Austral Ecology (2003) 28, 48–52
Seedling mortality and damage due to non-trophic animal interactions in a northern New Zealand forest L. N. GILLMAN*1 AND J. OGDEN2 1 Earth and Oceanic Sciences Research Centre, Department of Applied Science, Auckland University of Technology, Private Bag 92006, Auckland, New Zealand (Email:
[email protected]) and 2 School of Geography and Environmental Science, University of Auckland, Auckland, New Zealand
Abstract The importance of non-trophic animal damage (biting and uprooting without consumption) and mortality of canopy tree seedlings were investigated in a warm temperate forest, in northern New Zealand. Two hundred seedlings 10–30 cm in height were monitored at 4–6-week intervals for 2 years. Non-trophic animal damage accounted for more seedling mortality in the first year (37.5% of all mortalities) than any other cause. Of the seedlings damaged in non-trophic animal interactions 73% were bitten off close to the ground and left uneaten and the remainder were uprooted. In the second year all non-trophic animal damage and mortality ceased following the control of rabbits (Oryctolagus cuniculus), suggesting that rabbits were the major cause of this damage. Total annual mortality rates (6–8%) were low. However, measured seedling growth rates indicated an average time for seedlings to grow from 10 to 30 cm of 37 years. Therefore, in the absence of rabbit control, mortality due to non-trophic animal interactions (3% per year) can have an important cumulative effect. Non-trophic animal damage found in the present study before rabbits were culled (5% per year) was similar to that reported for two tropical forests, but much less than that reported for some other tropical and temperate forests. Key words: microdisturbance, physical damage, rabbit, small-scale disturbance.
INTRODUCTION Understanding and managing factors that affect seedling survival and recruitment is crucial for managing natural ecosystems sustainably, and consequently there has been extensive attention given to the primary effects on seedlings due to browsing by introduced mammals in New Zealand (Nugent et al. 2001). However, studies elsewhere show that in addition to the influence on plants due to browsing, animal activity can influence competitive outcomes between different plant species through incidental physical disturbance such as digging (Tilman 1983; Tardiff & Stanford 1998), leaf litter disturbance by birds (Theimer & Gehring 1999) and antler rubbing by deer (Latham 1999). Trampling by animals and nesting seabirds can affect seedling survival and some species can eliminate all ground plants in heavily frequented areas (Gillham 1961; McNaughton 1983; Vanleeuwe & Gautierhion 1998; Maesako 1999). Jackson and Bach (1999) demonstrated that seedlings can suffer high mortality due to an interaction between insect herbivory and incidental damage from vertebrate digging. In addition, several authors have used the results from artificial seedling assays to emphasize the importance of nontrophic animal–plant interactions (Clark & Clark 1989; McCarthy & Facelli 1990; Drake & Pratt 2001). In *Corresponding author. Accepted for publication August 2002.
New Zealand it has been recognized that pigs can destroy seedlings when digging for other food items (Wardle 1984), and physical damage due to litterfall can be important (Gillman & Ogden 2001). On Stephens Island, New Zealand, Mulder and Keall (2001) found that seedling populations were reduced by the burrowing activity of fairy prions (Pachyptila turtur). However, there have been no studies at the community level in mainland New Zealand that measure the impact of incidental physical damage to seedlings due to animals. The present study investigates the importance of non-trophic animal damage on seedlings at the Huapai Scientific Reserve, in northern New Zealand.
Study area
The Huapai Scientific Reserve is a 15-ha mature forest remnant located west of Auckland at latitude 3646S at an altitude of 90 m a.s.l. There is pasture adjacent to the north-eastern boundary of the reserve, whereas the boundary to the north-west is contiguous with privately owned forest, and there is a forest–residential mix on the southern boundaries. The climate is warm temperate and mild all year, with temperatures ranging from a monthly mean summer maximum of 19.0C (February) to a mean winter minimum of 10.4C (July). Annual rainfall averages approximately 1330 mm (Enright 1992). The vegetation is dominated
N O N - T R O P H I C A N I M A L DA M AG E TO S E E D L I N G S
suitable grazing for rabbits was lacking on the other boundaries.
by the conifers, Agathis australis on the ridges and Dacrycarpus dacrydioides in the valleys, growing with mixed angiosperms in the canopy, while the treefern Cyathea dealbata and the palm Rhopalostylis sapida are abundant in the understorey. Gaps containing advanced regeneration generally contain the pioneer Kunzea ericoides in the canopy and treeferns in the subcanopy. Brush-tailed possum (Trichosurus vulpecula) densities were high at Huapai throughout the study (6.8– 7.7 ha–1; J. Weihong, pers. comm.). Rats (Rattus norvegicus or R. rattus) were seen during the day, suggesting that they were abundant, and Yellow Crested Cockatoos (Kakatoe galerita) were usually present. Rabbits (Oryctolagus cuniculus) were often sighted in grassland adjoining the north-eastern boundary of the reserve and occasionally sighted within the forest, but Table 1.
METHODS The effect of animals was measured directly on a monthly basis by monitoring labelled seedlings for animal damage. Four 100-m transects approximately 100–150 m apart were established in December 1995 by following magnetic compass bearings of 30. Two transects were located on ridges and two within valleys. The nearest canopy tree seedling (10–30 cm in height) to every 2 m mark on each transect was labelled for a total of 200 labelled seedlings. The plastic labels lay flat on the ground approximately 75 mm from the seedling and were attached to the stem with green plastic-
Seedling damage and mortality in each of 2 years due to non-trophic animal interactions and due to all other causes † Sample size Year 1 Year 2
Species Corynocarpus laevigatus (Corynocarpaceae) Hedycarya arborea (Monimiaceae) Beilschmiedia tarairi (Lauraceae) Melicytus ramiflorus (Violaceae) Coprosma arborea (Rubiaceae) Knightia excelsa (Proteaceae) Beilschmiedia tawa (Lauraceae) Myrsine australis (Myrsinaceae) Carpodetus serratus (Escalloniaceae) Dacrycarpus dacrydioides (Podocarpaceae) Vitex lucens (Verbenaceae) Phyllocladus trichomanoides (Podocarpaceae) Kunzea ericoides (Myrtaceae) Melicytus macrophyllus (Violaceae) Nestegis lanceolata (Oleaceae) Pittosporum tenuifolium (Pittosporaceae) Podocarpus totara (Podocarpaceae) Agathis australis (Araucariaceae) Total †
49
Non-trophic animal All other causes Year 1 Year 2 Year 1 Year 2 Damage Mortality Damage Mortality Damage Mortality Damage Mortality
86
86
6
3
1
0
9
3
17
5
24
24
1
0
0
0
2
1
6
1
20
19
1
1
0
0
3
1
2
1
14
12
0
0
0
0
2
1
2
1
14
15
0
0
0
0
1
0
4
0
10
9
1
1
0
0
0
0
2
2
9
10
0
0
0
0
1
1
0
0
7
7
0
0
0
0
1
1
1
1
3
2
1
1
0
0
0
0
2
1
3
3
0
0
0
0
0
0
0
0
3
3
0
0
0
0
0
0
0
0
2
2
0
0
0
0
0
0
0
0
1
2
0
0
0
0
1
1
0
0
1
0
0
0
0
0
1
1
0
0
1
1
0
0
0
0
0
0
0
0
1
2
0
0
0
0
0
0
0
0
1
2
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
200
200
10
6
1
0
21
10
36
12
‘All other causes’ includes animal browse, litterfall, pathogens and physiological stress such as desiccation.
50
L. N. GILLMAN AND J. OGDEN
coated wire. These became inconspicuous within 1 or 2 months. Seedlings of 18 species (Table 1) were monitored for ‘damage’ at 4–6-week intervals for two 12-month periods. Seedlings reported as ‘damaged’ included both those killed and those remaining alive that had been flattened against the ground, or completely defoliated, or uprooted. A subset of the damaged seedlings was reported as ‘dead’ if they remained leafless at the end of the 12-month monitoring period and had a dead cambium layer. Four causes of damage and mortality were defined as follows: (i) seedlings that were uprooted, trampled flat against the ground, or bitten off without any portion of the seedling having been eaten were recorded as nontrophic; (ii) seedlings that were completely defoliated with only the stem base remaining were assumed to have been eaten and were recorded as browsed; (iii) seedlings pinned to the ground or 80% covered by litterfall were recorded as litterfall; (iv) seedlings that dropped all leaves due to pathogens or physiological stress such as desiccation were recorded as ‘other’. Seedlings that were partially browsed with some leaves remaining were not recorded as damaged. At the end of the first 12 months of monitoring all seedlings damaged or killed were substituted using the same criteria as that used for the initial selection. The 2 test for non-random association was used to test whether more seedlings of a species were damaged than would be expected on the basis of its abundance and the overall damage rate. Seedling growth rates were calculated based on height measurements taken in December 1995 and again in 1997. The relationship between transect proximity to a population of rabbits on the north-eastern boundary of the reserve and animal damage to seedlings was presented by arranging half-transects in rank order of
increasing distance from this boundary and plotting the total number of seedlings that were non-trophically damaged in each half transect.
RESULTS The overall seedling mortality was low in each year (8%, year 1; 6%, year 2). In the first year animals damaged 5% and killed 3% of seedlings (37.5% of all mortalities) in non-trophic interactions (Table 1). In contrast, 0.5% of seedlings were killed due to browse, 2% due to litterfall, and 2.5% due to all other causes combined. Of the seedlings non-trophically damaged 73% had been bitten off close to the ground and left uneaten and the remainder had been uprooted. In the second year one seedling was found to be nontrophically damaged by an animal in the second month. However, following rabbit control at the end of the second month all non-trophic animal damage ceased. Karaka (Corynocarpus laevigatus) seedlings suffered the majority (62%) of the non-trophic animal damage. However, it was also the most frequent seedling species (0.43), and it was not damaged at a rate significantly greater than expected based on abundance (2 = 2.89; P = 0.1). The number of seedlings damaged by animals declined with increasing distance from the pasture to the north of the reserve (Fig. 1). The pasture was approximately 100 m from the nearest seedling and approximately 600 m from the furthest seedling. The average seedling growth rate (excluding damaged plants) at Huapai was low (5.4 mm year–1). Assuming that this growth rate remains constant, the period required for the average seedling to grow through the 10–30-cm size class would be 37 years. Therefore, if the 1995–1996 non-trophic damage rate continued to occur every year, the projected proportion of a seedling cohort that could be damaged during the time it takes for the cohort to grow through the 10–30-cm size class would be 85%. Similarly, the cumulative non-trophic mortality projection would be 68%.
DISCUSSION Species causing the damage
Fig. 1. Numbers of seedlings non-trophically damaged by animals in each half transect. Half transects arranged in rank order of increasing distance from the grassland where rabbits were regularly observed during the first year of monitoring.
Most of the seedlings damaged by animals at Huapai were non-trophically damaged, and it is possible that the few seedlings assumed to have been browsed were also non-trophically damaged. Some of the seedlings damaged were uprooted, but most were bitten off 1–2 cm from the base with a clean cut and left uneaten. Animal species at Huapai that were likely
N O N - T R O P H I C A N I M A L DA M AG E TO S E E D L I N G S
to be capable of biting off seedlings included rabbits, possums, rats, and Yellow Crested Cockatoo. Mice (Mus musculus) and invertebrates such as weta (Hemideina species), although not sighted, were likely to be present at Huapai and may be capable of biting off seedlings. There is little information on the effects that brushtailed possums have on seedlings and hence forest regeneration (Nugent 1994). Atkinson (1992) observed extensive possum browsing of seedlings and saplings on Kapiti Island, and possums can spend 10–15% of their time on the ground (Cowan & Clout 2000). However, possums prefer full-light canopy leaves to shaded subcanopy leaves (Leutert 1988) and may therefore avoid seedlings unless they are in gaps. Furthermore, species preferred by possums as adult trees can establish as seedlings in the absence of ungulates (Coleman et al. 1980; Allen & Rose 1983; Nugent et al. 2001). Although possums could have been responsible for biting off seedlings without eating them, this behaviour has not been recorded elsewhere. Kiore (Rattus exulans) have been observed biting off seedlings close to the ground and limiting the abundance of nikau and karaka seedlings (Campbell 1978). Norway rats (R. norvegicus) are known to destroy seedlings of several species (Beveridge & Daniel 1965) and to affect seedling populations (Allen et al. 1994). Rabbits can spend most of the day in dense forest and emerge at dusk to feed on grass (Brockie 1992). They are hypothesized to retard the expansion of forest into grassland, but to have little ecological impact in established forest, although they have been seen barking and killing trees (Wardle 1984). Possum densities were high in the study area throughout the monitoring period (J. Weihong, pers. comm.), and no rat control was done within the forest. However, the owners of the pasture controlled rabbits in February 1997 and, following this, all non-trophic seedling damage by animals ceased. Rabbits were often seen in the pasture–forest margin on the north-east boundary to the forest until that time. If rabbits were responsible for the seedling damage, this could account for the gradient of decreasing seedling damage away from the boundary. We suggest therefore that rabbits were probably responsible for most of the non-trophic seedling damage at Huapai. The number of seedlings bitten off without being eaten suggests that this is a common behaviour. It is unclear why animals prune seedlings. However, the behaviour may reduce wetting from vegetation and it may help to maintain their food resource by inhibiting forest encroachment into grassland. Most of the damage occurred to karaka, but it was not damaged at a greater rate than could be expected due to its abundance and the overall damage rate. This suggests that the non-trophic animal damage is not highly selective for a particular species.
51
Importance of non-trophic animal damage at Huapai
It is recognized that the high projected mortality of the seedling cohort (68%) due to non-trophic animal interactions is unlikely to be realized because seedling growth rates differ considerably between individuals. Faster growing seedlings have a reduced risk of mortality and slower growing seedlings may be eliminated by other causes before the non-trophic animal mortality projections are reached. However, the projections illustrate that a non-trophic animal mortality of 3% can have a greater influence on slow growing seedling populations than is initially apparent. Other studies have found greater impacts on seedlings. For example, in an Australian tropical forest Theimer and Gehring (1999) found approximately 10–90% mortality of four tree species of newly germinated seedlings within a 6-month period due to a litterdisturbing bird. At Huapai, non-trophic seedling damage due to animals in the first year (5%) was similar to rates of non-trophic animal damage to artificial seedlings (constructed from plastic straws and wire) found in Papuan (7% year-1) and Hawaiian (4.7% year–1) tropical montane forest (Mack 1998; Drake & Pratt 2001). However, much greater rates have been reported in tropical forest by Clark and Clark (1989) (16.4–25.6% year-1), Scariot (2000) (1–20% year–1) and Roldan and Simonetti (2001) (14–78% year–1), and by McCarthy and Facelli (1990) (39% year–1) in a temperate hardwood forest in New Jersey, USA. Unlike the biting damage at Huapai, most of the damage in these studies (with the exception of that of Roldan & Simonetti 2001) was due to uprooting by animals digging in the immediate vicinity of the artificial seedling, and therefore the differences in damage rates between these communities may be largely due to differences in the abundance of digging animals. However, inferences from damage to artificial seedlings must be treated with caution because over-estimates of animal damage can occur if there is a ‘novelty response’ from animals to the artificial seedlings (Gillman et al. in press). These results demonstrate the potential importance of non-trophic animal damage to seedlings, especially for seedling populations near forest–grassland margins in New Zealand where rabbits are often abundant. The present study justifies further investigation into the influence of these interactions on tree regeneration both in New Zealand and elsewhere.
ACKNOWLEDGEMENTS We thank L. M. Wilson for assistance in the field and S. D. Wright, M. Clout, M. Bull, T. Theimer and one
52
L. N. GILLMAN AND J. OGDEN
anonymous reviewer for helpful comments on the manuscript. Financial assistance from the Auckland University of Technology and University of Auckland is gratefully acknowledged.
REFERENCES Allen R. B., Lee W. G. & Rance B. D. (1994) Regeneration in indigenous forest after eradication of Norway rats, Breaksea Island, New Zealand. NZ J. Bot. 32, 429–39. Allen R. B. & Rose A. B. (1983) Regeneration of Southern rata (Metrosideros umbellata) and kamahi (Weinmannia racemosa) in areas of dieback. Pac. Sci. 37, 433–42. Atkinson I. A. E. (1992) Effects of Possums on the Vegetation of Kapiti Island and Changes Following Possum Eradication. Report no. 92/52. DSIR Land Resources, Wellington. Beveridge A. E. & Daniel M. J. (1965) Observations on a high population of Brown rats (Rattus norvegious Berk 1767) on Mokoia Is., Lake Rotorua. NZ J. Sci. 8, 174–89. Brockie R. (1992) A Living Forest. Bateman, Auckland. Campbell D. J. (1978) The effects of rats on vegetation. In: The Ecology and Control. of Rodents in NZ Nature Reserves. (eds P. R. Dingwall, I. A. E. Atkinson & C. Hay) pp. 99–120. NZ Department of Lands and Survey, Wellington. Clark D. B. & Clark D. A. (1989) The role of physical damage in the seedling mortality regime of a neotropical rain forest. Oikos 55, 225–30. Coleman J. D., Gillman A. & Green W. Q. (1980) Forest patterns and possum densities within podocarp/mixed hardwood forests on Mt. Bryan O’Lynn, Westland, New Zealand. NZ J. Ecol. 3, 66–84. Cowan P. & Clout M. (2000) Possums on the move: Activity patterns, home ranges, and dispersal. In: The Brushtail Possum (ed. T. L. Montague) pp. 24–34. Manaaki Whenua Press, Christchurch. Drake D. R. & Pratt L. W. (2001) Seedling mortality in Hawaiian rain forest: The role of small-scale physical disturbance. Biotropica 33, 319–23. Enright N. J. (1992) Factors affecting reproductive behaviour in the NZ nikau palm, Rhopalostylis sapida Wendl. et Drude. NZ J. Bot. 30, 69–80. Gillham M. E. (1961) Alteration of the breeding habitat by seabirds and seals in Western Australia. J. Ecol. 49, 289–300. Gillman L. N. & Ogden J. (2001) Physical damage by litterfall to canopy tree seedlings in two temperate New Zealand forests. J. Veg. Sci. 12, 671–6. Gillman L. N., Wright S. D. & Ogden J. (2002) Use of artificial seedlings to estimate damage of forest seedlings due to litterfall and animals. J. Veg. Sci. 13, 635–40.
Jackson R. V. & Bach C. E. (1999) Effects of herbivory on growth and survival of seedlings of a rainforest tree, Alphitonia whitei (Rhamnaceae). Aust. J. Ecol. 24, 278–86. Latham J. (1999) Interspecific interactions of ungulates in European forests: An overview. For. Ecol. Manage. 120, 13–21. Leutert A. (1988) Mortality, foliage loss, and possum browsing in southern rata (Metrosideros umbellata) in Westland, New Zealand. NZ J. Bot. 26, 7–20. McCarthy B. C. & Facelli J. M. (1990) Micro-disturbances in oldfields and forests: Implications for woody seedling establishment. Oikos 58, 55–60. Mack A. L. (1998) The potential impact of small-scale physical disturbance on seedlings in a Papuan rainforest. Biotropica 30, 547–52. McNaughton S. J. (1983) Serengeti grassland ecology: The role of composite environmental factors and contingency in community organization. Ecol. Monogr. 53, 291–320. Maesako Y. (1999) Impacts of streaked shearwater (Calonectris leucomelas) on tree seedling regeneration in a warmtemperate evergreen forest on Kanmurijima Island, Japan. Plant Ecol. 145, 183–90. Mulder C. P. H. & Keall S. N. (2001) Burrowing seabirds and reptiles: impacts on seeds, seedlings and soils in an island forest in New Zealand. Oecologia 127, 350–60. Nugent G. (1994) Effects of possums on native flora. In: Possums as Conservation Pests: Proceedings of a Workshop on Possums as Conservation Pests (ed. C. F. O’Donnell) pp. 5–10. Department of Conservation, Wellington. Nugent G., Fraser K. W. & Sweetapple P. J. (2001) Top down or bottom up? Comparing the impacts of introduced arboreal possums and ‘terrestrial’ ruminants on native forests in New Zealand. Biol. Conserv. 99, 65–79. Roldan A. I. & Simonetti J. A. (2001) Plant–mammal interactions in tropical Bolivian forests with different hunting pressures. Conserv. Biol. 15, 617–23. Scariot A. (2000) Seedling mortality by litterfall in Amazonian forest fragments. Biotropica 32, 662–9. Tardiff S. E. & Stanford J. A. (1998) Grizzly bear digging: Effects on subalpine meadow plants in relation to mineral nitrogen availability. Ecology 79, 2219–28. Theimer T. & Gehring C. (1999) Effects of a litter-disturbing bird species on tree seedling germination and survival in an Australian tropical rain forest. J. Trop. Ecol. 15, 737–49. Tilman D. (1983) Plant succession and gopher disturbance along an experimental gradient. Oecologia 60, 285–92. Vanleeuwe H. & Gautierhion A. (1998) Forest elephant paths and movements at the Odzala National Park, Congo: The role of clearings and marantaceae forests. Afr. J. Ecol. 36, 174–82. Wardle J. (1984) The New Zealand Beeches: Ecology Utilisation and Management New Zealand. Forest Service, Christchurch, New Zealand.
