Tourism and conservation: The effects of track proximity on avian reproductive success and nest selection in an open sanctuary

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Tourism Management 29 (2008) 730–739 www.elsevier.com/locate/tourman

Tourism and conservation: The effects of track proximity on avian reproductive success and nest selection in an open sanctuary Karen Lindsaya, John Craiga,, Matthew Lowb,1 a

School of Geography and Environmental Science, The University of Auckland, Private Bag 92019, Auckland, New Zealand b Ecology Group, Massey University, Private Bag 11222, Palmerston North, New Zealand Received 5 January 2006; accepted 3 August 2007

Abstract While tourism may provide economic benefits for conservation projects, this relationship is unsustainable if visitors reduce the viability of local ecosystems through the disturbance of wildlife. Tiritiri Matangi Island, in New Zealand, encourages tourism in order to fund its ongoing species’ recovery and habitat restoration programs, yet the impact of this tourism on the local wildlife is currently unknown. We examined nest site selection in open nesting forest birds, and the reproductive success and nest box selection of the endangered cavitynesting stitchbird or hihi Notiomystis cincta, relative to their proximity to public walking tracks. Birds did not avoid nesting near walking tracks and there was no difference between the reproductive parameters of hihi nesting in areas close to public pathways and those in areas where the public had no access. The general population trends of all species monitored on the island suggest that any negative effects posed by tourism are minor and are currently outweighed by the benefits it generates. However, such a relationship is not guaranteed, and ongoing monitoring of tourism impacts on the conservation values of the island is encouraged. r 2007 Elsevier Ltd. All rights reserved. Keywords: Tourism effects; Nest site selection; Avian reproductive success; Stitchbird; Hihi; Tiritiri Matangi Island

1. Introduction Natural area tourism involves experiencing natural ecosystems or wildlife for recreation or education (Haysmith & Hunt, 1995). Although there is a segment of the nature-based tourism market which seeks ‘consumptive’ uses of wildlife such as hunting and fishing, it is the demand for nature-based tourism that focuses on ‘non-consumptive’ uses of wildlife that has grown dramatically in recent times (Parliamentary Commissioner for the Environment, 1997). Non-consumptive use includes observation and photography, which are intended to have little or no deliberate interference with the focal species (Parliamentary Commissioner for the Environment, 1997). A significant proportion of wildlife tourism focuses on Corresponding author. Tel.: +64 9 373 7599x85280; fax: +64 9 373 7042. E-mail addresses: [email protected] (K. Lindsay), [email protected] (J. Craig), [email protected] (M. Low). 1 Current address: Department of Ecology, Swedish University of Agricultural Sciences, PO Box 7002, SE 75007 Uppsala, Sweden.

0261-5177/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tourman.2007.08.001

endangered or threatened species (Shackley, 1996), and much nature-based tourism takes place in protected areas (Ceballos-Lascurain, 1996). Because of this, tourism is both a threat and an opportunity to the long-term conservation of these species and areas. It has long been recognised that tourism can potentially destroy or degrade the environmental resources on which it is based, eventually resulting in reduced conservation values and reduced tourist satisfaction and demand (Butler, 1980). The relationship of tourism to conservation can be classified into three groupings (Budowski, 1976): (1) conflict, where tourism is detrimental to the local environment, (2) coexistence, where tourism has no impact on the area in which it operates, and (3) symbiosis, where conservation values are enhanced by tourism. While these categories are often seen as mutually exclusive, this need not be the case; tourism may have a direct negative impact on the local environment, but partly compensate for this by generating revenue to enhance local conservation values. The goal of protected area managers is to foster a relationship between tourism and conservation that ensures

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‘conflict’ is always less than the compensating ‘symbiosis’. Such an approach increases the likelihood that both ventures will be sustainable. Because the success of conservation ultimately depends on public support (Craig & Stewart, 1994), allowing people to personally experience an area or endangered species builds support for their conservation (Ceballos-Lascurain, 1996). Tourism can also provide the economic rationale for the long-term conservation of endangered and rare species (e.g. Wilson & Tisdell, 2001), and result in the creation or continued existence of protected areas (Hunter & Green, 1995). Despite this potential, creating a symbiotic relationship between tourism and conservation has often been unattainable (Higham & Lu¨ck, 2002). In the past, non-consumptive wildlife tourism has been considered relatively harmless in terms of its effects on wildlife. However, there is growing recognition that activities such as wildlife viewing, photography, and even the simple act of walking through an animal’s territory, can have serious negative impacts on wildlife (Boyle & Samson, 1985; Gutzwiller, 1995; Knight & Cole, 1995; Larson, 1995). Wildlife tourism often attracts high visitor pressure during the breeding seasons of the animals involved, when animals may be particularly vulnerable to disturbance (Parliamentary Commissioner for the Environment, 1997). Much of the research on the impacts of wildlife tourism has focussed on these times (Holmes, Knight, Stegall, & Craig, 1993). In birds, negative impacts of tourism can result in nest failure and reduced reproductive success, which potentially affects population growth or stability of species (Haysmith & Hunt, 1995). In order to conserve the number and diversity of species in tourist locations, it is critical to ensure that populations do not decline as a result of human activities (Gill, Sutherland, & Watkinson, 1996). If tourism is in direct conflict with conservation, neither is sustainable in the long-term and measures need to be put in place to mitigate the negative impacts of tourism on the local wildlife. In order to do this, information is needed to quantify the effects tourism has on the breeding success of target species so that, if a problem is identified, strategies to mitigate potentially adverse effects can be developed and implemented before irreparable damage is caused to the ecosystem. Such policies facilitate the long-term conservation of wildlife populations and hence the sustainability of wildlife tourism activities. 1.1. Avian reproductive success The effects of human activities on the reproductive success of birds is influenced by four factors: (1) the characteristics of the disturbance, (2) the frequency of disturbance, (3) the phase of nesting in which the disturbance occurs, and (4) the degree to which individual birds are habituated to humans (Anderson, 1988; Anderson & Keith, 1980; Bolduc & Guillemette, 2003; Datta & Pal, 1993; Keller, 1989; Knight, 1984; Robert & Ralph,

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1975; Safina & Burger, 1983). A correlation between declines in breeding success and human disturbance has been found particularly among colonial breeding species and predominantly in temperate regions Burger & Gochfeld, 1998. Studies showing this relationship include the following species: herring gulls (Larus argentatus; Hunt, 1972); western gulls (Larus occidentalis; Robert & Ralph, 1975); Heermann’s gulls (Larus heermanni; Anderson & Keith, 1980); black skimmers (Rynchops niger; Safina & Burger, 1983); mourning doves (Zenaida macroura; Westmoreland & Best, 1985); California brown pelicans (Pelecanus occidentalis californicus; Anderson, 1988); piping plovers (Charadrius melodus; Flemming, Chiasson, Smith, Austin-Smith, & Bancroft, 1988); great crested grebes (Podiceps cristatus; Keller, 1989); least terns (Sterna antillarum; Burger, Gochfeld, & Niles, 1995); and Adelie penguins (Pygoscelis adeliae; Giese, 1996). Lowered reproductive success can result from nest desertion by disturbed adult birds, which leaves eggs and young vulnerable to predation or exposure to heat or cold (Go¨tmark, 1992). Nest abandonment has been recorded in several species including: double-crested cormorants (Phalacrocorax auritus; Ellison & Cleary, 1978); black-crowned night herons (Nycticorax nycticorax; Tremblay & Ellison, 1979); California brown pelicans (Anderson & Keith, 1980; Anderson, 1988); black skimmers (Safina & Burger, 1983); and piping plovers (Burger, 1995). Frequent short-term nest abandonment and altered parental attentiveness is often associated with increased nest predation levels in disturbed areas (MacInnes & Misra, 1972, in Anderson, 1988; Anderson & Keith, 1980; Bolduc & Guillemette, 2003; Ellison & Cleary, 1978; Keller, 1991; Robert & Ralph, 1975). Predation levels may also be elevated near walking trails (Miller & Hobbs, 2000) because of human disturbance and/or the fact that trails create habitat edges which are often associated with higher levels of predation (Miller, Knight, & Miller, 1998; Paton, 1994; Wilcove, 1985). In contrast with most studies investigating levels of predation and visitor disturbance, Osborne and Osborne (1980) found that Eurasian blackbird (Turdus merula) nests near human activity had higher reproductive success, possibly because predators in this case were avoiding human contact. Human disturbance can also affect reproductive success by influencing the amount of parental care given to chicks (Verhulst, Oosterbeek, & Ens, 2001); the age at which chicks fledge or leave the nest (which may affect the future survival of young) (Burger et al., 1995; Higham, 1998); and the foraging or energy budgets of both adults and chicks (Burger, 1995; Burger et al., 1995; Flemming et al., 1988; Gabrielsen & Smith, 1995; Henson & Grant, 1991; Leseberg, Hockey, & Loewenthal, 2000; Yalden & Yalden, 1990). In situations where such problems associated with human disturbance are identified, it may be necessary to reduce contact between people and susceptible species at sensitive times; for example, by closing breeding grounds to human activity (Gutzwiller, 1995; Hunter & Green, 1995).

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However, this is only feasible for colonial nesting species that nest in defined areas; consequently, solitary nesters are much more difficult to protect from impacts (Burger, 1995). While tourism is directly responsible for many of these impacts, very little research has focused on the positive effects tourism can have on animal reproduction. At Phillip Island Penguin Reserve in Australia, money raised from tourism has directly enhanced the little blue penguin (Eudyptula minor) colony’s habitat and allowed for the implementation of a predator control scheme, resulting in a significant increase in penguin numbers (Scrase, 1995). At the Oamaru Little Blue Penguin Colony, an ecotourism site in New Zealand, annual visitor numbers to the site doubled from 13,067 to 26,387 between 1994 and 2000 (Houston, 2000, in Higham & Lu¨ck, 2002), and the number of occupied nesting sites also increased from 33 to 103 between 1993 and 1999 (Houston & Russell, 2000, in Higham & Lu¨ck, 2002). Monitoring undertaken by New Zealand’s Department of Conservation at this and another nearby little blue penguin colony, closed to public visitation, has revealed that the ecotourism site consistently outperformed the control colony on most key indicators of breeding success between 1993 and 1999 (Houston & Russell, 2000, in Higham & Lu¨ck, 2002). 1.2. Avian nest site selection Human activities in natural areas are also known to influence avian nest site selection. Serious consequences, including declines in reproductive success, can result if birds are forced to nest in sub-optimal locations. Changes in nesting location may lead to higher levels of energy expenditure needed to reach nests or foraging sites, or to greater exposure of eggs or chicks to wind and temperature changes (Green & Higginbottom, 2001). Ecotourism has been linked to changes in selection of nesting sites in great blue herons (Ardea herodias; Werschkul, McMahon, & Leitschuh, 1976); double-crested cormorants (Ellison & Cleary, 1978); black skimmers (Safina & Burger, 1983); California brown pelicans (Anderson, 1988); golden plovers (Yalden & Yalden, 1990); trumpeter swans (Henson & Grant, 1991); masked, red-footed and bluefooted boobies (Sula dactylatra, Sula sula and Sula nebouxii; Burger & Gochfeld, 1993); openbill storks (Anastomus oscitans; Datta & Pal, 1993); piping plovers (Burger, 1995); least terns (Burger et al., 1995); and northern royal albatross (Diomedea epomophora sanfordi) (Parliamentary Commissioner for the Environment, 1997). Birds of prey reportedly stop nesting altogether in areas visited by tourists (Buckley, 2001). Research indicates that birds learn to avoid factors associated with past failure in nesting attempts (Marzluff, 1988). Black-billed magpies (Pica pica) may alter the placement of their subsequent nests following a human disturbance, making them less accessible (i.e. higher in the canopy; Knight & Fitzner, 1985; but see Dhindsa, Komers,

& Boag, 1989). As predation is a predominant cause of nest failure, and increased nest predation is often found in disturbed areas and near trails, making nests less accessible to humans (also potential predators) and further from trails should be adaptive, if birds can find suitable habitat (Knight & Temple, 1986). Miller et al. (1998) found that nests in grassland ecosystems were more likely to be established away from trails, while nests were evenly distributed around control transects where there was no trail. 1.3. Tiritiri Matangi Island Tiritiri Matangi Island (361360 S, 1741530 E), is a 220 ha scientific reserve managed by New Zealand’s Department of Conservation as an open sanctuary allowing controlled access for tourists (see Fig. 1 for location map). Since 1984, the island has been the site of a large volunteer-based restoration programme, with the investment of over NZ$5 million in public, sponsor and government resources; a significant part of this restoration included the planting of 300,000 trees over 10 years (Craig & Stewart, 1994). Tiritiri Matangi is home to a number of rare and endangered New Zealand forest birds (many of which have been reintroduced to the restored habitat) and it also receives high levels of visitor pressure (over 30,000 people per year), particularly over the summer months. Thus, tourism pressure coincides with the breeding of many avian species on the island, potentially leading to conflict between tourism and conservation. If such conflict is present,

Fig. 1. Location of Tiritiri Matangi Island.

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tourism on Tiritiri Matangi might not be sustainable, as visitors adversely affecting the reproduction of the island’s bird populations may lead to population declines, greatly hindering conservation efforts. A number of species on Tiritiri Matangi are monitored during the breeding season, for conservation management or academic research. The most comprehensive and robust nesting records are those of stitchbird or hihi (Notiomystis cincta). The hihi is a threatened endemic species which is extinct on the New Zealand mainland and found only on a few islands free of introduced predators (Heather & Robertson, 1996). Hihi populations have been the subject of considerable research, with studies focusing primarily on the behaviour and population dynamics of translocated hihi and issues relating to hihi translocations (e.g. Armstrong, Castro, Alley, Fenestra, & Perrott, 1999; Armstrong et al., 2002; Castro, Alley, Empson, & Minot, 1994). Several studies have also looked specifically reproductive behaviour (e.g. Castro, Mason, Armstrong, & Lambert, 2004; Castro, Minot, Fordham, & Birkhead, 1996; Ewen & Armstrong, 2000; Ewen, Armstrong, & Lambert, 1999; Low, 2005; Rasch, 1985) and the links between food supply and population viability (e.g. Armstrong & Ewen, 2001; Armstrong & Perrott, 2000; Castro, Brunton, Mason, Ebert, & Griffiths, 2003). Hihi breed between September and February laying up to three clutches (Wilson, 1998). They are cavity nesters, however on Tiritiri Matangi, nesting occurs in artificial nest boxes, which are provided due to the shortage of mature trees with natural cavities. A pre- and post-breeding census and regular monitoring of hihi nests is carried out by the Department of Conservation and university researchers each breeding season. All hihi on Tiritiri Matangi are colour-banded, allowing the examination of the nesting success of individual females over several clutches and seasons. Consequently, the breeding records of hihi are ideal for an in-depth investigation on the potential effects of visitors and track proximity on reproduction. Anecdotal observation would suggest that other forest birds on the island which have natural, open nests (as opposed to artificial nest boxes) do not avoid proximity to people when nesting; indeed the nests of many species, including tui (Prosthemadera novaeseelandiae), North Island robin (Petroica australis longipes), North Island kokako (Callaeas cinerea wilsoni) and bellbird (Anthornis melanura) can often be found in very close proximity to the tracks. This study is part of a wider investigation into the sustainability of tourism on Tiritiri Matangi Island and which addresses both social and ecological impacts (see Lindsay, 2004). The aim of the current study is to use indicators of negative effects of tourism known for other birds to determine the effects of visitors on the island. Specifically we address the following questions: first, is the reproductive success of hihi affected by the proximity of their nests to a well-used public walking track and viewing area? Second, do hihi avoid nesting in areas closer to the

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walking track? Third, do female hihi preferentially move away from the walking track when they renest after a failed nesting attempt? Finally, is there evidence of any species altering their nesting distribution relative to the presence of walking tracks used by tourists? 2. Methods 2.1. Data collection Hihi breeding data were collected during four breeding seasons from 2000 to 2004 on Tiritiri Matangi Island. This involved daily monitoring of nest boxes from September to February and recording (1) the identity of birds using each nest box, (2) the number of eggs laid, (3) the number of chicks that fledged from each nest, and (4) the number of fledglings that survived and became breeders in the following year. These data were combined with data sourced from breeding records collected by the New Zealand Department of Conservation in 1997/98, 1998/99 and 1999/00 to give a 7-year longitudinal dataset for hihi breeding on the island. For this study, only nesting attempts in the two largest forest fragments were used; these sites were selected because they represent areas where the highest concentration of hihi breeding occurs on the island, with one site having a public walking track through its middle and the other having no public access. In the publicly accessible forest fragment, a boardwalk has been constructed through its middle to provide tourists with the opportunity to see forest-dwelling birds in this habitat. In here we used a tape measure to determine the horizontal position of each hihi nesting box relative to this walking track. This was carried out at the end of the breeding season to minimise disturbance to any nesting birds. In some cases, nest boxes that hihi had used in previous years had been moved; in these instances their original position was determined and the distance to the track was measured from this point. To examine the general distribution of other forest nesting birds (excluding hihi) relative to the public track, four 45-min line-transect surveys were carried out. These involved two observers moving slowly along a predetermined path, recording any nests observed from this line. These surveys were undertaken in the two forest fragments most heavily accessed by visitors to the island (Wattle Valley and Kawerau Bush). Two surveys were carried out in each of the forests; the first was along the public track and the second was taken from a random compass-bearing, which ran through the middle of the forest. The line-transect following the compass bearing was the same length as the public track, and crossed the public track at one point during the survey. If a nest was seen during a survey, then the horizontal and direct distance from the closest point of the line-transect to the nest was estimated (Fig. 2). All four transects were undertaken on the same day, and an equal search effort was maintained on each transect (after Miller et al., 1998). Because we were

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Nest Direct distance

Edge of transect

Horizontal distance

Fig. 2. Distance measurements taken from transects during nest surveys.

interested in a relative comparison of nest frequency between the two transects in each forest fragment, we used absolute numbers of nests observed, rather than a corrected measure that took into account nest sightability with increasing distance from the survey line (e.g. distance sampling; Buckland, Anderson, Burnham, & Laake, 1993). Major differences in vegetation types between these two surveyed forest fragments and others on the island precluded a comparison of nest distribution in areas that received visitors and those that did not.

on whether a female successfully fledged a chick from the nest or not. Nest distances from the track were measured in metres, with birds moving closer to the track being assigned a negative value. While successive clutches have been considered in other studies even if they occur in the following breeding season (up to 8 months apart; Knight & Fitzner, 1985; Marzluff, 1988), we only considered successive clutches if they occurred in the same season. The reason for this is that we were primarily interested in the short-term proximate factors associated with disturbance, and the result of these on the immediate renesting decision-making processes of the female. In all analyses parametric statistics were only used when data or their residuals were normally distributed or were transformed prior to analysis. Tests are two tailed, significance recognised at Po0.05 and means are expressed 71SE unless otherwise stated. All analyses were carried out in Statisticas (version 6.0, StatSoft Inc., 2001). 3. Results 3.1. Hihi reproductive success and nest selection

2.2. Data analysis Hihi nest box occupancy rates relative to distance from the public walking track were examined for three seasons (2000–2003) by partitioning them into three distance categories: o15 m from the track (where there is a visual impact of visitors and noise levels are loudest), 15–40 m from the track (where the track and visitors are less visible and noise levels are moderate) and 440 m from the track (where the visual impact of visitors is minimal and noise levels are low or non-existent). Only box usage for the first clutch of each season was examined, as the total number of clutches for individual females varied between seasons and females. Similar total numbers of boxes were available in the three distance categories in the analysis: o15 m (n ¼ 32), 15–40 m (n ¼ 30), and 440 m (n ¼ 36). If a box was in place for three seasons it was counted as being available for use three times. The relationship between exposure to visitor disturbance and reproductive parameters in the hihi during all seven seasons was examined in two ways; first, a multiple regression compared distance from the walking track relative to three variables—number of eggs laid, number of chicks fledged and number of chicks recruited into the breeding population in the following year. Because female age is known to affect reproductive variables in the hihi (Castro et al., 2003), and the distribution of females relative to the walking track may be non-uniform, female age was included in the regression analysis. The second analysis compared the same reproductive parameters between two sites, a forest fragment where the public had access and a matched site from which the public were excluded. For analyses examining the movement of birds between nesting attempts, group membership was determined based

During the study, approximately half of the available boxes in each distance category were occupied by hihi females for their first nesting attempt each breeding season, with there being no significant association between the level of occupancy and distance category from the track (occupancy rate: category 1 ¼ 50%, category 2 ¼ 53%, category 3 ¼ 47%; Chi-square: w2 ¼ 0.24, d.f. ¼ 2, P ¼ 0.89). There was no relationship between the distance hihi nests were from the walking track and reproductive success (Fig. 3), as measured by the number of eggs laid (F2,67 ¼ 2.51, R2 ¼ 0.04, P ¼ 0.08; female age beta ¼ 0.26, P ¼ 0.02; track distance beta ¼ 0.01, P ¼ 0.89), chicks fledged from the nest (F2,67 ¼ 1.25, R2 ¼ 0.01, P ¼ 0.29; female age beta ¼ 0.16, P ¼ 0.17; track distance beta ¼ 0.07, P ¼ 0.51), or young adults recruited into the breeding population in the following year (F2,56 ¼ 1.26, R2 ¼ 0.01, P ¼ 0.31; female age beta ¼ 0.04, P ¼ 0.71; track distance beta ¼ 0.19, P ¼ 0.15). Also, there was no difference in reproductive parameters between hihi in the forest where visitors had access and a matched area where visitors were not allowed (visitors versus non-visitors; eggs: 4.270.1 versus 4.270.1, t ¼ 0.11, d.f. ¼ 122, P ¼ 0.91; fledglings: 2.270.2 versus 2.270.2, t ¼ 0.0, d.f. ¼ 122, P ¼ 1.0; recruits: 0.770.1 versus 0.870.1, t ¼ 0.91, d.f. ¼ 99, P ¼ 0.36). Females were not more likely to move away from the walking track after a nest failure compared to a nest that successfully fledged chicks (fail versus fledge; mean7SD, 6.2723.6 versus 2.9716.8 m; Mann–Whitney U test: Z ¼ 1.59, n1 ¼ 15, n2 ¼ 28, P ¼ 0.11). This did not change even if we only considered birds that initially nested within 30 m of the track (fail versus fledge; mean7SD; 8.8716.4

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Number of chicks fledged per nest

Number of eggs laid per nest

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5 4 3 2 1 0 20 40 60 80 100 Distance to walking track (m) Number of chicks recruited per nest

0

120

735

4

3

2

1

0 0

20 40 60 80 100 Distance to walking track (m)

120

2

1

0 0

20 40 60 80 100 Distance to walking track (m)

120

Fig. 3. Reproductive parameters in the hihi relative to the distance from the public walking track. There was no significant relationship between proximity to the track and (a) number of eggs laid (n ¼ 70), (b) number of chicks fledged (n ¼ 70), or number of chicks recruited into the breeding population (n ¼ 59). Not all points are represented in the figures because of superimposition.

versus 5.1715.3 m; Z ¼ 0.96, n1 ¼ 11, n2 ¼ 16, P ¼ 0.34). However, on 7/8 occasions when the female renested in the same box in the same year, she had successfully fledged chicks from that nest (7/28 successful females renested in the same box versus 1/15 unsuccessful females; Fisher’s exact test: P ¼ 0.22). Because of the limited power of this test, we expanded this analysis to include all nesting attempts in the Tiritiri Matangi hihi population from 1997 to 2004. Females showed a trend for remaining in the same box after successfully fledging chicks (23/123 occasions) when compared to the likelihood of them renesting in the same box immediately after their nest had failed (3/42 occasions; Fisher’s exact test, P ¼ 0.09). 3.2. Naturally nesting species Fifteen nests were detected during the survey transects along the public walking tracks, and 12 nests were found on the off-track transects. There was no significant difference between the transect types in the measures of mean horizontal distance to nests (track versus off-track; 3.570.8 versus 3.970.7 m; Mann–Whitney U test: U ¼ 68.5, P ¼ 0.29) or direct distances to nests (track versus off-track; 4.570.8 versus 5.571.0 m; U ¼ 71, P ¼ 0.35).

4. Discussion This study provided no evidence to support the hypothesis that proximity to the public walking track affects the reproductive parameters of hihi. Reproductive success ultimately depends on the recruitment of young into the breeding population; thus, it was important to examine the long-term impacts on breeding and not restrict analyses to short-term parameters such as egg production or fledging success. This highlights the strength of this study; we had a 7-year longitudinal dataset of a population containing marked individuals of known age and sex, which allowed us to examine factors such as recruitment— something that previous studies have been unable to do. While we found that hihi females did not avoid nest boxes closer to public areas and did not associate nest failure with track proximity, these results should be interpreted with caution. Because of the lack of natural nesting cavities on the island, nest boxes are provided in clusters throughout likely nesting areas. Thus, the distribution of nest boxes is non-uniform and may confound investigations into nest box choice. Also, territorial birds like the hihi are constrained by the activity of conspecifics: i.e. they cannot necessarily choose where they nest, as other birds may exclude them from a preferred area. Despite this

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caution, the fact that birds in nest boxes near tracks were just as likely to successfully rear chicks that survived to successfully breed suggests that there is no selection pressure to avoid public areas. Effects reported in the literature that lead to lowered reproductive success, such as short- and long-term abandonment of nests by disturbed females (Anderson, 1988; Anderson & Keith, 1980; Burger, 1995; Ellison & Cleary, 1978; Safina & Burger, 1983; Tremblay & Ellison, 1979), and increased or decreased nest predation near people or tracks (MacInnes & Misra, 1972, in Anderson, 1988; Anderson & Keith, 1980; Bolduc & Guillemette, 2003; Ellison & Cleary, 1978; Keller, 1991; Miller & Hobbs, 2000; Miller et al., 1998; Osborne & Osborne, 1980; Paton, 1994; Robert & Ralph, 1975; Wilcove, 1985), may be mitigated in the hihi by the fact that females nest in cavities and are not as exposed to disturbance or predators as the non-cavity nesting birds examined in other studies. One aspect that was not addressed in this study was the vertical dimension of nest-box selection. In Knight and Fitzner (1985) and Datta and Pal (1993), they document the altered location of nests away from human disturbance following nest failure; however, in their studies the change was vertical rather than horizontal. Hihi were unable to alter their nest height because of constraints placed on them by the position of the nest boxes, thus, we could not examine this possibility. It was interesting to note that females across the island were more likely to renest in the same box immediately after successfully rearing a brood than if that nesting attempt had failed. This suggests that individual birds associate nest failure with the attributes of a nest location or box as suggested by Marzluff (1988). One confounding variable that we could not control in this study, was disturbance of nesting females by researchers and conservation managers. Hihi on Tiritiri Matangi Island are intensively studied and managed, with the impact of this disturbance currently unknown. In some species the frequency of visits by researchers to the nest can reduce reproductive success (Go¨tmark, 1992). On Tiritiri Matangi this type of disturbance may have a greater impact than that of visitors, and therefore may have prevented us from detecting subtle influences of tourism on breeding biology. The potential effects of research and management is an area frequently overlooked, and one which may need to be addressed on Tiritiri Matangi Island in the future. However, the ongoing viability of the island’s hihi population suggests that these activities are unlikely to negatively affect reproduction at present. Based on the transect surveys, there similarly was no evidence to support the hypothesis that open-nesting forest species avoid nesting close to public tracks. Therefore, in contrast with previous studies (e.g. Burger & Gochfeld, 1993; Miller et al., 1998; Werschkul et al., 1976), it appears that the natural (non-box) nesting birds of Tiritiri Matangi do not avoid (or favour) proximity to tracks in their nest site selection at the two sites investigated. In other studies, changes in nesting distribution have been related to

predation rates, with higher predation in areas associated with tracks and/or people. This suggests that predation rates on Tiritiri Matangi are not influenced by proximity to areas where people frequent. This is likely to be because on Tiritiri Matangi, and in many areas of the North Island of New Zealand, the only diurnal forest predator is the Australasian harrier (Circus approximans) which is highly averse to being near people (J. Craig, pers. obs.). Thus, New Zealand forest birds in areas associated with people could benefit from their presence, although research on predation levels is needed to confirm this. Another possibility is that many New Zealand species are naı¨ ve to ground predators and naturally curious, potentially mitigating human disturbance that might affect other species. Habituation is a documented behavioural response of wildlife exposed to human disturbance: a process whereby an animal gradually learns not to respond to a predictable disturbance if the disturbance has no consequences for the individual (Knight & Temple, 1995; Reynolds & Braithwaite, 2001; Shackley, 1996). In some cases, habituation is advantageous to both the visitor experience and the wildlife populations involved. It can facilitate the coexistence of humans and wildlife populations with minimal negative effects, as habituated animals do not ‘waste’ energy responding to humans (Green & Higginbottom, 2001; Shackley, 1996). Habituation also maximises viewing opportunities for visitors, as animals will allow closer approaches and generally be less wary of people (Burger & Gochfeld, 1991; Reynolds & Braithwaite, 2001). However, not all species will habituate to human disturbance, and those which do may still be sensitive to human disturbance in certain situations, such as during the breeding season (Shackley, 1996). Several investigations have confirmed that birds can habituate to human disturbance if it occurs in the absence of persecution (e.g. Burger & Gochfeld, 1991; Burger et al., 1995; Cooke, 1980; Kenney & Knight, 1992). Short-term avian behavioural responses under varied visitor densities were examined as part of a wider investigation into the sustainability of tourism on Tiritiri Matangi Island (see Lindsay, 2004). For all species studied, visitor density was found to have no significant effect on the frequency of occurrence of the majority of behaviours examined. This result suggests that the avian populations on the island are relatively well habituated to the highly predictable visitor disturbance they are exposed to. The results of the current investigation on reproductive success and nest site selection on the island add further weight to this hypothesis. In fact, it appears that the biggest threat to sustainability of tourism on the island are social impacts, such as crowding perceptions experienced by visitors, rather than any negative impacts on the island’s avian populations (Lindsay, 2004). The effects of tourism on avian reproduction on Tiritiri Matangi need only be managed if there are clear negative population trends. General trends in bird numbers on the island appear no cause for concern; in fact, bird counts

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from the Ornithological Society of New Zealand from the last 15 years show continual increases in all native populations (Graham & Veitch, 2002). Tourism (largely via voluntary donations by visitors) directly funds much of the conservation work carried out on the island, with the Supporters of Tiritiri Matangi Island Inc. (the organisation that raises funds for the management of Tiritiri Matangi) providing resources for the supplementary feeding of the hihi population. This supplementary feeding is recognised as necessary for the viability of this population (Taylor, Castro, & Griffiths, 2005) and is likely to have significantly contributed to the large increase in hihi numbers since their reintroduction 10 years ago. So successful has this project been, that the New Zealand Department of Conservation’s Stitchbird Recovery Group is now using surplus hihi (stitchbirds) from Tiritiri Matangi Island to establish new populations elsewhere (e.g. Karori Wildlife Sanctuary in Wellington). For hihi on Tiritiri Matangi Island, and the recovery of this species in general, the relationship between tourism and conservation can be seen as one of ‘symbiosis’ (Budowski, 1976). Given the seeming indifference of other forest nesting species which are also sustained at high population levels, this symbiotic relationship between visitors and native birds appears to apply to Tiritiri Matangi Island as a whole.

5. Conclusions Despite the positive relationship between tourism and conservation highlighted in this study, this relationship is dynamic and may change in the future (Parliamentary Commissioner for the Environment, 1997). Consequently, long-term monitoring of tourism’s impacts and an adaptive management framework, which are generally regarded as essential to the sustainability of tourism in natural areas (Fennell, 2002; Green & Higginbottom, 2001) are required. Long-term monitoring of population trends of all species on the island will ensure that any changes are detected and can be investigated before irreparable ecological damage is sustained. It is also important that social impacts and the visitor experience on the island are regularly monitored, as these types of impacts currently appear to be more of a threat to overall sustainability than wildlife impacts. Currently Tiritiri Matangi Island’s popularity with tourists generates public and political interest and provides a significant revenue source for implementing conservation programmes. From experiences in other parts of the world, such a positive outcome for both tourism and conservation is unusual, thus, there needs to be mechanisms in place to ensure this positive relationship continues. For tourism on the island to be truly sustainable, there needs to be a longterm commitment that the users of this ecosystem will contribute financially to its maintenance (Lindsay, 2004). At least some of the funds raised in this way can contribute to an improved research base and more effective understanding of the potential effects of tourism on the island’s

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endangered species and the ways in which the visitor experience can be enhanced. Acknowledgements The authors would acknowledge the Supporters of Tiritiri Matangi Inc. for providing financial assistance to this investigation, and the Department of Conservation staff on the island (Ray and Barbara Walter, Ian Price and Sandra Jack) for their invaluable support and assistance. References Anderson, D. W. (1988). Dose–response relationship between human disturbance and brown pelican breeding success. Wildlife Society Bulletin, 16, 339–345. Anderson, D. W., & Keith, J. O. (1980). The human influence on seabird nesting success: Conservation implications. Biological Conservation, 18, 65–80. Armstrong, D. P., & Ewen, J. G. (2001). Testing for food limitation in reintroduced hihi populations: Contrasting results for two islands. Pacific Conservation Biology, 7, 87–92. Armstrong, D. P., & Perrott, J. K. (2000). An experiment testing whether condition and survival are limited by food supply in a translocated hihi population. Conservation Biology, 14, 1171–1181. Armstrong, D. P., Castro, I., Alley, J. C., Fenestra, B., & Perrott, J. K. (1999). Mortality and behaviour of hihi, an endangered New Zealand honeyeater, in the establishment phase following translocation. Biological Conservation, 89, 329–339. Armstrong, D. P., Davidson, R. S., Dimond, W. J., Perrott, J. K., Castro, I., Ewen, J. G., et al. (2002). Population dynamics of reintroduced forest birds on New Zealand islands. Journal of Biogeography, 29(5–6), 609–621. Bolduc, F., & Guillemette, M. (2003). Human disturbance and nesting success of common eiders: Interaction between visitors and gulls. Biological Conservation, 110, 77–83. Boyle, S. A., & Samson, F. B. (1985). Effects of non-consumptive recreation on wildlife: A review. Wildlife Society Bulletin, 13, 110–116. Buckland, S. T., Anderson, D. R., Burnham, K. P., & Laake, J. L. (1993). Distance sampling. London: Chapman & Hall. Buckley, R. (2001). Ecotourism impacts: Environmental impacts. In D. B. Weaver (Ed.), The encyclopedia of ecotourism (pp. 379–394). Oxon: CABI Publishing. Budowski, G. (1976). Tourism and environmental conservation: Conflict, coexistence, or symbiosis? Environmental Conservation, 3(1), 27–32. Burger, J. (1995). Beach recreation and nesting birds. In R. L. Knight, & K. J. Gutzwiller (Eds.), Wildlife and recreationists: Coexistence through management and research (pp. 281–295). Washington: Island Press. Burger, J., & Gochfeld, M. (1991). Human disturbance and birds: Tolerance and response distances of resident and migrant species in India. Environmental Conservation, 18(2), 158–165. Burger, J., & Gochfeld, M. (1993). Tourism and short-term behavioural responses of nesting masked, red-footed and blue-footed boobies in the Gala´pagos. Environmental Conservation, 20(3), 255–259. Burger, J., & Gochfeld, M. (1998). Effects of ecotourists on bird behaviour at Loxahatchee National Wildlife Refuge, Florida. Environmental Conservation, 25, 13–21. Burger, J., Gochfeld, M., & Niles, L. J. (1995). Ecotourism and birds in coastal New Jersey: Contrasting responses of birds tourists, and managers. Environmental Conservation, 22(1), 56–65. Butler, R. W. (1980). The concept of a tourist-area cycle of evolution and implications for management. The Canadian Geographer, 24, 5–12. Castro, I., Alley, J. C., Empson, R. A., & Minot, E. O. (1994). Translocation of hihi or stitchbird (Notiomystis cincta) to Kapiti Island, New Zealand: Transfer techniques and comparison of release

ARTICLE IN PRESS 738

K. Lindsay et al. / Tourism Management 29 (2008) 730–739

strategies. In M. Serena (Ed.), Reintroduction biology of Australian and New Zealand fauna (pp. 113–120). Chipping Norton: Surrey Beatty. Castro, I., Brunton, D. H., Mason, K. M., Ebert, B., & Griffiths, R. (2003). Life history traits and food supplementation affect productivity in a translocated population of the endangered hihi (stitchbird, Notiomystis cincta). Biological Conservation, 114, 271–280. Castro, I., Mason, K. M., Armstrong, D. P., & Lambert, D. M. (2004). Effect of extra-pair paternity on effective population size in a reintroduced population of the endangered hihi, and potential for behavioural management. Conservation Genetics, 5(3), 381–393. Castro, I., Minot, E. O., Fordham, R. A., & Birkhead, T. R. (1996). Polyandry, face-to-face copulation and sperm competition in the Hihi Notiomystis cincta (Aves: Meliphagidae). Ibis, 138(4), 765–771. Ceballos-Lascurain, H. (1996). Tourism, ecotourism, and protected areas: The state of nature-based tourism around the world and guidelines for its development. Gland, Switzerland: The World Conservation Union. Cooke, A. S. (1980). Observations on how close certain passerine species will tolerate an approaching human in rural and suburban areas. Biological Conservation, 18, 85–88. Craig, J. L., & Stewart, A. M. (1994). Conservation: A starfish without a central disk? Pacific Conservation Biology, 1, 163–168. Datta, T., & Pal, B. C. (1993). The effect of human interference on the nesting success of the openbill stork Anastomus oscitans at the Raijganj wildlife Sanctuary, India. Biological Conservation, 64, 149–154. Dhindsa, M. S., Komers, P. E., & Boag, D. A. (1989). Nest height of black-billed magpies: Is it determined by human disturbance or habitat type? Canadian Journal of Zoology, 67, 228–232. Ellison, L. N., & Cleary, L. (1978). Effects of human disturbance on breeding of double-crested cormorants. Auk, 95, 510–517. Ewen, J. G., & Armstrong, D. P. (2000). Male provisioning is negatively correlated with attempted extrapair copulation frequency in the stitchbird (or hihi). Animal Behaviour, 60(4), 429–433. Ewen, J. G., Armstrong, D. P., & Lambert, D. M. (1999). Floater males gain reproductive success through extrapair fertilizations in the stitchbird. Animal Behaviour, 58(2), 321–328. Fennell, D. A. (2002). Ecotourism Programme Planning. Oxon: CABI Publishing. Flemming, S. P., Chiasson, R. D., Smith, P. C., Austin-Smith, P. J., & Bancroft, R. P. (1988). Piping plover status in Nova Scotia related to its reproductive and behavioural responses to human disturbance. Journal of Field Ornithology, 59(4), 321–330. Gabrielsen, G. W., & Smith, E. N. (1995). Physiological responses of wildlife to disturbance. In R. L. Knight, & K. J. Gutzwiller (Eds.), Wildlife and recreationists: Coexistence through management and research (pp. 95–107). Washington: Island Press. Giese, M. (1996). Effects of human activity on Adelie penguin Pygoscelis adeliae breeding success. Biological Conservation, 75, 157–164. Gill, J. A., Sutherland, W. J., & Watkinson, A. R. (1996). A method to quantify the effects of human disturbance on animal populations. Journal of Applied Ecology, 33, 786–792. Go¨tmark, F. (1992). The effects of investigator disturbance on nesting birds. In D. M. Power (Ed.), Current Ornithology 9 (pp. 63–104). New York: Plenum Press. Graham, M. F., & Veitch, C. R. (2002). Changes in bird numbers on Tiritiri Matangi Island, New Zealand, over the period of rat eradication. In C. R. Veitch, & M. N. Clout (Eds.), Turning the tide: The eradication of invasive species (pp. 120–123). Gland, Switzerland: IUCN SSC Invasive Species Specialist Group. Green, R., & Higginbottom, K. (2001). The Negative Effects of Wildlife Tourism on Wildlife. Wildlife Tourism Research Report Series: No 5. Status Assessment of Wildlife Tourism in Australia Series. Australia: Cooperative Research Centre for Sustainable Tourism. Gutzwiller, K. J. (1995). Recreational disturbance and wildlife communities. In R. L. Knight, & K. J. Gutzwiller (Eds.), Wildlife and recreationists: Coexistence through management and research (pp. 169–181). Washington: Island Press. Haysmith, L., & Hunt, J. D. (1995). Nature tourism: Impacts and management. In R. L. Knight, & K. J. Gutzwiller (Eds.), Wildlife and

recreationists: coexistence through management and research (pp. 203–219). Washington: Island Press. Heather, B. D., & Robertson, H. A. (1996). The field guide to the birds of New Zealand. Auckland: Penguin Books Ltd. Henson, P., & Grant, T. A. (1991). The effects of human disturbance on trumpeter swan breeding behaviour. Wildlife Society Bulletin, 19, 248–257. Higham, J. E. S. (1998). Tourists and albatrosses: The dynamics of tourism at the northern royal Albatross colony, Taiaroa head, New Zealand. Tourism Management, 19(6), 521–531. Higham, J. E. S., & Lu¨ck, M. (2002). Urban ecotourism: A contradiction in terms? Journal of Ecotourism, 1(1), 36–51. Holmes, T. L., Knight, R. L., Stegall, L., & Craig, G. R. (1993). Responses of wintering grassland raptors to human disturbance. Wildlife Society Bulletin, 21, 461–468. Hunt, G. L. (1972). Influence of food distribution and human disturbance on the reproductive success of herring gulls. Ecology, 53(6), 1051–1061. Hunter, C., & Green, H. (1995). Tourism and the environment: A sustainable relationship? London: Routledge Chapter 2. Kenney, S. P., & Knight, R. L. (1992). Flight distances of black-billed magpies in different regimes of human density and persecution. Condor, 94, 545–547. Keller, V. E. (1989). Variations in the response of great crested grebes Podiceps cristatus to human disturbance—a sign of adaptation. Biological Conservation, 49, 31–45. Keller, V. E. (1991). Effects of human disturbance on eider ducklings Somateria mollissima in an estuarine habitat in Scotland. Biological Conservation, 58, 213–228. Knight, R. L. (1984). Responses of nesting ravens to people in areas of different human densities. Condor, 86, 345–346. Knight, R. L., & Cole, D. N. (1995). Wildlife responses to recreationists. In R. L. Knight, & K. J. Gutzwiller (Eds.), Wildlife and recreationists: Coexistence through management and research (pp. 51–69). Washington: Island Press. Knight, R. L., & Fitzner, R. E. (1985). Human disturbance and nest site placement in black-billed magpies. Journal of Field Ornithology, 56(2), 153–157. Knight, R. L., & Temple, S. A. (1986). Nest defence in the American goldfinch. Animal Behaviour, 34, 887–897. Knight, R. L., & Temple, S. A. (1995). Origin of wildlife responses to recreationists. In R. L. Knight, & K. J. Gutzwiller (Eds.), Wildlife and recreationists: Coexistence through management and research (pp. 81–91). Washington: Island Press. Larson, R. A. (1995). Balancing wildlife viewing with wildlife impacts: A case study. In R. L. Knight, & K. J. Gutzwiller (Eds.), Wildlife and recreationists: Coexistence through management and research (pp. 257–270). Washington: Island Press. Leseberg, A., Hockey, P. A. R., & Loewenthal, D. (2000). Human disturbance and the chick-rearing ability of African black oystercatchers (Haematopus moquini): A geographical perspective. Biological Conservation, 96, 379–385. Lindsay, K.A. (2004). The sustainability of natural area tourism: A case study of Tiritiri Matangi Island. Unpublished M.Sc. thesis, University of Auckland, Auckland, New Zealand. Low, M. (2005). Factors influencing mate guarding and territory defence in the stitchbird (hihi) Notiomystis cincta. New Zealand Journal of Ecology, 29(2), 231–242. Marzluff, J. M. (1988). Do pinyon jays alter nest placement based on prior experience? Animal Behaviour, 36, 1–10. Miller, J. R., & Hobbs, N. T. (2000). Recreational trails, human activity, and nest predation in lowland riparian areas. Landscape and Urban Planning, 50, 227–236. Miller, S. G., Knight, R. L., & Miller, C. K. (1998). Influence of recreational trails on breeding bird communities. Ecological Applications, 8(1), 162–169. Osborne, P., & Osborne, L. (1980). The contribution of nest characteristics to breeding-success among blackbirds Turdus merula. Ibis, 122, 512–517.

ARTICLE IN PRESS K. Lindsay et al. / Tourism Management 29 (2008) 730–739 Parliamentary Commissioner for the Environment. (1997). Management of the environmental effects associated with the tourism sector: Review of literature on environmental effects. Wellington: Parliamentary Commissioner for the Environment. Paton, P. W. (1994). The effect of edge on avian nest success: How strong is the evidence? Conservation Biology, 8(1), 17–26. Rasch, G. (1985). The ecology of cavity nesting in the stitchbird (Notiomystis cincta). New Zealand Journal of Zoology, 12, 637–642. Reynolds, P. C., & Braithwaite, D. (2001). Towards a conceptual framework for wildlife tourism. Tourism Management, 22, 31–42. Robert, H. C., & Ralph, C. J. (1975). Effects of human disturbance on the breeding success of gulls. Condor, 77, 495–499. Safina, C., & Burger, J. (1983). Effects of human disturbance on reproductive success in the black skimmer. Condor, 85, 164–171. Scrase, D. (1995). Phillip island Penguin reserve. In R. Harris, & N. Leiper (Eds.), Sustainable tourism: An Australian perspective. Chatswood: Butterworth-Heinemann. Shackley, M. (1996). Wildlife tourism. London: International Thompson Business Press. StatSoft, Inc. (2001). STATISTICA (data analysis software system), version 6. /www.statsoft.comS.

739

Taylor, S., Castro, I., & Griffiths, R. (2005). Hihi/stitchbird (Notiomystis cincta) Recovery Plan 2004–2009. Wellington: New Zealand Department of Conservation. Tremblay, J., & Ellison, L. N. (1979). Effects of human disturbance on breeding of black-crowned night herons. Auk, 96, 815–816. Verhulst, S., Oosterbeek, K., & Ens, B. J. (2001). Experimental evidence for effects of human disturbance on foraging and parental care in oystercatchers. Biological Conservation, 101, 375–380. Werschkul, D. F., McMahon, E., & Leitschuh, M. (1976). Some effects of human activities on the great blue heron in Oregon. Wilson Bulletin, 88(4), 660–662. Westmoreland, D., & Best, L. B. (1985). The effect of disturbance on mourning dove nesting success. Auk, 102, 774–780. Wilcove, D. S. (1985). Nest predation in forest tracts and the decline of migratory songbirds. Ecology, 66(4), 1211–1214. Wilson, C., & Tisdell, C. (2001). Sea turtles as a non-consumptive tourism resource especially in Australia. Tourism Management, 22, 279–288. Wilson, L. (1998). Breeding season management of the stitchbird (hihi) on Tiritiri Matangi Island. Auckland Conservancy Technical Report Series no. 18. Auckland Conservancy: Department of Conservation. Yalden, P. E., & Yalden, D. W. (1990). Recreational disturbance of breeding golden plovers Pluvialis apricarius. Biological Conservation, 51, 243–262.