kuiti for help with field work, Graham Ussher and Ken Kawiti for help with mustelid autopsies, and Amanda Campbell for library assistance. We thank Nic Alterio, John Dowding, Terry Greene, Don Newman and an anonymous referee for their comments on earlier drafts of this manuscript. REFERENCES Alterio, N. 1996: Secondary poisoning of stoats (Mustela erminea), feral ferrets (Mustela furo), and feral house cats (Felis catus) by the anticoagulant poison, brodifacoum. New Zealand journal of zoology 23: 331-338. Alterio, N.; Moller, H. in press: Restoration of New Zealand's mainland ecological communities by secondary poisoning of introduced mammalian predators. Proceedings of the 18th Vertebrate Pest Conference, California. Alterio, N.; Brown, K.; Moller, H. 1997: Secondary poisoning of mustelids in New Zealand Nothofagus forest. Journal of zoology, London 243: 863-869. Bradfield, P.; Flux, I. 1996: The Mapara kokako project 1989-1996. A summary report. Hamilton, Department of Conservation. 19 p. Brown, K. P.; Alterio, N.; Moller, H. in press: Multipredator control at low mouse (Mus musculus) abundance in a New Zealand Nothofagus forest. Wildlife Research. Buskirk, S. W.; Lindstedt, S. L. 1989: Sex biases in trapped samples of Mustelidae. Journal of mammalogy 7: 88-97. Day, M. G. 1966: Identification of hair and feather remains in the gut and faeces of stoats and weasels. Journal of zoology, London 148: 21-217. Dilks, P. J.; O'Donnell, C. F. J.; Elliott, G. P.; Phillipson, S. M. 1996: The effect of bait type, tunnel design, and trap position on stoat control operations for conservation management. New Zealand journal of zoology 23: 295-36. Dunn, E. 1977: Predation by weasels (Mustela nivalis) on breeding tits (Parus spp.) in relation to the density of tits and rodents. Journal of animal ecology 4(5:633-651. Eason, C. T.; Spurr, E. B. 1995: Review of the toxicity and impacts of brodifacoum on non-target wildlife in New Zealand. New Zealand journal of zoology 22: 371-379. Erlinge, S. 1974: Distribution, territoriality and numbers of the weasel Mustela nivalis in relation to prey abundance. Oikos 25: 38-314. Erlinge, S. 1975: Feeding habits of the weasel Mustela nivalis in relation to prey abundance. Oikos 26: 378-384. Erlinge, S. 1983: Demography and dynamics of a stoat Mustela erminea population in a diverse community of vertebrates. Journal of animal ecology 52: 75-726. Erlinge, S.; Sandell, M. 1988: Co-existence of stoat (Mustela erminea) and weasel (Mustela nivalis): social dominance, scent communication and reciprocal distribution. Oikos 53: 242-246. Gillies, C. 1997: Monitoring the effects of secondary poisoning in predators at Trounson Kauri Park. In: Sim, J; Saunders, A. ed. Predator workshop 1997. Proceedings of a workshop held 21-24 April 1997 St. Arnaud, Nelson Lakes. Wellington, Department of Conservation. Pp. 79-81. Godfrey, M. E. R. 1985: Non-target and secondary poisoning hazards of "second generation" anticoagulants. Acta zoologica fennica 173: 29-212. Grue, H. E.; King, C. M. 1984: Evaluation of age criteria in New Zealand stoats (Mustela erminea) of known age. New Zealand journal of zoology 11: 437-443. Heather, B. D.; Robertson, H. A. 1996: The field guide to the birds of New Zealand. Auckland, Viking. Hegdal, P. E.; Gatz, T. A.; Fite, E. C. 1981: Secondary effects of rodenticides on mammalian predators. In: Chapman, J. A.; Pursley, D. eds. Proceedings of the First Worldwide Furbearer Conference. Frostburg, Worldwide Furbearer Conf, Inc. Pp. 1781-1793. Henderson, R J.; Frampton, C. M.; Thomas, M. D.; Eason, C. T. 1994: Field evaluation of cholecalciferol, gliftor, and brodifacoum for the control of brushtail possums (Trichosurus vulpecula). Proceedings of the 47th N.Z. Plant Protection Conference: 112-116. Innes, J. G. 199: Ship rat. In: King, C. M. ed. The handbook of New Zealand mammals. Auckland, Oxford University Press. Pp. 26-225.

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328 New Zealand Journal of Zoology, 1998, Vol. 25 Saunders, A. 199: Mapara: Island management "mainland" style. In: Towns, D. R.; Daugherty, C. H.; Atkinson, I. A. E. ed. Ecological restoration of New Zealand Islands. Wellington, Department of Conservation. Pp. 147-149. Spurr, E. B. 1994: Review of the impacts on non-target species of sodium monofluoroacetate () in bait used for brushtail possum control in New Zealand. The Royal Society of New Zealand miscellaneous series 28: 124-133. Tapper, S. C. 1979: The effect of fluctuating vole numbers (Microtus agrestis) on a population of weasels (Mustela nivalis) on farmland. Journal of animal ecology 48: 53-517.