Nursery conditions affect seedling chemistry, morphology and herbivore preferences for Eucalyptus nitens

https://doi.org/10.1016/S0378-1127(02)00315-8Get rights and content

Abstract

We examined intraspecific variation in leaf chemistry and seedling morphology of Eucalyptus nitens grown under three different nursery conditions, and compared these with preferences of two species of marsupial herbivore: red-bellied pademelons, Thylogale billardierii, and common brushtail possums, Trichosurus vulpecula. Chemical and morphological variation with nursery treatment reflected variation in light and nitrogen limitation to seedlings. This variation is discussed in terms of the carbon-nutrient balance hypothesis. The most resource-limited seedlings had the lowest biomass and nitrogen level, but highest specific leaf area, lignin:leaf area ratio, gallotannin:nitrogen ratio and sideroxylonal levels. Both pademelons and possums preferred these resource-limited seedlings least. Possums showed greater discrimination than pademelons for the two other nursery treatments, indicating differences in the two species’ responses to seedling characteristics. Results show that environmental variation in nursery growing conditions has potential in reducing palatability to seedlings, and hence browsing damage, in plantation forestry.

Introduction

Eucalyptus nitens is the major plantation eucalypt species in Tasmania at altitudes above ca. 400 m (Eldridge et al., 1993). It is currently being grown primarily as a pulpwood crop (Wardlaw and de Little, 2000). Browsing damage to newly planted E. nitens seedlings by mammalian herbivores is a widespread problem and a significant economic cost to the forestry industry (Bulinski, 1999, Bulinski and McArthur, 1999, Coleman et al., 1997, Wilkinson and Neilsen, 1995). The most common method currently used for reducing browsing damage is lethal control of herbivore populations by poisoning or shooting. Non-lethal methods for reducing this damage are being sought due to public concern over the killing of native animals. One approach involves reducing palatability of seedlings, in essence increasing resistance to herbivores. Intraspecific variation in resistance of plants to herbivory can have a genetic (Dimock et al., 1976, Marquis, 1990, Mutikainen et al., 2000) and/or an environmental basis, both of which are potentially exploitable.

A genetic basis to variation in resistance to browsing mammals has recently been demonstrated in E. globulus, its hydrids with E. gunnii (O’Reilly-Wapstra et al., 2002, Scott et al., 2002) and in E. nitens (Dungey, 1996). Variation in damage to E. globulus seedlings by swamp wallabies (Wallabia bicolor) and European rabbits (Oryctolagus cuniculus) has been associated with different nursery practices (Marks and Moore, 1998), although the mechanisms behind this variation were unknown. Shade and nutrient levels are two environmental variables that can influence resistance of plants to herbivores through their effects on leaf chemistry (Hartley et al., 1997, Lawler et al., 1997). An explanation for these effects has been formalised in the carbon-nutrient balance (CNB) hypothesis (Bryant et al., 1983, Bryant et al., 1987, Bryant et al., 1991). This hypothesis proposes that when nutrients are limiting or light intensity is high, excess carbon is produced that cannot be used for growth, but can be allocated to carbon-based secondary metabolites such as phenolics and essential oils. Although this hypothesis has been questioned recently (Hamilton et al., 2001), the fact remains that intraspecific differences in plant chemistry are often observed in conjunction with differences in the abiotic environment.

Both genetic and environmental factors affecting herbivory are worth incorporating into a strategy for managing browsing damage in forestry. Browsing often occurs soon after seedlings are planted (Bulinski, 1999). Manipulation of seedling chemistry in the nursery may, therefore, provide one step in reducing this early browsing. In this study, our first aim was to test whether three nursery regimes, which incorporated three different slow-release fertilisers and levels of shading, affected the morphology, primary and secondary leaf chemistry of E. nitens seedlings grown for commercial use. Our second aim was to determine whether red-bellied pademelons, Thylogale billardierii, and common brushtail possums, Trichosurus vulpecula, demonstrated any preferences (differences in intake) for seedlings grown under these three treatments. These are two of the three native herbivore species that cause browsing damage in forestry plantations in Tasmania (Coleman et al., 1997, Statham, 1983). Our third aim was to determine whether any preferences could be explained by observed differences in seedling characteristics, including leaf chemistry.

Section snippets

Animal husbandry

We used captive animals in a paired-treatment feeding trial: six pademelons (three males and three females, mean body weight 7.0 kg, S.D. 1.9) and six brushtail possums (three males and three females, mean body weight 3.5 kg, S.D. 0.5). Pademelons were from a captive population maintained in an animal enclosure at the School of Zoology, University of Tasmania, Hobart. Possums were caught in mascot traps in the bushland surrounding the University of Tasmania. Animals were housed in individual pens

Seedling characteristics

Details of morphological and dry matter characteristics of seedlings grown using the three nursery treatments are shown in Table 1. Treatment B seedlings were significantly taller than the other seedlings (treatment effect F2,76=14.44,P=0.0001), while Treatment A seedlings had significantly less biomass than the other seedlings (treatment effect F2,76=6.96,P=0.0017). Despite these differences, all three treatments produced seedlings with a similar proportion of leaf to stem (73–74% leaf)

Seedling responses to nursery treatments

Nursery treatments induced morphological and chemical differences between seedlings. Relatively low height, biomass and SLA in Treatments A and C compared with B is consistent with light limitation under 50% shadecloth. Fifty percent shadecloth, other factors being equal, has been demonstrated using growth analysis to cause light limitation to E. nitens seedlings (Close, 2001). Further, given the similar light environment, the fertiliser used in Treatment A resulted in nitrogen limitation

Conclusions

Nursery conditions induced different chemical and structural characteristics between seedling treatments. Differences were not extreme, but were sufficient to be detected by the herbivores, as shown by their distinct preferences. These preferences were evident despite the fact that animals did not need to eat any foliage for nutritional or energetic reasons, because they were provided with alternative food. This suggests that whatever seedling characteristics affected their choice, animals did

Acknowledgements

Captive animal feeding trials were performed under Parks and Wildlife Permit #FA99053, and University of Tasmania Animal Ethics Permit #99038. We thank the staff at Forestry Tasmania Nursery for supplying seedlings, Bart Dryden and Julianne O’Reilly for assistance with animal husbandry, Dr. Karen Barry for the use of tetra-galloylglucose standard data and Drs. Bart Eschler and William Foley for the sideroxylonal standard. This research was funded by the CRC-SPF, the Browsing Damage Management

References (53)

  • J Bulinski

    A survey of mammalian browsing damage in Tasmanian eucalypt plantations

    Aust. For.

    (1999)
  • A.L Chung-McCoubrey et al.

    Effects of tannins on digestion and detoxification activity in gray squirrels (Sciurus carolinensis)

    Physiol. Zool.

    (1997)
  • Close, D.C., 2001. Cold-induced photoinhibition, pigment chemistry, growth and nutrition of Eucalyptus nitens and E....
  • D.C Close et al.

    Cold-induced photoinhibition affects establishment of Eucalyptus nitens (Deane and Maiden) Maiden and Eucalyptus globulus Labill

    Trees: Struct. Funct.

    (2000)
  • D.C Close et al.

    Cold-induced photoinhibition and foliar pigment dynamics of Eucalyptus nitens seedlings during establishment

    Aust. J. Plant Physiol.

    (2001)
  • D.C Close et al.

    Temporal variation of tannins (galloylglucoses), flavonols and anthocyanins in leaves of Eucalyptus nitens seedlings: implications for light attenuation and antioxidant activities

    Aust. J. Plant Physiol.

    (2001)
  • Coleman, J.D., Montague, T.L., Eason, C.T., Statham, H.L., 1997. The management of problem browsing and grazing mammals...
  • Cork, S.J., 1992. Polyphenols and the distribution of arboreal, folivorous marsupials in Eucalyptus forests of...
  • B Demmig-Adams et al.

    Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation or excess excitation

    Physiol. Plant.

    (1996)
  • E.J Dimock et al.

    Genetic resistance in Douglas-fir to damage by snowshoe hare and black-tailed deer

    For. Sci.

    (1976)
  • Dungey, H.S., 1996. The susceptibility of hybrid eucalypts to pests. Ph.D. Thesis. University of Tasmania,...
  • Eldridge, K.G., Davidson, J., Harwood, C., van Wyk, G., 1993. Eucalypt Domestication and Breeding. Clarendon Press,...
  • J.R Evans et al.

    Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain

    Plant Cell Environ.

    (2001)
  • Fitzgerald, A.E., 1984. Diet of the possum (Trichosurus vulpecula) in three Tasmanian forest types and its relevance to...
  • W.J Freeland et al.

    Evolutionary consequences of eating: Trichosurus vulpecula (Marsupialia) and the genus Eucalyptus

    J. Chem. Ecol.

    (1975)
  • Goering, H.K., van Soest, P.J., 1970. Forage fiber analyses (apparatus, reagents, procedures, and some applications)....
  • Cited by (20)

    • Tree assisted migration in a browsed landscape: Can we predict susceptibility to herbivores?

      2021, Forest Ecology and Management
      Citation Excerpt :

      Additionally, generalist herbivores might take advantage of new, palatable species or populations and the concentrated resources available in plantations (Averill et al., 2016). Planted seedlings could be especially attractive to mammalian herbivores, because fertilization during nursery cultivation likely increases their nutritional value (McArthur et al., 2003; Reimoser, 2003; Close et al., 2004). In this context, the success of assisted migration plantations in high-browsing pressure systems is uncertain and potentially at risk.

    • The effects of deer herbivory and forest type on tree recruitment vary with plant growth stage

      2013, Forest Ecology and Management
      Citation Excerpt :

      Site conditions, however, namely the nutrient content of soils prevailing under a particular forest type, may also affect the plant nutritional quality (Campo and Dirzo, 2003; Lindroth et al., 2007). Plant fertilization in nurseries, for example, is known to change the leaf chemistry of nursery saplings (McArthur et al., 2003) making these saplings more attractive to feeding herbivores (Close et al., 2004; Hartley and Mitchell, 2005). Although the browse content of deer diets varies among species, deer are generally categorized as intermediate feeders (sensu Hoffman, 1989) as they feed both on herb (grazing) or woody (browsing) plant communities (Horsley et al., 2003).

    • Seasonal dynamics in understorey abundance and carbohydrate concentration in relation to browsing and bark stripping of Tasmanian Pinus radiata plantations

      2013, Forest Ecology and Management
      Citation Excerpt :

      Small perimeter: area, higher degree of canopy closure in surrounding vegetation and greater proportion of stand perimeter adjoining forest are associated with high risk of browsing within eucalypt plantations (Bulinski and McArthur, 2003). Inter- (e.g. surrounding forest and vegetation types, altitude rainfall and soil) and intra- (e.g. planting density, stem diameter, tree branch number, internode length, browser density, patch characteristics such as alternate feed quality and structure) site factors also affect the incidence and severity of bark stripping (McArthur et al., 2003; Pietrzykowski et al., 2003; Jacometti et al., 2007; Miller et al., 2007). However it is not always possible to predict the risk of browsing damage in this way.

    View all citing articles on Scopus
    View full text