Long‐term response of temperate canopy trees to removal of browsing from an invasive arboreal herbivore in New Zealand

Defoliation of forest tree canopies by herbivores and other agents, leading to tree mortality and reduced productivity, threatens the ecological stability of forests globally. This study shows that long‐term control of a mammalian arboreal folivore (brushtail possums; Trichosurus vulpecula Phalangeridae) reduces crown dieback and increases foliage cover in browsing‐damaged canopy trees. We monitored indices of possum density, possum browsing, tree foliage cover and crown dieback for 20 years following initiation of possum control in 1994 that repeatedly reduced possum densities to near zero every 5–6 years and kept the population below 35% of pre‐control levels over the entire period. Observable possum browsing was recorded on 20–49% of individuals of three palatable tree species at the time of first control. Those percentages fell to zero after control and never exceeded 2–10% for individual species over the next 19 years. We recorded significant increases in foliage cover attributable to recovery from defoliation by possums for all three species during the first 10 years. Large increases in foliage cover occurred on individuals that were heavily browsed in 1994 (mean increases: 36–89%), but mean population increases were modest (3–19%) because only 10–19% of trees were initially heavily browsed. Twenty‐year mortality rates were similar for plants with, or without, initial possum browsing, indicating no residual impact of pre‐control browsing on tree mortality. Times for full recovery of crown foliage cover varied from 10 years for the youngest trees and faster growing species to more than 20 years for mature individuals of the slowest growing species.     

Mistletoe (

The condition of 79 plants of the loranthaceous mistletoe Tupeia antarcticain a podocarp-hardwood forest in the central North Island, New Zealand, was monitored over 4 years during a period of increasing possum density, following previous possum control. Mistletoe comprised 1.2% of total possum diet during the three years following possum control. Incidence of possum browse on mistletoe plants increased from 2.6% of plants when the trap-catch index of possum density was < 3%, to 75.9% of plants when trap-catch rates reached 4.6%. Mistletoe foliage cover declined from 49.8% to 15.6% and mean plant size declined by about 55% over the same period. The mistletoe population was dominated by plants with large haustoria, located in heavily shaded locations in the lower crown of their Carpodetus serratus hosts. Most plants established more than 20 years ago, and the current potential for recruitment of new individuals into the population is severely limited by possum browsing and the senescent nature of the mistletoe population. Intensive management of host crowns and possum populations will be necessary to ensure the long-term viability of mistletoe at the study site.     

Phylogenetic relationships ofPseudopanax species (Araliaceae) inferred from parsimony analysis of rDNA sequence data and morphology

Sequence data from internal transcribed spacer (ITS) regions of rDNA and data from morphology, cytology and wood anatomy are used to study phylogenetic relationships inPseudopanax. The molecular and non-molecular data are analysed as independent data sets and in combination using parsimony. Results supported the conclusion that the genusPseudopanax is polyphyletic.Pseudopanax species emerge in two major monophyletic groups. The Anomalus group containsPseudopanax anomalus, P. edgerleyi, andP. simplex; these species share a common ancestor withCheirodendron trigynum and more distantly withPseudopanax gunnii. The second major group consists of two smaller groups: the Arboreus group, includingPseudopanax arboreus, P. colensoi, P. kermadecensis, P. laetus, andP. macintyrei, and the Crassifolius/Discolor group, includingP. chathamicus, P. crassifolius, P. discolor, P. ferox, P. gilliesii, P. lessonii, andP. linearis. Meryta species are close relatives of thePseudopanax Arboreus and Crassifolius/Discolor groups.     

Possum (

To assess the effect of possum browse on plant growth, an index of the amount of foliage on about 50 trees of Fuchsia excorticata and the number of trees that died or were completely defoliated was measured at five sites in South Westland over 5 years. This index was compared to possum density indices taken at each site each year. At one site, possums were reduced from a high density about 6 months before the final measurement. The degree of defoliation of fuchsia was significantly related to the density of possums at each site. Possums defoliate and kill fuchsia within two years once the catch-rate index of their density exceeds about 25%. However, this impact can be halted and quickly reversed by reducing possum density.     

The impact of brodifacoum on non-target wildlife: gaps in knowledge

To assess the effect of possum browse on plant growth, an index of the amount of foliage on about 50 trees of Fuchsia excorticata and the number of trees that died or were completely defoliated was measured at five sites in South Westland over 5 years. This index was compared to possum density indices taken at each site each year. At one site, possums were reduced from a high density about 6 months before the final measurement. The degree of defoliation of fuchsia was significantly related to the density of possums at each site. Possums defoliate and kill fuchsia within two years once the catch-rate index of their density exceeds about 25%. However, this impact can be halted and quickly reversed by reducing possum density.     

The relationship between possum density and browse damage on kamahi in New Zealand forests

To minimize the impacts of introduced pests and to justify and prioritize pest control, managers need to know the relationship between pest density and damage. This relationship can be difficult to quantify because pest impacts can be highly variable. In New Zealand, introduced brushtail possums (Trichosurus vulpecula) browse a wide range of native forest species. However, possum browse is extremely patchy making it difficult to quantify the relationship between density and damage, meaning the benefits of reducing possum densities are poorly understood. We quantified patterns of possum browse on kamahi (Weinmannia racemosa), a common canopy tree species, at 21 forest sites that were repeat‐measured over an 8‐year period in the North Island, New Zealand, during which time possum densities fluctuated widely. We fitted a multilevel statistical model in order to quantify the relationship between possum density and browse damage while simultaneously quantifying how browse varied among trees, sites and years. Higher possum densities were associated with greater browse damage, but browse was also patchily distributed among trees at the same site, and among sites and years for a given possum density. This heterogeneity meant there was no simple density damage relationship, with the relationship differing from tree to tree and among sites and years. Our results show that at most sites reductions in possum density would have little benefit in reducing the probability of heavy browse on kamahi trees, but at a few sites there would be substantial benefits. This approach provides insights into the pattern and potential causes of variability in possum impacts, and a quantitative basis for prioritizing sites for possum control.     

Factors influencing brushtail possum (

Damage by introduced brushtail possums (Trichosurus vulpecula) to Pinus radiata trees was assessed in 41 compartments of a commercial forestry plantation on the Coromandel Peninsula, New Zealand. All the trees assessed were less than 3 years old. Possum damage in the compartments was low (median prevalence 3.3%) but highly variable (range 0?30%). Eight of 37 measured habitat factors differed significantly (P < 0.05) between the sites with damaged and undamaged trees. The best predictor of mean damage was stand age, but this explained only 21% of the variation in damage among compartments. Including both stand age and New Zealand bracken (Pteridium esculentum) cover improved the model significantly and explained 36% of variation in damage. Damage was apparently unrelated to compartment size, distance from the compartment boundary, and possum den-site availability. Surprisingly, the relationship between browse damage and a trap-catch index of possum abundance was weakly negative (r_S = −0.53, P = 0.05). The dense understorey associated with young pine stands tends to increase possum damage to associated P. radiata trees, but the possums in such stands may be less mobile at ground level and thus less easily trapped. Assessment of stand age and understorey characteristics, together with visual inspection for early signs of damage, is likely to be more cost-effective than possum surveys for identifying forest compartments at risk from possum browse.     

Species‐ and site‐specific impacts of an invasive herbivore on tree survival in mixed forests

Invasive herbivores are often managed to limit their negative impact on plant populations, but herbivore density – plant damage relationships are notoriously spatially and temporally variable. Site and species characteristics (both plant and herbivore) must be considered when assessing the potential for herbivore damage, making it difficult to set thresholds for efficient management. Using the invasive brushtail possum Trichosurus vulpecula in New Zealand as a case study, we parameterized a generic model to predict annual probability of browse‐induced mortality of five tree species at 12 sites. We compared predicted and observed tree mortality for each species + site combination to establish herbivore abundance – tree mortality thresholds for each site on a single and combined tree species basis. Model results indicated it is likely that possum browse was the primary cause of all tree mortality at nine of the 12 species‐site combinations, allowing us to estimate site‐specific thresholds below which possum population numbers should be reduced and maintained to keep tree mortality under a predetermined level, for example 0.5% per year. The browse model can be used to set site‐ and species‐specific management action thresholds, and can be adapted easily for other plant or herbivore species. Results for multiple plant or herbivore species at a single site can be combined to create conservative, site‐wide management strategies, and used to: determine which sites will be affected most by changes in herbivore abundance; quantify thresholds for herbivore management; and justify expenditure on herbivore control.     

Inferring changes in foliar mass and area from foliage cover: A mechanistic model

Measuring foliar area or mass directly is destructive, and precludes long‐term, repeated observations of individual trees as they suffer or recover from foliar damage. Instead, foliage cover indices are often used as a proxy for foliar mass. Patterns of fluctuations in foliage cover indices can be used to infer qualitative changes in canopy health. However, foliage cover is not necessarily linearly related to foliar area or mass, and this may confound the detection of significant foliar damage, and comparisons of herbivore browse impacts between individual trees, tree species or sites. I derived a mechanistic model to quantify the relationship between foliar area or mass and foliage cover measured as the proportion of sky occluded by leaves. This one parameter model is close to linear for single‐tiered trees, but increasingly non‐linear for multi‐tiered trees. I compared the non‐linear model to a linear model using foliage cover data from an artificial defoliation experiment on two single‐tiered, sub‐canopy species and from simulated photographic images of single‐ and multi‐tiered canopies. The non‐linear model had lower errors than the linear model, and errors did not increase with foliage density (leaf area per unit area), variation (of leaf sizes within and between canopies) or leaf geometry. The non‐linear model can be easily parameterized from relatively low‐cost observations of foliage cover, independently of empirical measurements of foliar area or mass, and is applicable to a wide range of tree species. It should therefore help managers quantify how changes in foliage cover due to natural fluctuations or foliar damage affect foliar area and mass, and can be used to quantify parameters for models of browse impacts in mixed forest.     

Thresholds in plant–herbivore interactions: predicting plant mortality due to herbivore browse damage

Patterns of herbivore browse at small scales, such as the rate of leaf consumption or plant preferences, drive the impact of herbivores on whole-plant processes, such as growth or survival, and subsequent changes in plant population structure. However, herbivore impacts are often non-linear, highly variable and context-dependent. Understanding the effect of herbivores on plant populations therefore requires a detailed understanding of the relationships that drive small-scale processes, and how these interact to generate dynamics at larger scales. We derive a mathematical model to predict annual rates of browse-induced tree mortality. We model individual plant mortality as a result of rates of foliage production, turnover and herbivore intake, and extend the model to the population scale by allowing for between-tree variation in levels of herbivore browse. The model is configurable for any broadleaved tree species subject to vertebrate or invertebrate browse, and is designed to be parameterized from field data typically collected as part of browse damage assessments. We parameterized and tested the model using data on foliage cover and browse damage recorded on kamahi trees (Weinmannia racemosa) browsed by possums (Trichosurus vulpecula) in New Zealand forests. The model replicated observed patterns of tree mortality at 12 independent validation sites with a wide range of herbivore densities and browse damage. The model reveals two key thresholds; in plant foliar cover, indicating when individual trees may be at high risk from browse-induced mortality, and in herbivore intake, leading to high rates of mortality across the whole population.     

Heterogeneity in vertebrate and invertebrate herbivory and its consequences for New Zealand mistletoes

Vertebrate herbivores generally have greater effects than invertebrates on plants. However, few studies have investigated the effects of both invertebrate and vertebrate herbivores on a single plant species. In New Zealand, nationwide declines in mistletoe populations have often been attributed to possum herbivory, but never to insect herbivory. The main goal of the present study was to document levels of vertebrate and invertebrate herbivory on endemic New Zealand mistletoe plants to suggest whether herbivory is leading to mistletoe decline. In the present study, the annual amount of leaf loss from herbivory by the brushtail possum (Trichosurus vulpecula), insect herbivory and leaf abscission were measured in two populations each of three mistletoe species (Alepis flavida, Peraxilla colensoi, and Peraxilla tetrapetala, Loranthaceae). In two populations of each species from February 1997 to February 1998, abscission accounted for the most leaf loss (range 10–84% of total mean leaf area, mean 33%), whereas insects and possums usually removed small and similar amounts (less than 3%). Possum browse caused large amounts of abscission in only one population (A. flavida at Eglinton). Observed possum browse was more heterogeneous than insect browse among branches within a plant (possum coefficient of variation = 2.63, insect CV = 1.98, P < 0.001), among plants in a population (possum CV = 2.15, insect CV = 0.69, P < 0.001), and between populations (possum CV = 1.36, insect CV = 1.09). Moreover, insects damaged 100% of the study plants but never removed more than 16% of leaf area on a single plant, whereas possums only browsed 32% of the study plants but severely defoliated some plants. Thus, while the mean amount of biomass removed across a population may have important consequences for mistletoe survival, the effect of possums on mistletoe populations may also depend on the heterogeneity of browse among individuals in the population.     

Long-term changes and seasonal patterns in possum (

Possum leaf diet from 1976 to 1989 in the Orongorongo Valley was compared with the diet recorded from four previous years, using faecal analysis. There were large differences in the proportions of species eaten in different seasons and between different years. There was little overall change in the proportion of the main diet tree species, Metrosideros robusta and Weinmannia racemosa, and seasonal increases or declines in one were usually balanced by opposite changes in the other. However, the results of a study of forest composition in the same area showed that living stems of both species declined substantially in abundance, the former mostly before 1978. Melicytus ramiflorus maintained both an important contribution to the diet and its stem density in the forest. The lianes Metrosideros fulgens and Ripogonum scandens both increased their proportion of the diet, but no data were available on their abundance in the study area. At present browse levels, Weinmannia racemosa will become extinct locally, and Metrosideros robusta more rare, especially if drought and higher than average possum densities coincide. Given their large contribution to possum diet, the decline of these species will have a significant effect on possum feeding habits, including increased browsing pressure on Melicytus ramiflorus, Ripogonum scaldens and Metrosideros fulgens. The trend for formerly less palatable tree species to replace those previously important in the diet will continue, with consequent changes in forest species composition.     

Methods for monitoring herbivory and growth of New Zealand mistletoes (Loranthaceae)

This study provides the first quantitative comparison of methods for monitoring herbivory and growth of New Zealand beech mistletoes (Alepis flavida, Peraxilla colensoi and Peraxilla tetrapetala). Four monitoring methods-leaf maps, volume estimates visual estimates of browse and foliage density, and rePeat fixed-point photographs-were used to assess the health of 60 permanently tagged mistletoe plants in four South Island beech forests between February 1997 and February 1998. Leaf maps provided the most detailed information but were extremely labour-intensive so could only be used to monitor a small number of plants. Photographs were much faster to use, and the results corresponded well to leaf map data, but A. flavida could not be photographed because it was frequently hidden by host foliage. Visual scoring methods and volume measurements did not correlate well with leaf maps, probably because leaf loss and growth were not obvious without images of plants from previous seasons. Thus, photographs can provide valuable reference points for future evaluation of plant condition. However, because photos require more time and money than visual scoring and can only be used on a subset of the population, their most practical use is as a supplement to visual scoring.     

Essential oils from the leaves of three New Zealand species of Pseudopanax (Araliaceae)

Essential oils from three of the eleven endemic New Zealand species of Pseudopanax, P. arboreus, P. discolor and P. lessonii, were found to have a fairly uniform composition which was different from that of the oils of Raukaua species that were formerly classified in the Pseudopanax genus. Oils of the three Pseudopanax species all contained significant proportions of viridiflorol and a closely related unidentified hydroazulene alcohol in common. In addition, the oil of P. arboreus contained bicyclogermacrene, linalool and long chain hydrocarbons. The oil of P. discolor contained nerolidol in abundance (36.3%) together with linalool and epi-alpha-muurolol. The oil of P. lessonii contained a complex mixture of sesquiterpene alcohols including epi-alpha-muurolol and a mixture of long chain hydrocarbons. Nerolidol and linalool provided the oil of P. discolor with a pleasant floral aroma, but the yield of oil was very low (0.01%).     

Differential susceptibility to Eucalyptus secondary compounds explains feeding by the common ringtail (Pseudocheirus peregrinus) and common brushtail possum (Trichosurus vulpecula)

The effect of two plant secondary metabolites, tannins and formylated phloroglucinol compounds (FPCs), on the intake of Eucalyptus foliage by common ringtail (Pseudocheirus peregrinus) and common brushtail possums (Trichosurus vulpecula) was studied. We manipulated the amount of tannin that was free to bind with protein by coating foliage with polyethylene glycol 4000 (PEG) and relied on natural intraspecific variation in FPC concentrations. In contrast to ringtail possums, brushtail possums showed a greater tolerance to FPCs and ate more foliage when it was coated with PEG, suggesting that tannins limited their food intake. Brushtails detected the effects of tannins through immediate oral sensations rather than through systemic effects. Ringtail possums appeared highly tolerant of foliar tannins yet susceptible to low concentrations of FPCs. We could not detect any interaction between tannins and FPCs that affected the intake of Eucalyptus foliage by either species of possum. Although ringtail and brushtail possums are widely regarded as specialist and generalist folivores, respectively, their differential susceptibility to co-occurring secondary metabolites suggests greater complexity. Each possum species appears to be a specialist in its own right, which leads to a partitioning of available foliage. Brushtails avoid tannins and ringtails avoid FPCs.     

Spatial variation in impacts of brushtail possums on two Loranthaceous mistletoe species

Browsing by introduced brushtail possums is linked to major declines in mistletoe abundance in New Zealand, yet in some areas mistletoes persist, apparently unaffected by the presence of possums. To determine the cause of this spatial variation in impact I investigated the abundance and condition (crown dieback and extent of possum browse) of two mistletoes (Alepis flavida, Peraxilla tetrapetala) and abundance and diet of possums in two mountain beech (Nothofagus solandri var. cliffortioides) forests in the central-eastern South Island of New Zealand. Mistletoe is common and there are long-established uncontrolled possum populations in both forests. Mistletoes were abundant (216?1359 per hectare) and important in possum diet (41?59% of total diet), but possum density was low (c. 2 per hectare) in both areas. Possum impacts were slight with low browse frequencies and intensities over much of the study sites. However, impacts were significantly greater at a forest margin, where possum abundance was highest, and at a high-altitude site where mistletoe density was lowest. Mistletoe crown dieback was inversely proportional to intensity of possum browsing. These results suggest that the persistence of abundant mistletoe populations at these sites is due to mistletoe productivity matching or exceeding consumption by possums in these forests of low possum-carrying capacity, rather than low possum preference for the local mistletoe populations.     

Native plant/herbivore interactions as determinants of the ecological and evolutionary effects of invasive mammalian herbivores: the case of the common brushtail possum

In their native range, mammalian herbivores exist in a suite of direct and indirect ecological and evolutionary relationships with plant populations and communities. Outside their native range these herbivores become embedded in a multitude of new ecological and evolutionary interactions with native plant species in the new range. Sound knowledge of the plant/herbivore interactions in the herbivores’ native range provides an ideal framework to better understand their effects in the introduced range. The example of the common brushtail possum (Trichosurus vulpecula) and its introduction to New Zealand from Australia provides an excellent case study. In Australia, the common brushtail possum is a widespread generalist herbivore and it is thought that this generalist lifestyle has equipped the species well for successful colonisation of New Zealand. In Australia the brushtail possum has co-existed with highly chemically defended foliage since the Oligocene and recent papers have supported the role of possums as agents of selection on eucalypt defences. While the chemical profile of New Zealand foliage is comparatively poorly understood, possums do show clear selectivity between and within populations and some of these interactions may be mediated by the animals ability to ‘cope’ with PSMs, coupled with maintaining its generalist diet. While possums have had less time to effect evolutionary change in New Zealand species, their impacts on plant fitness have been well documented. However, further knowledge on variation and heritability of foliage traits driving possum preferences is needed to elucidate the ecological and evolutionary plant/possum interactions in the invasive range.     

马鹿和狍饲料植物的营养质量

本项研究测定了１４种木本植物的枝和叶以及苔草、非禾本和莎草科草、蕨、榆树皮的粗蛋白（ＣＰ）、中性洗涤纤维（ＮＤＦ）、酸性洗涤纤维（ＡＤＦ）、钙（Ｃａ）、磷（Ｐ）、钠（Ｎａ）、钾（Ｋ）等营养成分和体外干物质消化率（ＩＶＤＤＭ）。结果表明,各类饲料植物中营养成分的含量存在显著的差异（Ｐ＜０．０５）。木本植物叶中ＣＰ的含量在全年呈最高趋势,枝条中ＣＰ含量为最低;木本植物枝条中ＮＤＦ和ＡＤＦ的四季含量最高,非禾本和莎草科草中的ＮＤＦ和ＡＤＦ的含量最低。Ｃａ在木本植物的枝条和非禾本及莎草科草中的四季含量最高,在苦草中的含量最低;Ｋ在非禾本和莎草科草以及蕨类中的四季含量最高,在木本植物枝条中的含量最低;Ｐ和Ｎａ在各类饲料植物中的四季含量变化很大。木本植物枝条中ＣＰ含量的季变化很小,木本植物的叶、苔草、非禾本和莎草科草及蕨中ＣＰ的含量从春到秋逐渐减少。各类饲料植物中ＮＤＦ和ＡＤＦ在春季的含量明显地低于其它季节。Ｋ在各类饲料植物中的含量由春季到冬季呈下降趋势,而Ｃａ、Ｐ、Ｎａ在不同饲料植物中的含量表现出不同的季节变化。马鹿和狍对饲料植物干物质的体外消化率与饲料植物中ＣＰ的含量存在显著的正相关,与ＡＤＦ存在显著的负相关。     

Predicting Summer Site Occupancy for an Invasive Species,the Common Brushtail Possum (Trichosurus vulpecula), in an Urban Environment

Invasive species are often favoured in fragmented, highly-modified, human-dominated landscapes such as urban areas. Because successful invasive urban adapters can occupy habitat that is quite different from that in their original range, effective management programmes for invasive species in urban areas require an understanding of distribution, habitat and resource requirements at a local scale that is tailored to the fine-scale heterogeneity typical of urban landscapes. The common brushtail possum (Trichosurus vulpecula) is one of New Zealand’s most destructive invasive pest species. As brushtail possums traditionally occupy forest habitat, control in New Zealand has focussed on rural and forest habitats, and forest fragments in cities. However, as successful urban adapters, possums may be occupying a wider range of habitats. Here we use site occupancy methods to determine the distribution of brushtail possums across five distinguishable urban habitat types during summer, which is when possums have the greatest impacts on breeding birds. We collected data on possum presence/absence and habitat characteristics, including possible sources of supplementary food (fruit trees, vegetable gardens, compost heaps), and the availability of forest fragments from 150 survey locations. Predictive distribution models constructed using the programme PRESENCE revealed that while occupancy rates were highest in forest fragments, possums were still present across a large proportion of residential habitat with occupancy decreasing as housing density increased and green cover decreased. The presence of supplementary food sources was important in predicting possum occupancy, which may reflect the high nutritional value of these food types. Additionally, occupancy decreased as the proportion of forest fragment decreased, indicating the importance of forest fragments in determining possum distribution. Control operations to protect native birds from possum predation in cities should include well-vegetated residential areas; these modified habitats not only support possums but provide a source for reinvasion of fragments.     

Host specificity in parasitic mistletoes (Loranthaceae) in New Zealand

1. We quantify the degree of host specificity for the five extant New Zealand loranthaceous mistletoes ( Alepis flavida, Ileostylus micranthus, Peraxilla colensoi, Peraxilla tetrapetala and Tupeia antarctica ).
2. Host specificity is highest for A. flavida, P. colensoi and P. tetrapetala which primarily parasitize species of Nothofagus , and lowest for T. antarctica and especially I. micranthus which parasitize a wide range of host species.
3. These patterns of host specificity support the suggestion that relative host abundance is a key factor determining the degree of host specialization in mistletoes (resource fragmentation hypothesis). While evolutionary history may be important in the specificity of the mistletoe–host relationship in some situations, our data suggest that for New Zealand mistletoes evolutionary history simply reflects the temporal component of relative host abundance.
4. We conclude that it is the stability of host availability through time and space which is the dominant factor determining host specificity patterns.