Course Hero - We put you ahead of the curve!
You have requested the below document.
- Title: Austral Ecology
- Type: Notes
- School: UC Davis
- Course: EVE 2
- Term: Fall
Ecology Austral (2001) 26, 447 457 Bene ts and risks of biotic exchange between Eucalyptus plantations and native Australian forests SHARON Y. STRAUSS Section of Evolution and Ecology, One Shields Avenue, University of California, Davis, Davis, CA 95616, USA (Email: systrauss@ucdavis.edu) Abstract Australia is unique in having two highly diverse plant genera, Eucalyptus and Acacia, that dominate the vegetation on a continent-wide scale. The recent shift in plantation forestry away from exotic Pinus radiata to native Eucalyptus species has resulted in much more extensive exchange of biota between native forest and plantation ecosystems than exchange in the past with plantations of exotic species. Growing numbers of hectares are being planted to Eucalyptus globulus across Australia, and plantations are providing resources and corridors for native biota. The present paper focuses on both the bene ts and risks of having large-scale forestry plantations of native species that are closely related to dominant native taxa in local forests. At least 85 species of insects have been recorded as pests of Eucalyptus plantations around Australia; the vast majority of these have been insects using the same host species, or closely related taxa, in native forests. Plantations of native species may also bene t from closely related local forests through the presence of: (i) the diverse array of ectomycorrhizal fungi favourable for tree growth; (ii) natural enemies harboured in native habitats; and (iii) recruitment of other important mutualists, such as pollinators. Exchanges work in two directions: plantations are also likely to in uence native forests through the large amount of insect biomass production that occurs in outbreak situations, or through the introduction or facilitation of movements for insects that are not native to all parts of Australia. Finally, older plantations in which trees ower may exchange genes with surrounding forest species, given the high degree of hybridization exhibited by many Eucalyptus species. This is an aspect of exchange for which few data have been recorded. In summary, because of Australia s unique biogeography, plantation forestry using eucalypt species entails exchanges with natural habitats that are unparalleled in scale and diversity in any other part of the world. More exchanges are likely as plantations occupy greater area, and as the time under cultivation increases. Key words: ectomycorrhizal fungi, Eucalyptus, managed ecosystems, Myrtaceae, plantations, plant insect interactions. INTRODUCTION Forestry products grown in Australia are important for the production of sawlog timber, veneer timber and paper pulp within Australia, and are also exported to markets abroad. Pinus radiata, native to the western United States, is still the species with the greatest area under cultivation in Australia (approximately 700 000 ha in 1999; Anonymous 1997); however, there is a growing movement to shift away from planting Pinus radiata and toward planting eucalypt species. In 1995, 19 000 new hectares of hardwood were planted, and this number has increased steadily over successive years to 84 000 new hectares in 2000 (Wood & Allison 2000). The proportion of new acreage planted to hardwood has also increased steadily, and in 2000, 80% of this acreage will be planted to species of Eucalyptus, most importantly, Eucalyptus globulus ssp. globulus (Turner et al. 1999; Wood & Allison 2000). The vision for Australian forestry is to have 3 million Accepted for publication November 2000. hectares in cultivation by 2020 (Anonymous 1997). More than two-thirds of the new hardwood plantings are expected to be in Eucalyptus globulus, and the remainder in other native eucalypt species. Eucalyptus globulus is a variable species with a native distribution limited to south-eastern mainland Australia and Tasmania. Its value as a forestry species lies in its rapid growth rate, high-quality wood bre and its tolerance of a large range of environmental conditions. Ecologically, the difference between planting exotic Pinus radiata and semi-native E. globulus is dramatic. I use the word semi-native because E. globulus is native only to a limited area of Australia; its range throughout Australia has been expanded greatly through forestry plantings. Little of the native fauna or ora can use tree resources and habitats within P. radiata plantations (e.g. Neumann 1978; Friend 1982). Most mammalian arboreal herbivores, insectivores, nectivores and tree-hollow nesters are absent from P. radiata habitat (Friend 1982; Lindenmayer et al. 1999). In addition, the proportion of mammalian species that is non-native is greater in P. radiata 448 S. Y. STRAUSS Table 1. List of insect pest species recorded from Eucalyptus plantations in 6 states in 1991 and 2000 (see last page for key) Tas. 2000 1991 Vic. 2000 1991 SA 2000 1991 NSW 2000 1991 Qld 2000 1991 WA 2000 1991 Year Coleoptera Chrysophtharta agricola Chrysophtharta bimaculata Chrysophtharta cloelia Chrysophtharta variicolis Chrysophtharta spp. Paropsis atomaria Paropsis charybdis Paropsis deboeri Paropsis delittlei Paropsis porosa Paropsis spp. Paropsistern nucea Monolepta australis Cadmus excrementarius Chrysomelid spp. Heteronychus arator Scarab beetles Anoplognathus spp. Anoplognathus chloropygus Anoplognathus hirsutus Anoplognathus porosus Anoplognathus montanus Anoplognathus boisduvali Liperetrus discipennis Lipertus spp. Colpochila spp. Heteronyx spp. Heteronyx elongatus Weevils Gonipterus scutellatus Rhachiodes dentifer Eriothis inaequalis Cerambycids Phorocantha spp. Phorocantha semipunctata Tryphocaria acanthocera Tryphocaria solida Tryphocaria mastersi Lepidoptera Acrocercops spp. Acrocercops calicella Aenetus eximus Aenetus ligniveren Agrotis sp. Antherae eucalypti Apino callisto Doratifera spp. Doratifera casta Doratifera oxleyi Endoxyla sp. Hesthesis cingulata Mnesampela privata (AGM) Ogmograptis spp. Panacela lewinae Perthida sp. Tinea nectarea Uraba lugens Xyleutes boisduvali Zelotypia stacyi 1e 1 1e 1 1 1e 1 X X 1e 1e, 1 m 1e X Xe X 7 5, 4* 1 1e X 1e 4, 5* 1 1 1e 1e 1e 1e 1e 1e 1e m m,e 1e 1e X 1e,m X X m X X 5e, 1 1 3 2 X 1 1 m,e 1e X 1 3e 3e 4e, 3 2 2e m 2 1 X X X X 7e m m X 9 X m m 1 1e X 1e 1e, 1e* 1e 1e 1e 1e 4 5 1e 3, 3* X m X BIOTIC EXCHANGE BETWEEN EUCALYPTUS PLANTATIONS AND FORESTS 449 plantations than in adjoining native eucalypt forests (Friend 1982). There are also substantial differences between pine and eucalypt plantations in their physicochemical impacts on soils and nutrient recycling (e.g. Crockford & Richardson 1998; Turner et al. 1999). Plantations of E. globulus and other eucalypt species are environmentally bene cial in that they provide shelter and food for native animals. More than 85 insect species have been recorded as pests in eucalypt plantations (Table 1), and it is likely that many more native species use these trees at very low densities and are thus undocumented by foresters. In general, eucalypt plantation forestry is likely to be less destructive to natural forest habitats than selective logging, in which large machinery selectively removes older trees or speci c species from natural forests (e.g. jarrah Table 1. (Cont.) Tas. 2000 1991 Vic. 2000 1991 SA 2000 1991 NSW 2000 1991 Qld 2000 1991 WA 2000 1991 Year Hemiptera Amorbus spp. Gelonus tasmanicus Eriococcus coriaceous Cardiaspina spp. Cardiaspina scella Cardiaspina maniformis Creis sp. nr. literata Ctenarytaina eucalypti Glycapsis baileyi Glycapsis nigrocincta Eurymela spp. Eurymela distincta Nysius vinitor Orthoptera Phaulacridium vittatum Grasshoppers Podocanthus wilkinsonii Didymuria violescens Ctenomorphodes tessulatus Hymenoptera Phylacteophaga eucalypti Phylacteophaga froggatti Saw ies Perga af nis Perga dorsalis Perga spp. Pergagrapta polita Isoptera Coptotermes acinaciformis Coptotermes frenchi Glyptotermes spp. Vertebrates Port Lincoln parrots Black Cockatoos Rabbits Wallabies Pademelons Possums m X X 5 6, 6* X X X X X 1 1 X 3 3 1 m 1 1 8 X 2 X X m 4 1 1e Xe 1 3e 3e 1 1 2* 1 1 5 2 m m m m 5 6 2 X 1 m 2 1 1 1 1e 1e 1e 1 1 Numbers represent rankings of pests where 1 = most injurious, 6 = least injurious; X, presence of species (when no ranking available, or when simply noted as present); e, pests of trees < 3 years of age; m, recorded as minor pest. 1991 data: Abbott 1993; Bashford 1993; Neumann 1993; Phillips 1993; Stone 1993; Wylie & Peters 1993. 2000 data: presentations and handouts (i.e. pers.comm.) in Pest Management in Eucalypt Plantations Workshop, Canberra, 2000. Sources: CALM (WA); C. Phillips, ForestrySA; T. Wardlaw, D. de Little, Forestry Tasmania, North Eucalypt Technologies; N. Collett, Centre for Forest Tree Technology (VIC); K. Mullan, Timbercorp Treefarms (VIC, SA, WA); A. Partridge, M. Krygsman, Australian Paper Plantations (VIC); S. Lawson, M. Ivory, Queensland Forestry Research Institute; A. Carnegie, State Forests of NSW. *Australian Paper Plantations data (when two sources for one area were used). 450 S. Y. STRAUSS harvesting). Selective logging has impacts on both forest species composition, as well as on animals that live within the forests (Eyre & Smith 1997; Ochoa-G 1998; Lemckert 1999). Thus, the effort to establish Eucalyptus plantations is ecologically commendable, particularly if the land used for plantations does not result in the loss of native forests, but rather comes from conversion from other kinds of land use (e.g. pasture). Whereas eucalypts as plantation species have their bene ts, they may also pose threats to native eucalypt forests through the exchange of biota and genetic material. In the present paper, I will describe both documented and potential ecological and evolutionary exchanges between native forests and eucalypt plantations in Australia, along with their bene ts and detriments. In keeping with the subject of the symposium, I place an emphasis on plant insect interactions. I. UNIQUE ASPECTS OF EUCALYPTS AND THEIR IMPORTANCE IN AUSTRALIAN ECOSYSTEMS The special biogeography of Australia makes many ecological issues associated with forestry unique to Australia. Most notably, other continents exhibit an array of disparately related tree species as part of the native canopy cover. In contrast, eucalypts dominate (comprising 30 70% of foliage cover) in all regions of Australia, except for the arid interior, where they are still present, but are not as abundant as in other regions (Williams & Brooker 1997). The species diversity of Eucalyptus (or Eucalyptus/Corymbia) is stunning: more than 700 species span the range of Australian habitats, with only four species found exclusively outside Australia (Wardell-Johnson et al. 1997). Phyllodinous Acacia have also radiated to an extraordinary extent in Australia, and although the species diversity of Acacia is almost double that of Eucalyptus, Acacia is not as numerically abundant as eucalypts in most habitats. Australia is unique in having forest communities dominated by two plant genera on a continent-wide scale. The prominence of eucalypts across Australia appears to have taken place primarily in the Miocene (Martin 1994). Radiations in herbivorous (sensu lato) insects have also occurred in response to the radiation in Eucalyptus. Radiations are striking in the coleopterous taxa Chrysomelidae (3000 spp.; of these, several subfamilies feed almost exclusively on Eucalyptus), Lepidoptera: Oecophoridae (>> 2650 spp. of moths, of which 70% feed on Eucalyptus), Hemiptera: Psylloidea (67% of psyllids use eucalypts as hosts), Cicadellidae (> 750 spp. feed on Eucalyptus) and Hymenoptera (140 spp. of saw ies use Eucalyptus and Angophora; 1652 spp. of bees, which are all largely dependent on Myrtaceae) (Majer et al. 1997). The sugary exudates of eucalypt-feeding psyllids, lerps and scales, and carbohydrate-rich manna provide important resources for insects, birds and mammals (Paton 1979; Recher et al. 1985; Steinbauer 1996; Dorr 1999). Hard-capsuled fruits of abundant Eucalyptus species also provide food for specialized seed-feeding parrots in temperate Australia (Woinarski et al. 1997). In summary, the continental scale of dominance by Eucalyptus has provided resources for a large diversity of animal taxa. Planting monocultures of one species of Eucalyptus into diverse communities of other Eucalyptus species can be both bene cial and detrimental to plantations, and to native eucalypt forests that are widespread, numerically dominant and closely taxonomically related to plantation species. Because E. globulus is the species currently projected to be planted across many thousands of hectares in at least four States within Australia over the next 5 years, I have focused my discussion on that species. The arguments I make, however, are generally applicable to any Eucalyptus plantation species. II. EXCHANGES OF BIOTA BETWEEN PLANTATION AND NATIVE FORESTS Because insect herbivores typically use host plants that are taxonomically related and/or chemically similar (e.g. Futuyma et al. 1995; Becerra 1997; Steinbauer & Wanjura 2001), Eucalyptus plantations acquire more pests (both fungal pathogens and insects) from native forests than do exotic plantation species. For example, Pinus radiata plantations in Australia have approximately 40 insect pests, many of them introduced (Neumann 1979). In contrast, at least 85 species have been recorded as pests of Eucalyptus plantations in Australia (Table 1). In general, native forest species used as plantation species have a greater number of pests than do exotic species (Gadgil & Bain 1999). Thus, the physical and chemical similarity of Eucalyptus plantation species to native forest species around Australia will make these trees more prone to use by a range of native ora and fauna. Within Australia, the species composition of native Eucalyptus forests varies over the geographical range through which E. globulus is planted, and pests of E. globulus may differ in both their composition and importance across regions (Table 1). Generic categories such as chrysomelid beetles are ubiquitous; but often, the particular species of beetles that cause the most damage differ from region to region within this category (e.g. Chrysophtharta variicolis and Cadmus excrementarius in WA vs Chrysophtharta bimaculata and Chrysophtharta agricola in the east). Even when the same species are present in different areas, the impact on plantation eucalypts can vary tremendously. For BIOTIC EXCHANGE BETWEEN EUCALYPTUS PLANTATIONS AND FORESTS 451 example, autumn gum moth, Mnesampela privata, causes large losses to young E. globulus trees in the east, but it is not (yet?) a big defoliator of trees in WA, where it is also present (Table 1; A. D. Loch, pers. comm.). Thus, even the same species may represent greater or lesser threats to production depending on the region. As the length of time in plantation and the number of hectares planted to E. globulus increase, the likelihood that additional pests will accrue also increases. Both longer time under cultivation and greater geographical range will expose trees to a large array of insect species (Strong 1974; Strong et al. 1977), and to mutations within herbivore species that could confer the ability to use E. globulus better as a host. The opportunity for selection is high, given that the resource base of E. globulus is ever-growing. In other words, even a very rare mutation that allowed better use of E. globulus would increase rapidly in the insect herbivore population because the tness bene ts of the mutation to the insects carrying it would be great. Thus, one expects the pest species within plantations to be dynamic, changeable and increasingly ef cient at using E. globulus. Table 1 contains pest lists from regions of Australia in 1991 and 2000, based on the rankings presented by industry and State forest representatives at a Eucalyptus pest management workshop that followed the Symposium on Insect Eucalypt Interactions. Table 1 illustrates the diversity of pests found on E. globulus throughout Australia, and also indicates the shifting status of some pests. For example, weevils and chrysomelid beetles have increased in importance in WA over the intervening 9 years between censuses. Unfortunately, the 1991 pest species were not always ranked by injuriousness in all regions, so comparisons for many areas are limited. The diversity of pests and their impacts will make creating a universally applicable management plan for pest problems in Eucalyptus plantations challenging, and will likely result in site- or region-speci c guidelines for control practices. Despite large differences in the insect fauna between regions in Australia, planting large expanses of E. globulus will homogenize the landscape (see subsequent discussion), and will therefore also tend to homogenize pest problems, barring the role of other biotic and abiotic factors in limiting the distribution of herbivores. which the origin is uncertain (Loch & Floyd 2001). These species may have been introduced from eastern Australia (e.g. leafblister saw y; Abbott 1993), dispersed on their own to WA and thrived on their newly planted native hosts, or they may have always been in WA at low and previously undetected levels. As more hectares are planted, the E. globulus estate will become more contiguous, and movements between regions by insects and diseases that can use this species may become more extensive. These exchanges may not just affect plantation pests. Native herbivore species that can use E. globulus (not at pest levels) may have the opportunity to expand their range eastward through plantations, and then have future opportunities to switch onto eucalypts native to other regions of Australia. An insect with this potential is the jarrah leafminer, Perthida glyphoda, which is native to WA but can complete development on E. globulus (Abbott 1993). The rearrangements of the ranges of native Australian insects via planting of E. globulus may also have impacts on native forest insect dynamics. Not only may plantations receive insects from native forests, but plantations may also act as exporters of pests into native forests. Populations of insect species that build up in plantations may spill over into native forests. If these insects can also use forest species, either because they are native to the area, or because they may be preadapted (exapted) to using related forest tree species, herbivore loads and potential competition among herbivore species within native forests could increase. The presence and/or impact of such exchanges will remain unknown unless research programs are established to monitor native communities in forests adjacent to plantations. Such monitoring should include both estimates of damage levels to trees, as well as assessments of the species composition of insect communities. Ideally monitoring should begin several years prior to and continue for years after plantations are planted. III. INSECT OUTBREAKS IN EUCALYPTUS GLOBULUS PLANTATIONS: RELATIONSHIPS WITH NATIVE FORESTS There are a number of plantation pests that exhibit outbreak behaviour in plantations but not in native forests. For example, Mnesampela privata is an endemic species that is often rare and inconspicuous in native forests (McQuillan et al. 1998; Steinbauer et al. 2001), and yet is very damaging to young E. globulus plantations in many areas of Australia (Table 1). A number of reasons may underlie the different impact of insects in native and managed forests. First, plantation monocultures of acceptable host species that are even-aged may present resource availability unequalled in native forests. Autumn gum moths specialize on juvenile foliage of Plantations as highways and exporters of pest species As the area of plantation acreage grows, plantations may act as highways along which insects and diseases can disperse across the country. There are already a number of insect species associated with E. globulus in WA that have originated in eastern Australia, or for 452 S. Y. STRAUSS E. globulus; under natural conditions, large amounts of juvenile foliage might be present only in large-scale recruitment or recovery after res. Large amounts of resource availability can cause increasing concentrations of insects (e.g. Root 1973). Second, how genetic variability is deployed in plantations may decrease attack from enemies. Eucalyptus globulus plantations grown from seed orchard seeds collected from a variety of provenances are expected to be genetically diverse, probably more so than native E. globulus forests, which exhibit ne-scale genetic structure (Skabo et al. 1998, B. M. Potts, pers. comm.). This variability is likely to decrease pest problems that might arise if trees were to be propagated clonally. That reduced variability leads to greater vulnerability to pests and disease and decreased yield is generally accepted (Simmonds 1962; Wolfe 1985; Zhu et al. 2000). An additional and under-utililized source of variation available to plantation managers is the practice of intercropping with different species, or with different provenances that are known to vary in their susceptibility to particular diseases or pests (e.g. Dungey et al. 1997, McCracken & Dawson 1994). Attention to the spatial array of these genotypes may also increase their effectiveness in reducing pest or disease populations. A recent, spectacular example of increased rice yield as a result of intercropping different races of rice in eld trials spanning thousands of hectares has been documented by Zhu et al. (2000). Intercropping in this case was so effective at reducing disease incidence that it obviated fungicide use. Other sources of variability that could be introduced into plantation monocultures might include staggered plantings within the same block. The mixture of different-aged trees will reduce resources present at any one time for pests that specialize on particular life-history stages (e.g. juvenile vs adult foliage in eucalypts). All these levels of heterogeneity may serve to reduce large-scale outbreaks of insect pests and diseases. IV. BENEFITS TO PLANTATIONS FROM NATIVE FORESTS Enemy acquisition from local forests Fig. 1. Number of predators and lepidopteran pest species found along transects running from plantations into native forests. ( ), Predators and parasitoids; ( ), lepidopteran pests. Enemies of pests decrease markedly in plantations relative to native forest while pest densities increase. Note that the lepidopteran counts are for pest species only; non-pest lepidopteran species followed the same patterns. Data from Bragan a et al. (1998). Current commercial forestry practices typically do not focus on promoting the recruitment of natural enemies from adjacent native forest systems for pest control. Yet these species may play an important role in regulating pests in natural systems (McClure 1995; Bragan a et al. 1998). Natural enemies that are found in native forests may be missing or absent in Eucalyptus plantations because they may require nectar resources or alternate prey items absent from traditionally farmed plantation monocultures. In addition, spraying of insecticide to control insect pests also removes insect predators and parasitic control agents. In E. globulus plantations in Brazil, there were clear gradients in both lepidopteran pests and enemy abundance across a transect running from native forest to 600 m within the plantation (Fig. 1). Populations of predators declined steeply along this transect, whereas populations of lepidopteran pest species had the reverse pattern and were most abundant within the plantation (Bragan a et al. 1998). Another important source of insect mortality in native eucalypt forests is predation by birds. Insectivorous birds may consume 55 70% of insect production in these forests (Ford 1985). Destruction of nest site areas or understorey cover can cause marked increases in insect outbreaks (Readshaw 1965). The experimental removal of bell miners, which defend psyllid outbreaks as sources of honeydew, resulted in a large increase in the numbers and diversity of insectivorous birds and in a reduction in the insect outbreaks (Loyn et al. 1983; Loyn 1985; Clarke & Schedvin 1999). Because plantations currently do not provide understorey resources, and because young plantations also do not provide tree-hole nest sites, they may be losing the bene cial effects of control from native vertebrate populations. A better understanding of the factors that limit insect herbivore populations in native forests may guide management practices in Eucalyptus plantations. Factors that promote longevity and movements of natural enemies into plantations from native forests may provide additional tools for the biocontrol of pests by native enemies in an environmentally friendly way. Such practices could include planting understorey strips between rows after E. globulus seedling establishment or adding arti cial sheltering structures between rows, paying closer attention to BIOTIC EXCHANGE BETWEEN EUCALYPTUS PLANTATIONS AND FORESTS 453 management of border vegetation, and increasing the diversity of plantings in terms of vegetation structure. Acquisition of mutualists from native forests Mutualists of Eucalyptus associated with native forests may also promote plantation eucalypts. Ectomycorrhizal (EM) fungi play an important role in Eucalyptus growth and health (May & Simpson 1997). Ectomycorrhizal fungi may dramatically increase the growth of E. globulus seedlings, particularly in phosphorus-poor soils. In Australia, there are an estimated 6500 species of EM fungi (Bougher 1995). A survey of 11 Eucalyptus plantations and two native forest sites in WA revealed 32 species of EM fungi in forests. Of these, 21 species were also found in the plantation sites, and plantations had 13 species not found in either of the two native forest sites surveyed (Lu et al. 1999). Most of the species shared between plantations and native forests were more abundant in older stands of blue gums. Community members that may facilitate the transmission of EM spores from forests to plantations are mammals. Mycorrhizal spores have been found in the scats of at least 12 different species of mammal, and for ve species, both spores and sporocarps were suf ciently abundant in scats that these mammals were considered likely consumers of mycorrhizal sporocarps (Reddell et al. 1997). Slurries made from scats effectively inoculated E. grandis seedlings with mycorrhizae, and resulted in signi cantly greater growth of these seedlings when compared with uninoculated controls. Thus, cultural practices that facilitate the use of plantations by these mammals may have direct bene ts for trees. Such practices may include keeping fragments of native forests interspersed with plantation forests, as several native mammal populations appear to be able to persist in even small fragments surrounded by plantations (Lindenmayer al. et 1999). Exchange with native forests promotes the diversity and dispersal of EM fungal associations that are bene cial to Eucalyptus plantation tree growth in areas with low phosphorus soils, and/or in areas where reduced fertilizer addition is desirable. V. GENETIC EXCHANGES BETWEEN LOCAL FORESTS AND NEARBY PLANTATIONS Another remarkable aspect of the biology of eucalypts is their propensity to hybridize (Grif n et al. 1988; Pryor & Johnson (1971, 1981), and many of the taxonomic problems associated with the clade may stem from incomplete reproductive barriers between species. Typically, hybridization takes place within sections of the genus (Pryor & Johnson 1971, 1981), although there may be some evidence for broader hybridization across sections (Brooker & Hopper 1991). The fact that hybridization is prevalent is demonstrated by the following example: of 528 species examined by Grif n et al. (1988), 289 had hybridized at least once, and the subsection Symphomyrtus, to which E. globulus belongs, has the highest hybridization rate within the genus Eucalyptus. Pollinators of Eucalyptus are generally not speci c, as the open oral morphology is accessible to a variety of pollinator species (reviewed in Potts & Wiltshire 1997). Thus, hybrids may be produced as a result of cross-fertilization between E. globulus or other plantation species and native forest species that ower at the same time. In Victoria, a naturally occurring hybrid population exists between E. globulus and Eucalyptus cypellocarpa (Kirkpatrick et al. 1973), and at least 14 other naturally occurring hybrids of E. globulus have been observed (Grif n et al. 1988; Williams & Potts 1996). In a case directly examining the rates of hybridization between plantation and native species in Tasmania, Barbour et al. (2000) recently documented the hybridization between a small stand of Eucalyptus ovata growing in close proximity to a Eucalyptus nitens trial. In this case, plantation trees had been treated with paclobutrazol to enhance owering. These authors found an average of 4% of the seed crop produced by native E. ovata were F1 hybrids with E. nitens, and production of hybrid seed ranged from 0.1 to a hefty 16% of individual seed crops. As expected, distance from the trial was inversely related to hybrid production by natives. Nearby Eucalyptus viminalis trees were also examined for hybrid seed production and none was found. This result is counterintuitive, as E. viminalis is in the same series as E. nitens, while E. ovata is not. Thus, degree of taxonomic relatedness may not be as important as other traits, such as overlapping owering phenology or similar oral size in predicting the likelihood of hybridization between plantation and native species. There are several implications of hybridization with native forest species. First, any genetic modi cation to plantation species, such as Bt resistance genes inserted into these species, could be transmitted to other species that hybridize with plantation Eucalyptus via their F1 and backcross progeny. If hybrids survive to owering, even if fecundity was relatively low, introgression through backcrossing could further spread the gene into the native population. The subsequent spread would be rapid if the inserted gene offered a strong selective advantage. We already know that insecticide treatments dramatically increase the growth and reproduction of many eucalypts in native forests (Morrow & LaMarche 1978; Lowman & Heatwole 1987; Fox & Morrow 1992). Thus, genetically engineered resistance genes have the potential to confer large tness bene ts to any plant containing them, including hybrids with native forest species. Given the large amount of insect biomass in native forests, and the dependence of many vertebrate taxa on this resource, 454 S. Y. STRAUSS the potential for impacts of gene transfer from plantations to forests on community-wide ecological processes is great. A more long-term effect of hybridization is the possibility that hybrids may act as bridges that enable host shifts of herbivores from one parental species to the other (Floate & Whitham 1993). Hybrids typically have phenotypes that are intermediate between both parental species (Whitham et al. 1999, 1994). In a hybrid zone in Tasmania, Eucalyptus risdonii Eucalyptus amygdalina backcrosses with the parental species suffered high levels of herbivory from a large variety of insect taxa from both parental hosts. Hybrids that combine cues and traits from both hosts might allow adaptation by herbivores to features in the novel parental species. For example, the aforementioned E. globulus E. cypellocarpa hybrids contain speci c terpenoids that are characteristic of E. cypellocarpa in combination with traits unique to E. globulus (Kirkpatrick et al. 1973). Terpenoid composition is correlated with differential attack by Christmas beetle herbivores in several species of Eucalyptus (Edwards et al. 1993). In poplars, a study of hybrid zones and patterns of insect attack suggested that the presence of hybrids with intermediate traits had facilitated shifts onto novel parental hosts (Floate & Whitham 1993). Thus, the long-term persistence of E. globulus genes in a background of locally native Eucalyptus as a result of hybridization may facilitate insect host shifts onto E. globulus in the future, and vice versa. Such a phenomenon might take decades or more to develop and detect. Genetic exchange between eucalypt forests and plantations is a less appreciated but potentially important link between these ecosystems. Native species with small distributions that are compatible with plantation species may be vulnerable to extinction through hybridization. Whereas this type of extinction has not been documented in the context of E. globulus, extinction or invasion through hybridization has been suggested for other native eucalypt species (reviewed in Potts & Wiltshire 1997). To date, we have little knowledge of the degree to which E. globulus will hybridize with other species, especially those in regions where the natural ranges have historically not overlapped. Grif n et al. (1988) and Potts et al. (in press) report that E. globulus has hybridized with 14 different eucalypt species in nature (Table 2). An additional 10 species can hybridize with E. globulus through human-made controlled crosses (Potts et al. in press). Grif n et al. (1988) also state that once natural geographical barriers are removed, hybridization could be quite possible even between geographically distant species. Within Symphomyrtus, there are 47 records of intersectional hybrids, comprising 13 interseries and 35 intraseries hybrids (Grif n et al. 1988). The threat of hybridization will depend on how closely related native forest species are to plantation species (Potts et al. 2000). If native trees belong to different subgenera, such as Jarrah (Eucalyptus marginata, subgenus Monocalyptus), successful hybridization is much less likely and there is reduced risk of genetic pollution (Potts et al. 2000). There are no Western Australian eucalypts that belong to the same taxonomic section (Maidenaria) as E. globulus, and no hybridization has yet been reported between section Maidenaria and the mallee symphyomyrts (sections Dumaria and Bisectaria) in Western Australia (Potts et al. 2000). Still, in regions where E. globulus has not historically occurred and where there has been no selection for isolating mechanisms, eucalypt species with similar traits to E. globulus (overlapping owering phenology, owers with small styles that would match E. globulus pollen tube growth, and general histocompatibility) may be candidates for successful hybridization. Two different approaches could be used to assess the potential for hybridization. First, lab and eld trials using hand pollinations could be used to check for compatibility with native species; these crosses would give an indication of which species, if any, are most likely to hybridize with plantation species in nature. Second, eld monitoring and genetic sampling for the presence of hybrid seedlings along native forest and plantation boundaries are essential to determine the degree to which hybridization occurs spontaneously in nature, and with which species. It should be noted that hybridization with native forests is not so much of an issue for pulp trees, as typically these trees are harvested before they ower. VI. EXCHANGES ON A GLOBAL SCALE: OTHER EUCALYPTUS-GROWING COUNTRIES Millions of hectares of Eucalyptus are planted throughout the world, particularly in Brazil, Chile and India, Table 2. List of naturally occurring hybrids with Eucalyptus globulus Species Eucalyptus Eucalyptus Eucalyptus Eucalyptus Eucalyptus Eucalyptus Eucalyptus Eucalyptus Eucalyptus Eucalyptus Eucalyptus Eucalyptus Eucalyptus Eucalyptus barberi bicostata brookeriana cordata cypellocarpa goniocalyx johnstonii kitsoniana nortonii perriniana pseudoglobulus rubida urnigera viminalis Reference Williams & Potts (1996) Grif n et al. (1988) Williams & Potts (1996) Williams & Potts (1996) Kirkpatrick et al. (1973) Grif n et al. (1988) Grif n et al. (1988) Grif n et al. (1988) Grif n et al. (1988) Williams & Potts (1996) Grif n et al. (1988) Grif n et al. (1988) Grif n et al. (1988) Grif n et al. (1988) BIOTIC EXCHANGE BETWEEN EUCALYPTUS PLANTATIONS AND FORESTS 455 but also in Africa and the Mediterranean regions. In regions where there are related native plants, such as Brazil, plantation trees also acquire local pest species and diseases (Majer & Recher 1999). Any exchange of living material, or even extensive travel between Australian plantations and those in other parts of the world, risks accidental introduction of non-native enemies of eucalypts to Australia. Because native and plantation forests are so closely related in Australia, any introduced threat to Eucalyptus plantations poses a threat to native forests. Although plantation owners often monitor and resort to spraying or other management techniques to control exotics once they are detected within plantations, the monitoring and care of native forests that may also suffer from introductions to plantations is much more at risk of going neglected. Thus, it seems essential that extreme measures be taken to prevent the introduction of pathogens and pests from other regions of the world growing Eucalyptus, and that any screening for introduced agents in plantations also be conducted in nearby native forests. VII. EUCALYPTUS PLANTATIONS OFFER RESOURCES TO NATIVE ECOSYSTEMS The same attributes that make Eucalyptus plantation species vulnerable to local insect pests also make them a potentially valuable resource to native wildlife. Again, little work has been done to determine the degree to which insect populations in plantations, and plantations in general, subsidize vertebrate populations in nearby native forests. We know that insect outbreaks in native forests can strongly in uence the population densities of some bird species (e.g. pied currawongs, bell miners and other insectivores (Readshaw 1965; Clarke & Schedvin 1999). Similar boosts to bird populations may occur when pests outbreak in plantations. In addition, older plantations can offer other limiting resources such as nesting sites in the form of tree hollows for many bird and mammalian taxa. Plantation subsidies might also be enhanced by adding understorey structure to plantations for nesting sites and shelter for vertebrates. Monitoring of vertebrate movements, resource use, diet, reproductive success and population densities near and far from plantations will provide more information about this potential bene cial exchange across natural and managed forests. same species, or closely related taxa, in native forests. More exchanges are likely as plantations occupy greater area, and as time under cultivation increases. Plantations are also likely to in uence native forests through the large amount of insect biomass production that occurs in outbreak situations. These surges in insect populations could affect vertebrate populations as well as herbivore loads and predator populations in adjacent forest tracts. The magnitude of these effects has yet to be investigated. In addition to exporting resources, plantations may also receive bene ts from local forests through the presence of a diverse array of ectomycorrhizal fungi favourable for tree growth, mammalian vectors of mycorrhizal fungi, and through the actions of natural enemies, both vertebrate and invertebrate, that are harboured in native habitats. Finally, plantations in which trees ower may exchange genes with surrounding forest species, given the high rates of hybridization exhibited by many Eucalyptus species. Again, this is an aspect of exchange for which few data have been recorded. In summary, because of Australia s unique biogeography, plantation forestry using eucalypt species entails exchanges with natural habitats that are unparalleled in diversity and scale by those in any other part of the world. Special attention should be paid to these exchanges both in terms of the bene ts they may provide plantation managers, and in terms of their impacts on native Eucalyptus forest communities. In particular, the establishment of more monitoring programs will better elucidate which bene ts and risks are currently most signi cant and, as importantly, will establish much-needed baseline data to examine long-term trends as a result of plantation exchanges with native forests. ACKNOWLEDGEMENTS Many thanks to Martin Steinbauer for organizing this feature, for helpful comments on the manuscript and for logistical support. Additional valued comments on the manuscript were provided by M. Matsuki and an anonymous reviewer. Thanks also to the Cooperative Research Centre for Sustainable Production Forestry (Hobart) and CSIRO Entomology (Canberra) for logistic and technological support, and to M. Steinbauer, M. Matsuki. A. Loch, B. Potts, R. Floyd and J. Majer for stimulating conversations and for bringing these issues more clearly into focus. Note, however, that the author bears sole responsibility for the content of this paper. CONCLUSIONS As reviewed in this article, there are already a lot of exchanges occurring across the boundaries between native forest and plantation ecosystems. At least 85 species of insects have been recorded as pests in Eucalyptus plantations around Australia, and the vast majority of these have been insects using the REFERENCES Abbott I. (1993) Insect pest problems of eucalypt plantations in Australia. 6. Western Australia. Aust. For. 56, 381 4. 456 S. Y. STRAUSS Anonymous (1997) Plantations 2020: A Plan to Achieve the Plantations 2020 Vision. Final Report Prepared by the Centre for International Economics, Canberra, ACT. Barbour R. C., Potts B. M., Vaillancourt R. E., Tibbits W. N. & Wiltshire W. E. (2000) Hybridisation between plantation and native eucalypts in Tasmania. In: Hybrid Breeding and Genetics of Forest Trees: Proceedings of QFRI/CRC-SPF Symposium, 9 14 April, 2000 (eds H. S. Dungey, M. J. Dieters & D. G. Nikles) pp. 395 9. Department of Primary Industries, Brisbane. Bashford, R. (1993) Insect pest problems of eucalypt plantations in Australia. 4. Tasmania. Aust. For. 56, 375 7. Becerra J. X. (1997) Insects on plants: Macroevolutionary chemical trends in host use. Science 276, 253 6. Bougher N. L. (1995) Diversity of ectomycorrhizal fungi associated with eucalypts in Australia. In: Mycorrhizas for Plantation Forestry in Asia (eds M. C. Brundrett, B. Dell, N. Malajczuk & M. Gong) pp. 8 14. Australian Centre for International Agricultural Research, Canberra. Bragan a M. A. L., Zanuncio J. C., Picanco M. & Laranjeiro A. J. (1998) Effects of environmental heterogeneity on Lepidoptera and Hymenoptera populations in Eucalyptus plantations in Brazil. For. Ecol. Manag. 103, 287 92. Brooker M. I. H. & Hopper S. D. (1991) A taxonomic revision of Eucalyptus wandoo, E. redunca and allied species (Eucalyptus series Leucospermae Maiden-Myrtaceae) in Western Australia. Nuytsia 8, 1 189. Clarke M. F. & Schedvin N. (1999) Removal of bell miners Manorina melanophrys from Eucalyptus radiata forest and its effect on avian diversity, psyllids and tree health. Biol. Conserv. 88, 111 20. Crockford R. H. & Richardson D. P. (1998) Litterfall, litter and associated chemistry in a dry sclerophyll eucalypt forest and a pine plantation in south-eastern Australia: 2. Nutrient recycling by litter, throughfall and stem ow. Hydrol. Proc. 12, 385 400. Dorr T. L. (1999) Foraging behaviour and habitat selection of the forty-spotted pardalote, Pardalotus quadragintus. Honours Thesis, University of Tasmania, Hobart. Dungey H. S., Potts B. M., Carnegie A. J. & Ades P. K. (1997) Mycosphaerella leaf disease: Genetic variation in damage to Eucalytpus nitens, Eucalyptus globulus and their F1 hybrid. Can. J. For. Res. 27, 750 9. Edwards P. B., Wanjura W. J. & Brown W. V. (1993) Selective herbivory by Christmas beetles in response to intraspeci c variation in Eucalyptus terpenoids. Oecologia 95, 551 7. Eyre T. J. & Smith A. P. (1997) Floristic and structural habitat preferences of yellow-bellied gliders (Petaurus australis) and selective logging impacts in southeast Queensland, Australia. For. Ecol. Manag. 98, 281 95. Floate K. D. & Whitham T. G. (1993) The hybrid bridge hypothesis: Host shifting via plant hybrid swarms. Am. Nat. 141, 651 62. Ford H. A. (1985) A synthesis of the foraging ecology of and behaviour of birds in eucalypt forests and woodlands. In: Birds of Eucalypt Forests and Woodlands: Ecology, Conservation Management (eds A. Keast, H. F. Recher, H. Ford, & D. Saunders) pp. 249 54. Surrey Beatty, Chipping Norton. Fox L. R. & Morrow P. A. (1992) Eucalypt responses to fertilization and reduced herbivory. Oecologia 89, 214 22. Friend G. (1982) Mammal populations in exotic pine plantations and indigenous eucalypt forests in Gippsland, Victoria. Aust. For. 45, 3 18. Futuyma D. J., Keese M. C. & Funk D. J. (1995) Genetic constraints on macroevolution: The evolution of host af liation in the leaf beetle genus Ophraella. Evolution 49, 797 809. Gadgil P. D. & Bain J. (1999) Vulnerability of planted forests to biotic and abiotic disturbances. New For. 17, 227 38. Grif n A. R., Burgess I. P. & Wolf L. (1988) Patterns of natural and manipulated hybridisation in the genus Eucalyptus L Herit.: A review. Aust. J. Bot. 36, 41 66. Kirkpatrick J. B., Simmons D. & Parsons R. F. (1973) The relationship of some populations involving Eucalyptus cypellocarpa and E. globulus to the problem of phantom hybrids. New Phytol. 72, 867 76. Lemckert F. (1999) Impacts of selective logging on frogs in a forested area of northern New South Wales. Biol. Conserv. 89, 321 8. Lindenmayer D. B., Cunningham R. B. & Pope M. L. (1999) A large-scale experiment to examine the effects of landscape context and habitat fragmentation on mammals. Biol. Conserv. 88, 387 403. Loch A. D & Floyd R. B. (2001) Insect pests of Tasmanian blue gum, Eucalyptus globulus globulus, in southwestern Australia: History, current perspectives and future prospects. Aust. Ecol. 26, 458 466. Lowman M. D. & Heatwole H. (1987) The impact of defoliating insects on the growth of eucalypt saplings. Aust. J. Ecol. 12, 175 82. Loyn R. H. (1985) Birds in fragmented forest in Gippsland, Victoria. In: Birds of Eucalypt Forests and Woodlands: Ecology, Conservation and Management (eds A. Keast, H. F. Recher, H. Ford & D. Saunders) pp. 323 31. Surrey Beatty and Sons, Chipping Norton. Loyn R. H., Runnals R. G. & Forward G. Y. (1983) Territorial Bell Miners and other birds affecting populations of insect prey. Science 221, 1411 12. Lu X., Malajczuk N., Brundrett M. & Dell B. (1999) Fruiting of putative ectomycorrhizal fungi under blue gum (Eucalyptus globulus) plantations of different ages in Western Australia. Mycorrhiza 8, 255 61. Majer J. D. & Recher H. F. (1999) Are eucalypts Brazil s friend or foe? An entomological perspective. Ann. Soc. Entomol. Brasil 28, 185 200. Majer J. D., Recher H. F., Wellington A. B., Woinarski J. C. Z. & Yen A. L. (1997) Invertebrates of eucalypt formations. In: Eucalypt Ecology: Individuals to Ecosystems (eds J. E. Williams & J. C. Z. Woinarski) pp. 278 303. Cambridge University Press, Cambridge. Martin H. A. (1994) Australian Tertiary phytogeography: Evidence from palynology. In: History of the Australian Vegetation: Cretaceous to Recent (ed. R. S. Hill) pp. 104 42. Cambridge University Press, Cambridge. May T. W. & Simpson J. A. (1997) Fungal diversity and ecology in eucalypt systems. In: Eucalypt Ecology: Individuals to Ecosystems (eds J. E. Williams & J. C. Z. Woinarski) pp. 246 77. Cambridge University Press, Cambridge. McClure M. S. (1995) Diapterobates humeralis (Oribatida: Ceratozetidae): An effective control agent of hemlock woolly adelgid (Homoptera: Adelgidae) in Japan. Environ. Entomol. 24, 1207 15. McCracken A. R. & Dawson W. M. (1994) Experience in the use of mixed-clonal stands of Salix as a method of reducing the impact of rust diseases. Nor. J. Agric. Sci. (Suppl.) 18, 101 9. McQuillan P. B., Taylor R. J., Bereton R. N. & Cale P. G. (1998) Seasonal patterns of activity in geometrid moths (Lepidoptera: Geometridae) from a lowland and highland eucalypt forest in Tasmania. Aust. J. Entomol. 37, 228 37. BIOTIC EXCHANGE BETWEEN EUCALYPTUS PLANTATIONS AND FORESTS 457 Morrow P. A. & LaMarche V. C. (1978) Tree ring evidence for chronic insect suppression of productivity in subalpine Eucalytpus. Science 201, 1244 6. Neumann F. G. (1978) Insect populations in eucalypt and pine forests in north-eastern Victoria. Aust. For. Res. 8, 13 24. Neumann F. G. (1979) Insect pest management in Australian radiata pine plantations. Aus. For. 42, 30 8. Neumann F. G. (1993) Insect pest problems of eucalypt plantations in Australia. 3. Victoria. Aus. For. 56, 370 4. Ochoa-G. J. (1998) Preliminary assessment of the effects of logging on the composition and structure of forests in the Venezuelan Guayana Region. Interciencia 23, 197 207, 259. Paton D. C. (1979) The importance of manna, honeydew and lerp in the diets of honeyeaters. Emu 80, 213 26. Phillips C. L. (1993) Insect pest problems of eucalypt plantations in Australia. 5. South Australia. Aust. For. 56, 378 80. Potts B. M., Barbour R. & Hingston A. (in press) The Risk of Genetic Pollution from Farm Forestry Using Eucalypt Species and Hybrids: A Report for Rural Industries Research and Development. Joint Venture Agroforestry Program, Cooperative Research Centre for Sustainable Production Forestry, Hobart. Potts B. M. & Wiltshire R. J. E. (1997) Eucalypt genetics and genecology. In: Eucalypt Ecology: Individuals to Ecosystems (eds J. E. Williams & J. C. Z. Woinarski) pp. 56 91. Cambridge University Press, Cambridge. Pryor L. D. & Johnson L. A. S. (1971) A Classi cation of the Eucalypts. Australian National University Press, Canberra. Pryor L. D. & Johnson L. A. S. (1981) Eucalyptus, the universal Australian. In: Ecological Biogeography of Australia (ed. A. Keast) pp. 501 36. Dr W. Junk, The Hague. Readshaw J. L. (1965) A theory of phasmatid outbreak release. Aust. J. Ecol. 13, 475 90. Recher H. F., Holmes R. T., Schulz M., Shields J. & Kavanagh R. (1985) Foraging patterns of breeding birds in eucalypt forest and woodland southeastern Australia. Aust. J. Ecol. 10, 399 420. Reddell P., Spain A. V. & Hopkins M. (1997) Dispersal of spores of mycorrhizal fungi in scats of native mammals in tropical forests of northeastern Australia. Biotropica 29, 184 92. Root R. B. (1973) Organization of a plant arthropod association in simple and diverse habitats: The fauna of collards (Brassica oleracea). Ecol. Monogr. 43, 95 124. Simmonds N. W. (1962) Variability in crop plants: Its use and conservation. Biol. Rev. 37, 422 65. Skabo S., Vaillancourt R. E. & Potts B. M. (1998) Fine-scale genetic structure of Eucalyptus globulus ssp. globulus forest revealed by RAPDs. Aust. J. Bot. 46, 583 94. Steinbauer M. J. (1996) A note on manna feeding by ants (Hymenoptera: Formicidae). J. Nat. His. 30, 1185 92. Steinbauer M. J., McQuillan P. B. & Young C. J. (2001) Life history and behavioural traits of Mnesampela privata that exacerbate population responses to eucalypt plantations: Comparisons with Australian and outbreak species of forest geometrid from the Northern Hemisphere. Aust. Ecol. 26, 525 534. Steinbauer M. J. & Wanjura W. J. (2001) Christmas beetles (Anthoplognathus spp. Coleoptera: Scarabeidae) mistake peppercorn trees for eucalypts. J. Nat. His,. in press. Stone C. (1993) Insect pest problems of eucalypt plantations in Australia 2. New South Wales. Aust. For. 56, 363 9. Strong D. R. (1974) Rapid asymptotic species accumulation in phytophagous insect communities: The pests of cacao. Science 185, 1064 6. Strong D. R., McCoy E. D. & Rey J. R. (1977) Time and the number of herbivore species: The pests of sugarcane. Ecology 58, 167 75. Turner J., Gessel S. P. & Lambert M. J. (1999) Sustainable management of native and exotic plantations in Australia. New For. 17, 17 32. Wardell-Johnson G. W., Williams J. E., Hill K. D. & Cumming R. (1997) Evolutionary biogeography and contemporary distribution of eucalypts. In: Eucalypt Ecology: Individuals to Ecosystems (eds J. E. Williams & J. C. Z. Woinarski) pp. 92 128. Cambridge University Press, Cambridge. Whitham T. G., Martinsen G. D., Floate K. D., Dungey H. S., Potts B. M. & Keim P. (1999) Plant hybrid zones affect biodiversity: Tools for a genetic-based understanding of community structure. Ecology 80, 416 28. Whitham T. G., Morrow P. A. & Potts B. M. (1994) Plant hybrid zones as centers of biodiversity: The herbivore community of two endemic Tasmanian eucalypts. Oecologia 97, 481 90. Williams J. E. & Brooker M. I. H. (1997) Eucalypts: An introduction. In: Eucalypt Ecology: Individuals to Ecosystems (eds J. E. Williams & J. C. Z. Woinarski) pp. 1 15. Cambridge University Press, Cambridge. Williams K. J. & Potts B. M. (1996) The natural distribution of Eucalyptus species in Tasmania. Tasforests 8, 39 165. Woinarski J. C. Z., Recher H. F. & Majer J. D. (1997) Vertebrates of eucalypt formations. In: Eucalypt Ecology: Individuals to Ecosystems (eds J. E. Williams & J. C. Z. Woinarski) pp. 304 41. Cambridge University Press, Cambridge. Wolfe M. S. (1985) The current status and prospects of multiline cultivars and variety mixtures for disease resistance. Ann. Rev. Phytopath. 23, 251 73. Wood M. & Allison B. (2000) National Forest Inventory (2000). National Plantation Inventory Tabular Report. Bureau of Rural Sciences, Canberra. Wylie F. R. & Peters B. C. (1993) Insect pest problems of eucalypt plantations in Australia. I. Queensland. Aust. For. 56, 358 62. Zhu Y. Y., Chen H. R., Fan J. H. et al. (2000) Genetic diversity and disease control in rice. Nature 406, 718 22.
Find millions of documents here - Study Guides, Homework Solutions, Papers, Exam Answer Keys and more.
Course Hero has millions of course related materials that will enable you to learn better, faster and get an A in all your courses.
Below is a small sample set of documents:
Lehtila and Strauss 1999.pdf
Path: UC Davis >> EVE >> 2 Fall, 2008
Path: UC Davis >> EVE >> 2 Fall, 2008
Path: UC Davis >> EVE >> 2 Fall, 2008
Path: UC Davis >> EVE >> 2 Fall, 2008
Path: UC Davis >> EVE >> 2 Fall, 2008
Path: UC Davis >> EVE >> 2 Fall, 2008
Path: UC Davis >> POSTHARVES >> 2008 Fall, 2008
Path: UC Davis >> HEALTHCENT >> 08 Fall, 2008
Path: UC Davis >> HEALTHCENT >> 08 Fall, 2008
Path: UC Davis >> UCIPM >> 05 Fall, 2005
Path: UC Davis >> CNPRC >> 6 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 204 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 204 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 1 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 2 Fall, 2008
Path: UC Davis >> PROVOST >> 1 Fall, 2008
Path: UC Davis >> RELIGIONS >> 1 Fall, 2008
Path: UC Davis >> RELIGIONS >> 2 Fall, 2008
Path: UC Davis >> RELIGIONS >> 3 Fall, 2008
Path: UC Davis >> RELIGIONS >> 4 Fall, 2008
Path: UC Davis >> IPM >> 091207 Fall, 2008
Path: UC Davis >> VETMED >> 2008 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 98 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 98 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 98 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 99 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 99 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 99 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 99 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 2000 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 2001 Fall, 2008
Path: UC Davis >> PSYCHOLOGY >> 2002 Fall, 2008
Path: UC Davis >> ENTOMOLOGY >> 5 Fall, 2008
Path: UC Davis >> ENTOMOLOGY >> 2 Fall, 2008
Path: UC Davis >> ENTOMOLOGY >> 1 Fall, 2008
Path: UC Davis >> DM >> 07 Fall, 2008
Path: UC Davis >> MATH >> 3 Fall, 2008
Path: UC Davis >> C >> 783 Fall, 2008
Path: UC Davis >> C >> 783 Fall, 2008
Path: UC Davis >> POSTHARVES >> 09 Fall, 2008
Path: UC Davis >> R >> 0601 Fall, 2008
Path: UC Davis >> R >> 2021 Fall, 2008
Path: UC Davis >> R >> 0294 Fall, 2008
Path: UC Davis >> R >> 0604 Fall, 2008
Path: UC Davis >> R >> 0603 Fall, 2008
Path: UC Davis >> R >> 0602 Fall, 2008
Path: UC Davis >> R >> 9903 Fall, 2008
Path: UC Davis >> R >> 0607 Fall, 2008
Path: UC Davis >> R >> 0502 Fall, 2008
Path: UC Davis >> R >> 0403 Fall, 2008
Path: UC Davis >> R >> 0406 Fall, 2008
Path: UC Davis >> R >> 0303 Fall, 2008
Path: UC Davis >> R >> 0407 Fall, 2008
Path: UC Davis >> R >> 0203 Fall, 2008
Path: UC Davis >> R >> 0101 Fall, 2008
Path: UC Davis >> R >> 0102 Fall, 2008
Path: UC Davis >> R >> 0103 Fall, 2008
Path: UC Davis >> R >> 0002 Fall, 2008
Path: UC Davis >> R >> 0001 Fall, 2008
Path: UC Davis >> R >> 0104 Fall, 2008
Path: UC Davis >> R >> 0003 Fall, 2008
Path: UC Davis >> R >> 0004 Fall, 2008
Path: UC Davis >> R >> 9901 Fall, 2008
Path: UC Davis >> R >> 9902 Fall, 2008
Path: UC Davis >> R >> 9801 Fall, 2008
Path: UC Davis >> R >> 9804 Fall, 2008
Path: UC Davis >> R >> 9806 Fall, 2008
Path: UC Davis >> R >> 9802 Fall, 2008
Path: UC Davis >> R >> 9805 Fall, 2008
Path: UC Davis >> R >> 9803 Fall, 2008