Arboreal activity of invasive rodents: conservation implications for the control of an island pest

Introduction

Invasive rodents, particularly rats (e.g. Rattus rattus, R. exulans, R. norvegicus) and mice (Mus musculus), are a leading cause of species population decline and extinction worldwide (Bellard et al. 2016; Doherty et al. 2016; Dueñas et al. 2021). These species have this effect due to their ability to rapidly reach high abundance, capacity to occupy a wide range of habitats, predatory behaviour, and omnivorous diets (Harper and Bunbury 2015; Witmer and Shiels 2018). Island ecosystems are particularly susceptible to invasive species given their high rates of vulnerable endemic species compared to mainland ecosystems (Kier et al. 2009; Ruffino et al. 2015). Alarmingly, 47% of the world’s islands that are home to one or more highly threatened vertebrate species also harbour one or more invasive Rattus species (Spatz et al. 2017). The ongoing threat invasive rodents pose to island and global biodiversity is therefore severe, with invasive rodent management a major conservation priority for island ecosystems (Duron et al. 2017).

Two major strategies used by conservation managers to protect biodiversity from invasive rodents are eradication (complete removal of rodents from the system; Howald et al. 2007) or population control (suppressing rodent abundance to reduce impact; Howald et al. 2015; Duron et al. 2017). Eradication programs are highly effective, with success rates of up to 96% on uninhabited islands (Keitt et al. 2015). However, in mainland regions or on islands with resident human populations, long-term control is often favoured over eradication due to the associated logistical and sociological aspects of species management (Engeman et al. 2018). Where rodent suppression is the chosen management strategy, long-term ground-based trapping and baiting programs are commonly used (Brown et al. 2015; Howald et al. 2015; Duron et al. 2017). Although long-term control programs can reduce rodent abundance, they can become less effective with time due to genetic or behavioural resistance to rodenticide, or as the proportion of bait- or trap-shy individuals within a population increases (Allsop et al. 2017; Gronwald and Russell 2022). In such situations, it is valuable to explore alternative strategies to improve rodent control outcomes (Fig. 1).

Fig. 1.

Conceptual diagram detailing the decision-making process for invasive rodent control once invasive rodents have been identified as a management concern (i.e. having a negative ecological impact on native species). Various scenarios or states need to be assessed (green boxes) to determine which actions (blue and yellow boxes) are required. The yellow box identifies the stage within the decision-making process at which the present study sits.

The potential interaction between ground-based control and arboreal behaviour of invasive rodents is an aspect of management that is not often explored despite this behaviour being well documented (see Shiels et al. 2014). Previous research has reported the climbing abilities of Rattus species in simulated environments (Foster et al. 2011) and has demonstrated directly and indirectly that Rattus species prey on arboreal taxa (e.g. Hadfield and Saufler 2009; Smith et al. 2016; Banko et al. 2019; Shiels and Ramírez de Arellano 2019; Nance et al. 2023). Although arboreal rodents may regularly come to ground (Lindsey et al. 1999), their behaviour has raised concerns over the effectiveness of control techniques that are solely ground-based (Nelson et al. 2002; Wegmann et al. 2011). Indeed, arboreal behaviour was considered a factor in the failure of the 2001–2002 rat (R. rattus) eradication attempt on Palmyra Atoll, leading researchers to place bait in the canopy to achieve success during the 2011 operation (Wegmann et al. 2014). This mirrors other studies showing that bait delivered above-ground can increase bait uptake from black rats (Tobin et al. 1997), and decrease uptake from non-target species (Ringler et al. 2021). Ecologically informed rodent management should consider both habitat use and foraging behaviour when placing bait and designing control networks (Krijger et al. 2017). Considering this, a more comprehensive understanding of arboreal rodent behaviour in systems that conduct long-term ground-based control, or those considering an eradication campaign would be beneficial.

In this study, we aimed to determine invasive rodent presence/absence and generate indices of rodent activity across multiple forest strata and forest types in an island system that has been subject to an extensive, long-term ground-baiting program. Understanding arboreal rodent activity in this context has the potential to inform local management strategies. More broadly, such insight is likely to be relevant to systems where long-term ground-based rodent control programs are exhibiting reduced efficacy over time.

Methods

Study system

Norfolk Island, an external Australian territory, is an oceanic island situated in the South Pacific Ocean (29°02′S 167°57′E) with a land area of 34.6 km² (Geosciences Australia 2021). Due to its geographical isolation (~1100 km from New Zealand and ~1500 km from Australia), this island group is home to many unique species, including 40 endemic plant species, eight endemic land bird species, and >100 known endemic invertebrate species. Fifty-eight species of plants and animals are recognised as threatened (Director of National Parks 2023). Current threats to biodiversity are associated with historical and contemporary human habitation, and include land clearing and degradation, feral and domestic cats (Felis catus), invasive rodents (Rattus rattus, R. exulans and Mus musculus), feral chickens (Gallus gallus) invasive woody and non-woody plants, and climate change (Director of National Parks 2023). Norfolk Island currently supports a resident human population of ~2200 (Australian Bureau of Statistics 2021).

This case study focused on the Norfolk Island National Park (NINP) and the adjoining Botanical Gardens (Fig. 2). Collectively, NINP and the Botanical Gardens protect 465.5 ha of Norfolk Island (Director of National Parks 2023). Plant communities in the park are characterised as sub-tropical rainforest, including native palm-dominated forest, and native hardwood forest (Fig. 2a, b; Director of National Parks 2023). Native palm forest is characterised by the dominance of the endemic Niau palm (Rhopalostylis baueri) and exhibits a high canopy (9–14 m) with an open, structurally simplistic understorey. Native hardwood forest is characterised by the dominance of Norfolk Island pine (Araucaria heterophylla) and hardwood species such as bloodwood (Baloghia inophylla), ironwood (Nestegis apetala), and beech (Myrsine ralstoniae), and exhibits a high canopy (6.5–14 m) with a structurally complex understorey. Exotic red cherry guava (Psidium cattleyanum) is a naturalised and invasive woody species on Norfolk Island and now dominates areas of forest within NINP (Fig. 2c; Director of National Parks 2023). Cherry guava is allelopathic and forms dense thickets that exhibit a lower, more uniform canopy (3.8–11.5 m) than native forests, with little to no understorey (Tng et al. 2016).

Fig. 2.

Location of 30 sites established to monitor invasive rodent activity in Norfolk Island National Park and adjoining Botanic Gardens (green polygons). Points indicate location of each site shaded by forest type, with typical forest structure of each respective forest type depicted in photographic images: white points represent forest sites dominated by (a) native Niau palm (Rhopalostylis baueri); grey points represent forest sites dominated by (b) Araucaria heterophylla and native hardwood species; black points represent forest sites dominated by (c) invasive red cherry guava (Psidium cattleyanum). Inset shows the location of the National Park relative to the island. Photo credits: A Nance.

Arboreal behaviour of invasive Rattus species was first documented in NINP in 1988, but is likely to have been prevalent since the arrival of black rats in the 1940s (Robinson 1988). Recent rodent surveys in the park (conducted in 2016) suggested very high levels of arboreality, with >80% of rodent detections made above-ground (R. Clarke, unpublished data). Combined with high levels of rodent activity within the National Park, practitioners and researchers expressed concerns around a solely ground-based baiting strategy for the purposes of long-term control. In line with adaptive management principles (Williams and Brown 2014), this study was conceptualised by practitioners and researchers to address the uncertainty around the extent of arboreal behaviour in the context of long-term ground-based control.

Sampling strategy

We established 30 sites along public walking tracks or non-public service tracks representing three focal forest types: invasive cherry guava (n = 10), native hardwood (n = 10), and native palm forests (n = 10; Fig. 2). There is a paucity of sites in the west and north-west sections of the Park because these areas are dominated by plantations of Eucalyptus sp., and thickets of African olive (Olea europaea; Fig. 2). At each site we established a 100 m transect and a circular buffer (radius = 90 m) from the transect mid-point (2.5 ha area). This buffer area (2.5 ha) corresponded to three times the mean core area occupied by an individual of the largest rodent species present on Norfolk Island (i.e. the ‘core home range’ of R. rattus; Shiels 2010). To ensure sampling independence, the buffer area for each site did not overlap with that of any other site, which equates to a minimum distance of 180 m between site mid-points.

Three monitoring stations were established at the centre of each site (transect mid-point), one for each focal stratum: ground, mid-storey and canopy spaced 5–10 m from any other station (Fig. 3). The mid-storey was defined as approximately half the height of the canopy, as measured by a laser range finder (Opti-Logic, model: 800LH). Each monitoring station comprised three commonly used passive monitoring devices: a motion-triggered infrared camera trap (Reconyx HyperFire HC600), a chew card baited with a non-toxic peanut butter lure (Connovation GC136), and a tracking tunnel with a non-toxic peanut butter lure (Gotcha Traps, Black Trakka standard size) (Blackwell et al. 2002; Sweetapple and Nugent 2011; Rendall et al. 2014). We deployed the three devices at each monitoring station as a cluster, with each device situated within 1 m of each other. A small number of cameras were pointed at another monitoring device, however all cameras were considered to be baited due to their proximity to baited chew cards and tunnels.

Fig. 3.

Deployment heights of invasive rodent monitoring stations by forest type across 30 sites in Norfolk Island National Park. Mean canopy height for each forest type is represented by the maximum height of trees. Mean deployment heights of monitoring stations per stratum (ground, mid-storey and canopy) are represented by the heights of monitoring station images. Box and whisker plots indicate variation in deployment heights of mid-storey (grey boxes) and canopy (white boxes) stations. All ground stations were deployed on the ground (i.e. 0 m) and did not vary in height. Lines inside boxes indicate median heights, lower and upper box boundaries indicate 25th and 75th percentiles respectively, lower and upper whiskers indicate 95% confidence intervals. Filled circles indicate outliers.

Monitoring equipment was deployed at each station across two seasons: austral spring 2019 (6 November – 14 December) and austral autumn 2020 (27 February – 1 April), resulting in 180 monitoring stations (three stations per site per season). Guava trees began fruiting during the second data collection period (autumn 2020), however fruits largely remained green (and therefore unpalatable to rodents) for the duration of the observation period. Equipment at each station was deployed for a continuous 29- to 30-day period resulting in 5379 trap nights. A handheld infrared thermal scanner (ThermoGEAR G100EX, Nippon Avionics Co., Ltd) was used to conduct two to three night-time surveys per site per season to independently estimate rodent density in the immediate vicinity of all fixed monitoring stations. Monitoring stations were checked opportunistically during thermal surveys (two to three times during the observation period) or after adverse weather (one to two times during the observation period) for compromised cameras, cards or tunnels. Parks staff refreshed bait stations with diphacinone- or coumatetralyl-based feed blocks on a monthly or bi-monthly basis in the months leading up to and during both monitoring seasons as part of routine rodent control activities.

Results

Rodent presence

Above-ground stations were deployed at heights ranging from 2.1 m to 12.3 m (Fig. 3) and we observed rodents across this vertical range. Rodent presence was uniformly distributed across strata: of the 169 stations (camera, tracking tunnel, and chew cards combined) that detected rodent presence (94% of all stations), 32% were ground-based, 34% were situated in the mid-storey and 34% were situated in the canopy. All passive monitoring methods detected high levels of rodent presence; 73.8% of camera traps, 84.9% of chew cards and 71.4% of tracking tunnels detected at least one rodent during the 29–30-day observation periods. Forest strata had a negligible effect on rodent presence (Table 1, Fig. 4), however, there was evidence of an effect of forest type where we observed a trend of decreased rodent presence in hardwood forest (probability of presence [‘prob’ henceforth] = 0.78; 95% CI = 0.50–0.93), compared to guava (prob = 0.91; 95% CI = 0.72–0.98) and palm forest (prob = 0.88; 95% CI = 0.65–0.97) though this difference was not statistically significant (Table 1). We did not detect any statistically significant difference in rodent presence across forest strata (Table 1), although chew cards tended to record higher proportions of rodent presence, which was consistent across all forest types (Fig. 4). We also recorded anecdotal evidence of arboreal rodent foraging and dwelling at mid-storey and canopy level monitoring stations, including presence of rodent scats, food caches and denning materials (Supplementary Material).

Table 1.Estimated regression parameters, standard errors and 95% credible intervals for a binomial generalised linear mixed-effects model predicting invasive rodent presence across vertical forest strata and forest type.

Term	Estimate	s.e.	z statistic	2.5%	97.5%
(Intercept)	2.10	0.72	2.90	0.68	3.52
StrataMid-storey	0.38	0.29	1.27	−0.20	0.95
StrataCanopy	0.25	0.29	0.86	−0.32	0.82
VegHardwood	−1.00	0.82	−1.22	−2.62	0.61
VegPalm	−0.31	0.84	−0.38	−1.95	1.32

Fig. 4.

Proportion of monitoring devices that detected rodent presence over a 30-day period separated by forest strata and forest type in Norfolk Island National Park. Rodent presence was recorded by camera traps, chew cards, and tracking tunnels, and was collected across three forest types: invasive red cherry guava (Psidium cattleyanum) thickets, native hardwood forests and native palm forests, and three forest strata: ground (dark grey), mid-storey (light grey) and canopy (white). The number of samples retained per treatment after removing failed cameras, chew cards and tracking tunnels is reported below each bar. Error bars indicate ± s.e. of the sample proportion.

Discussion

In a recent review, Taggart et al. (2023) called for a better understanding of how invasive animals use and move through their environment in order to design more targeted and effective conservation baiting strategies; our study directly addresses this by assessing invasive rodent activity in different forest strata. Previous studies have demonstrated that invasive rodents are capable climbers (Innes and Skipworth 1983; Shiels 2010; Foster et al. 2011; King et al. 2011), however this study provides a more comprehensive and species-specific assessment of this behaviour, in a system where long-term ground-based baiting has occurred (~1800 bait stations in the study system). These results provide compelling evidence that rats frequently use all vertical strata across structurally variable forest types, with most of this activity attributable to black rats and, to a lesser extent, Pacific rats. Further, we demonstrated that vertical activity patterns across forest strata are similar despite different physical forest structures and observed differences in rodent density. In systems where the effectiveness of long-term control strategies is declining or where eradication programs have failed, a mixed strategy of baiting across different strata (both on the ground and above) could lead to improved outcomes, particularly where black rats are present.

Black rats were the most common species overall and the dominant arboreal species, whereas most of the ground-level activity was attributable to Pacific rats. This observed dominance of black rats is consistent with previous studies (Harper 2006; Rendall et al. 2014), as is the evidence for vertical niche partitioning between black and Pacific rats (Shiels 2010; Witmer and Shiels 2018). Our findings also mirror those of a study conducted on Dekehtik Island, which found that although Pacific rats occupied the canopy during the day, they spent most of their active nocturnal hours on the ground (Wegmann et al. 2011). As such, the activity observed in the present study needs to be considered in the context of species-specific behaviour and composition. Except in guava sites, black rats only made up between one-fifth and one-third of rat detections at the ground level. Although studies have shown that arboreal rodents do come to ground (e.g. Dowding and Murphy 1994; Key and Woods 1996; Pryde et al. 2005; Shiels 2010; Loveridge et al. 2016), probability theory dictates that species that spend less time on the ground are likely to encounter ground-based devices less often. It then follows that ground-based rodent monitoring in this and similar systems has the potential to under-estimate the extent of black rat activity. As the black rat is considered one of the most harmful invasive rodent species globally (Banks and Hughes 2012), under-estimating their activity has substantial implications for the efficacy of subsequent control efforts.

There are various explanations for the distribution of rodent activity across strata observed in this study. It is possible that the high levels of arboreal activity could be a result of the long-term ground-based control program selecting for such behaviour. This is a plausible scenario considering that the rodent population in the Norfolk Island National Park has experienced extensive ground-based control for three decades. Long-term control programs are already known to impose substantial selective pressures on target species, creating populations that exhibit genetic resistance to toxins and behavioural resistance to bait stations (Allsop et al. 2017). Therefore, multi-decadal ground-based programs could impose an additional selective pressure on ground-based foraging. However, black rats are morphologically adapted to arboreal movement (Alpin et al. 2003; Loveridge et al. 2016; Smith et al. 2016), and arboreal Rattus behaviour was observed in the Norfolk Island National Park prior to any intensive baiting (Robinson 1988). The presence of free-roaming cats as predators may also drive arboreal behaviour, though rodents on Norfolk Island are also subject to predation from an aerial predator, the native owl (Sperring et al. 2021). Predation pressure from above and below could explain the significantly higher presence of black rats observed in the mid-storey compared to the ground and canopy. Variation in food sources across strata may also influence rodent activity, however, known and potential food sources are distributed across all strata: both tree-nesting and ground-nesting birds are present in the National Park, as are ground-dwelling and arboreal invertebrates such as snails, insects and other arthropods (Director of National Parks 2023). Seeds and fruits are also present across all strata, though mass seeding and fruiting events may lead to a higher abundance of resources in the canopy during certain times of the year, which could drive more arboreal activity. Whatever the drivers, arboreal activity is a key aspect of Rattus ecology on Norfolk Island, and exploiting this part of their niche through the incorporation of above-ground control may improve outcomes. This is one of numerous ways in which managers can exploit pest animal behaviour to improve control, thus other avenues should not be overlooked (see Garvey et al. 2020).

Implementation of above-ground control and monitoring will likely increase costs and effort compared to a solely ground-based program, however, an improvement in efficacy may offset those costs. In systems like Norfolk Island that experience high levels of rodent activity despite intensive and ongoing ground-based control, the long-term environmental and economic costs associated without such implementation would be much higher. By deploying control mechanisms above-ground in conjunction with ground-based control, our results suggest that land managers would likely increase encounter rates and subsequently, mortality rates of invasive rodents, particularly black rats (Tobin et al. 1997; Wegmann et al. 2014; Ringler et al. 2021). Raising bait stations off the ground can also mitigate interference from non-target species (Keitt et al. 2015). Preliminary results from small-scale trials in NINP undertaken in 2021 have produced promising results; a pilot field trial of lethal traps (Goodnature A24) deployed across three forest strata showed that canopy traps (6–10 m above-ground) were responsible for nearly 80% of rodent kills, all of which were identified as R. rattus (Nance et al. 2022). A subsequent camera-monitored trial conducted within the NINP found that by deploying rodenticide-baited tunnels ~1.5 m above-ground, bait uptake by rodents increased by 60%, and non-target bait uptake by feral chickens ceased (M. Wilson, unpublished data). Although these trials spanned relatively short sampling periods, results to date are encouraging. To determine if such gains can be maintained over time and across systems, longer-term and larger-scale trials that directly assess the efficacy of above-ground lethal trapping are needed. Additionally, assessing the lowest heights at which bait stations can be deployed while delivering meaningful rodent suppression outcomes will support managers in developing resource-efficient control programs. Finally, understanding the level of rodent control (at or above-ground) required to benefit native species, such as through the implementation of density-impact functions (Norbury et al. 2015), will be critical to the ongoing development of any rodent control program.

Although all activity indices developed in this study demonstrated similar trends for density estimates, high site-level variation suggests that a continuous measure of activity for chew cards and tracking tunnels is unlikely to yield reliable measures of relative density. Conversely, the activity index developed for camera trap detections (rodent-active nights) may be more informative, with the camera trap RAI aligning closely with the more robust thermal survey-based density estimates. Unlike camera traps, activity indices derived from chew cards and tracking tunnels lack temporal resolution, therefore it is not possible to know if high RAI (i.e. heavily chewed cards or heavily tracked tunnels) were produced by one very active rodent or many rodents. On the other hand, the use of camera traps for estimating densities of ground-dwelling mammals has been validated previously using theoretical and empirical evidence (Rowcliffe et al. 2008). Camera trapping to monitor for arboreal mammals is in its infancy (Haysom et al. 2021; Moore et al. 2021), however practical outputs such as that produced by Moore et al. (2021) will undoubtedly lead to improved utility of camera traps in above-ground strata over time. The use of a camera trap index to infer relative density of arboreal invasive rodents is therefore likely to become more precise, and could become a valuable alternative to more effort-intensive survey methods.

When comparing ground-based and above-ground devices, the potential for detectability biases should be considered. For example, the detection zone of a ground-based camera trap will be larger than that of an above-ground camera trap, as above-ground detection zones would be reduced by the empty space that a rodent could not traverse. Conversely, above-ground monitoring may be susceptible to the ‘funnelling’ of rodents near monitoring devices as rodents move to and from the ground along trunks and branches. This has the potential to inflate above-ground activity indices compared to ground-based indices where such funnelling would not occur. This could explain why black rats were more commonly detected in the mid-storey than the canopy. It is worth noting that in the context of rodent control, funnelling arboreal rodents past control devices may actually confer a benefit, as higher encounter rates may lead to higher mortality rates. When monitoring is the primary objective however, programs should consider such differences in detectability when comparing rodent activity across strata.

It is possible that rodents in this system have developed resistance to control (Allsop et al. 2017), though we believe the frequent rotation of rodenticide used in the study system would reduce the likelihood or prevalence of genetic resistance (see Materials and methods: Long-term rodent control). We did not test for this phenomenon in the present study, thus a clearer understanding of the prevalence of resistance, genetic or otherwise, among the rodent population would provide useful additional insight. However, since incorporating tree-based baiting in the NINP rodent control program, practitioners are recording measurable declines in rat activity through independent monitoring (M. Wilson, unpublished data). It is likely therefore that there are multiple causal factors, including arboreal behaviour, that impact the effectiveness of long-term ground-based rodent control programs.

Invasive arboreal rodents are a global threat to native arboreal species. This study highlights the need to understand the dynamics of species-specific rodent activity to design ecologically informed control in systems where long-term programs are experiencing a decline in efficacy, or when planning eradication campaigns for target species that exhibit arboreal behaviour. We provide evidence that neither height off the ground nor vegetation structure limit invasive rat movement above-ground, and suggest that ground-based control alone may not take full advantage of species’ behaviour when targeting the black rat. We argue that a misalignment between arboreal black rat activity and traditional control measures should be considered when assessing the risks to biodiversity, and when reviewing the performance of long-term rodent control programs. These results provide novel insights that can improve the long-term control of invasive rodents, recognising that replication across systems will further our understanding. In systems where black rats persist and the risk for non-target mortality of native species is low, it may be beneficial for practitioners to trial rodent baiting and trapping above-ground. This approach may be particularly beneficial where native species are threatened with imminent extinction and long-term rodent control programs are failing. Understanding the behavioural ecology of invasive species is necessary if we are to successfully minimise and mitigate their environmental and socioeconomic impacts. Research that seeks to optimise the efficacy of above-ground rodent control will be an important step to address the global conservation threat posed by invasive rodents.

Supplementary material

Supplementary material is available online.