Jay R. Malcolm

Quantifying the biodiversity value of tropical primary, secondary, and plantation forests

Biodiversity loss from deforestation may be partly offset by the expansion of secondary forests and plantation forestry in the tropics. However, our current knowledge of the value of these habitats for biodiversity conservation is limited to very few taxa, and many studies are severely confounded by methodological shortcomings. We examined the conservation value of tropical primary, secondary, and plantation forests for 15 taxonomic groups using a robust and replicated sample design that minimized edge effects. Different taxa varied markedly in their response to patterns of land use in terms of species richness and the percentage of species restricted to primary forest (varying from 5% to 57%), yet almost all between-forest comparisons showed marked differences in community structure and composition. Cross-taxon congruence in response patterns was very weak when evaluated using abundance or species richness data, but much stronger when using metrics based upon community similarity. Our results show that, whereas the biodiversity indicator group concept may hold some validity for several taxa that are frequently sampled (such as birds and fruit-feeding butterflies), it fails for those exhibiting highly idiosyncratic responses to tropical land-use change (including highly vagile species groups such as bats and orchid bees), highlighting the problems associated with quantifying the biodiversity value of anthropogenic habitats. Finally, although we show that areas of native regeneration and exotic tree plantations can provide complementary conservation services, we also provide clear empirical evidence demonstrating the irreplaceable value of primary forests.

MAMMALS OF THE RIO JURUÁ AND THE EVOLUTIONARY AND ECOLOGICAL DIVERSIFICATION OF AMAZONIA

Abstract We describe the nonvolant mammal fauna of the Rio Juruá of the western Amazon of Brazil, based on collections made during a year-long survey of the river. We, along with our colleagues Drs. Claude Gascon and Carlos Peres, designed the field project to examine the effects of the river on the differentiation among terrestrial vertebrates (mammals, birds, and amphibians and reptiles) at both the community and population levels. This monograph examines only the patterns of geographic variation and community structure of the small-bodied mammals. Species inventories were made at 16 primary trapping localities divided into eight pairs of cross-river sites, with two pairs in each of four regions from near the mouth to the headwaters of the Rio Juruá. A total of 81 species of nonvolant mammals were obtained, including nine new to science. Four of these are described herein; the others have been described elsewhere. We used a standardized trapping protocol to assess community structure at each of the 16 localities that included terrestrial and canopy trap stations in floodplain (várzea) and upland (terra firme) forest formations. Supplemental trapping was done in secondary habitats at all sites. We describe these sites, the trap effort expended, and the placement of trap stations relative to local habitats. We also describe each species of marsupial, sciurid rodent, murid rodent, and echimyid rodent encountered; comment on their systematics; and summarize aspects of habitat use, life history, geographic distribution, and geographic differentiation based on morphological and molecular traits. We examine patterns of differentiation in the mitochondrial cytochrome-b gene for samples of 41 of the 45 species of marsupials and rodents obtained within the Rio Juruá Basin, and discuss these patterns from the perspective of the entire Amazon and, in some cases, the Mata Atlântica of coastal Brazil. We also examine patterns of community organization within the Rio Juruá basin and throughout Amazonia, drawing attention to the geographic distribution of what appear to be major faunal units that are independent of habitat differences. Finally, we use principles of phylogeography to analyze patterns of geographic differentiation among the nonvolant mammals with regard to the Riverine Barrier Hypothesis. We show that, while there are few examples of taxa for which the Rio Juruá is apparently a barrier, most taxa either are largely undifferentiated throughout the basin or are sharply divided into reciprocally monophyletic mtDNA haplotype clades separable into upriver and downriver units. We argue that the concordance in the geographic placement of clade boundaries suggests a common history; moreover, both the age of these clades and their geographic position in relation to underlying geological features suggest that landform evolution has been an important, but underappreciated component of diversification within western Amazonia.

Edge Effects in Central Amazonian Forest Fragments

Current descriptive models of edge effects describe little more than the relationship between perimeter and area. A more realistic model, one that incorporates the additive nature of edge effects, is presented and tested. The total edge effect at a location within a patch is modelled as the sum of edge effects at points along the edges of the patch, weighted by the distances from the edge points to the location. At four sites in the central Amazon °80 km north of Manaus, Brazil, I measured vertical stratification of foliage in three primary forest habitats: (1) continuous forest close to linear edges, (2) 10—ha forest fragments, and (3) 1—ha forest fragments. Foliage thickness (foliage density along a vertical line) was scored in six height intervals (0—2, 2—5, 5—10, 10—20, 20—30, and 30—40 m). With decreasing distance from a linear edge, understory (0—5 m) foliage thickness increased and overstory (10—30 m) foliage thickness decreased, and the relationship between foliage thickness and distance to the edge agreed with that predicted by the model. Using parameter estimates obtained from the best “fit” of the model to these data from linear edges, understory and overstory thickness in 1— and 10—ha fragments was predicted. Foliage thickness varied extensively among fragments, but agreed quite closely with that predicted by the model, and the additive model performed better than a curvilinear non—additive one.

GENE GENEALOGY AND DIFFERENTIATION AMONG ARBOREAL SPINY RATS (RODENTIA: ECHIMYIDAE) OF THE AMAZON BASIN: A TEST OF THE RIVERINE BARRIER HYPOTHESIS

Sequence variation in the mitochondrial cytochrome b gene was examined in the arboreal spiny rat, Mesomys hispidus, collected at 15 sites along the Rio Juruá in western Amazonia, Brazil, to determine the importance of riverine barriers in the diversification of this taxon. Twenty individual haplotypes were uncovered, most of which were unique to single localities but some of which were shared among adjacent sites either along or across the river. Genealogical analyses suggest that gene flow is limited and, in combination with the unique distribution of most haplotypes, suggest that populations of this species are strongly substructured along the river. Thus, most sharing of haplotypes between adjacent localities is probably caused by historical association rather than to ongoing gene flow. Two haplotype clades were uncovered, but these correspond to headwaters versus mouth areas, not to opposite sides of the river, as would be expected by the Riverine Barrier Hypothesis. Moreover, haplotype sharing across the river was greater at its mouth than in the headwaters, a pattern opposite that expected if the river were a substantive barrier. Broader scale phylogeographic patterns of this species show that both clades have relationships to areas well outside the Rio Juruá basin. This suggests that the basin represents a relatively recent point of invasion between two more broadly distributed and differentiated geographic units of the species.

Conservation and development alliances with the Kayapó of south-eastern Amazonia, a tropical forest indigenous people

Summary Legally recognized Indian reserves of Brazilian Amazonia span over 100 million ha of largely intact forest and are potentially valuable for biodiversity conservation. An important example is provided by the Kayapo territories which span more than 13 million ha in Para and Mato Grosso, Brazil, and protect a unique and vulnerable Amazonian forest type that is poorly represented in existing nature reserves. The Kayapo of southern Para have stopped invasion of their lands by the most perverse threats to Amazonian forests, but they have become involved extensively in the sale of illegal logging concessions for the high-value timber species mahogany (Swietenia macrophylla). In 1992, the non-governmental organization Conservation International do Brasil (CI-Brasil) began a conservation and development project with the Kayapo community of A’Ukre with the objective of providing economic alternatives to logging and protecting a population of mahogany trees. This paper demonstrates the conservation benefits that can be achieved by supporting sustainable development of indigenous peoples in the Amazon. Specifically, we: (1) evaluate the ecological importance of the Kayapo reserves from a biodiversity conservation viewpoint, (2) evaluate the conservation success of the CI-Brasil project and test whether the implementation of the conservation alliance between A’Ukre and CI-Brasil satisfies common pool resource principles, and (3) propose a model for expanding the small-scale conservation results achieved by the CI-Brasil project to all Kayapo territories. Several mammals (Tayassu pecari, Pteronura brasiliensis, Priodontes maximus, Panthera onca) and at least one bird species (Anodorhynchus hyacinthinus) listed as endangered were regularly encountered within 15 km of A’Ukre. Taxa encountered at relatively high densities in the project area included large cracids, lowland tapir, and white-lipped peccary, indicating an ecosystem that is not severely impacted by hunting. Harvest offtakes of mahogany averaged 0.44 stems ha -1 within groves and 0.13 stems ha -1 at the landscape level. We estimate that 85% of the fruiting population of Swietenia macrophylla has been removed in harvested Kayapo territories in Para. We found Kayapo social organization in A’Ukre to meet criteria of successful common pool resource institutions. The CI-Brasil project resulted in protection of an intact mahogany population in 8000 ha of forest maintained by the community for ecological research purposes and mahogany preservation. Our analysis attributes the success of the conservation alliance with A’Ukre to: (1) direct benefits accruing to all members of the community, (2) fulfilment of criteria for development of common pool resource institutions, and (3) long-term commitment of an external agency. We propose that by implementing these three elements elsewhere, the modest conservation result achieved at A’Ukre could be expanded to include the entire Kayapo nation and thereby contribute to conservation of more than 13 000 000 ha of forest and cerrado in the south-eastern Amazon.

AMAZONIAN SMALL MAMMAL ABUNDANCES IN RELATION TO HABITAT STRUCTURE AND RESOURCE ABUNDANCE

Abstract Previous studies in tropical rain forests suggest that most small mammal species reach their highest densities in disturbed habitats; however, only a few sites have been examined. Consequently, habitat and resource use for many species is poorly understood. This is especially true in the Amazon Basin, where no studies of microhabitat associations of small mammals have been undertaken. We studied relationships with habitat variables and resource abundances for 5 species of marsupials and 9 species of rodents at a site in southeastern Amazonia. Small mammals were sampled with traps placed both on the ground and in the understory. Eight habitat variables were measured to quantify habitat structure. Measures of insect biomass were collected by the use of sticky traps, and fruit abundance was quantified. Patterns of habitat use were examined using logistic regression, multiple regression, and ordinations. Many species showed increased abundances with habitat features indicative of edge-affected or disturbed habitats, showing negative relationships with understory openness, understory woody-stem density, tree density, and tree size; and positive relationships with number of vines per tree, mean log size, number of logs, and volume of downed wood. We obtained support for the hypothesis that the cause of this pattern is increased resource abundances in these areas, because both insect biomass and number of fruiting trees showed similar relationships. However, for many species, measures of resource abundance were not important once habitat features were entered into the models, indicating that the relationship to resources is an indirect one.

Hierarchical genetic structure and gene flow in three sympatric species of Amazonian rodents

The population genetic structure of three species of Amazonian rodents (Oligoryzomys microtis, Oryzomys capito, and Mesomys hispidus) is examined for mtDNA sequence haplotypes of the cytochrome b gene by hierarchical analysis of variance and gene flow estimates based on fixation indices (NST) and coalescence methods. Species samples are from the same localities along 1000 km of the Rio Jurua in western Amazonian Brazil, but each species differs in important life history traits such as population size and reproductive rate. Average haplotype differentiation, hierarchical haplotype apportionment, and gene flow estimates are contrasted in discussing the current and past population structure. Two species exhibit isolation by distance patterns wherein gene flow is largely limited to geographically adjacent localities. Mesomys exhibits this pattern throughout its range along the river. More than 75% of haplotype variation is apportioned among localities and regions, and estimates of Nm for pair‐wise comparisons are nearly always less than 1. Oligoryzomys shows weak isolation by distance, but only over the largest geographical distances. Nm values for this species are nearly always above 1 and most (about 80%) of haplotype variation is contained within local populations. In contrast, Oryzomys exhibits no genetic structure throughout its entire distribution; Nm values average 17 and nearly 90% of the total haplotype variance is contained within local populations. Although gene flow estimates are high, the pattern of Nm as a function of geographical distance suggests that this species experienced a more recent invasion of the region and is still in genetic disequilibrium under its current demographic conditions.

Nest-Tree Use by Northern and Southern Flying Squirrels in Central Ontario

Abstract Little is known about nest use by flying squirrels (Glaucomys) in partially harvested forests, especially for northerly populations where cavity use is prevalent. We used radiotelemetry to examine nest use by 24 southern flying squirrels (G. volans) in 2003 in logged and unlogged hardwood forests, and by 18 northern flying squirrels (G. sabrinus) in 2004 in conifer forests, in Algonquin Provincial Park, Ontario, Canada. Of 76 nest trees used by G. volans, 71% were in declining trees and 22% were in snags. Sixty tree nests used by G. sabrinus included 28% snags, 46% declining trees, and 25% healthy trees, although nearly one-half of nests of G. sabrinus that were used on more than 3 occasions were in snags. G. volans used larger-diameter trees and American beech (Fagus grandifolia) more often than expected by chance, whereas G. sabrinus used trembling aspen (Populus tremuloides), white birch (Betula papyrifera), and yellow birch (B. alleghaniensis) more than expected by chance. Both species used a high proportion of cavity nests, few external nests, and trees that were decayed or diseased. We found indications that nest supply was limited in recently harvested sites, where there were fewer cavity trees and snags; however, G. volans may compensate by using abandoned yellow-bellied sapsucker nests and by nesting in aggregations. Hardwood snags and decaying trees appear to provide crucial nesting habitats for both squirrel species, particularly for females.

Sciurid habitat relationships in forests managed under selection and shelterwood silviculture in Ontario

Abstract Although partial forest harvesting is practiced over large areas, managers know little about its impacts on sciurid rodents, particularly on northern (Glaucomys sabrinus) and southern flying squirrels (G. volans) in the northeastern United States and Canada. We examined habitat relationships of sciurid rodents (northern flying squirrels, southern flying squirrels, red squirrels [Tamiasciurus hudsonicus], and eastern chipmunks [Tamias striatus]) at 2 spatial scales in managed and unmanaged coniferous and hardwood forests of Algonquin Provincial Park, Ontario, Canada. We live-trapped rodents in 26 northern hardwood stands and in 16 white pine (Pinus strobus) stands from 2002 to 2004. Northern flying squirrel and red squirrel densities were significantly lower in recently harvested (3–10 yr since harvest) shelterwood stands than in unmanaged stands. In contrast, southern flying squirrel densities were higher in selection-harvested stands than in old-forest areas. The densities of northern flying squirrels and red squirrels had a strong relationship with the density of large spruce (Picea sp.) and hardwood trees and snags in conifer sites. Southern flying squirrel numbers had a positive association with the density of mast trees at the landscape level but not at the stand level in hardwood forests. Eastern chipmunk density had a positive correlation with the volume of old downed woody debris and the stems per hectare of declining trees. We recommend forest managers retain more large spruce and hardwood trees to mitigate the impacts of shelterwood harvesting on northern flying squirrels and red squirrels, and that they maintain high mast availability at the landscape level to ensure the persistence of southern flying squirrels.

A Model of Conductive Heat Flow in Forest Edges and Fragmented Landscapes

Although the creation of edges during forest fragmentation can have important abiotic and biotic impacts, especially under conditions of future climate change, mechanistic models of edge effects have not been forthcoming. A simple numerical model of two-dimensional heat flow is developed and applied to a vertical forest/clearcut edge profile and to simulated fragmented landscapes. Height-specific thermal diffusivity and conductivity in the forest were assumed to vary in proportion to foliage densities measured in the central Amazon. In the edge profile, the clearcut that abutted the edge served as a heat source and its temperature was maintained at a constant value higher than in the initially cooler forest. In the fragmented landscapes, simulated treefall gaps were heat sources whose temperature varied with sun movements during the day. Gap frequency was varied so as to approximate the gap coverage observed in selectively logged forests. In one set of simulations, temperature in the openings was systematically varied; in another, thermal diffusivity of the forest was varied. Along the edge profile, high temperatures in the clearcut were rapidly transmitted into the upper canopy due to additive edge effects. Temperatures in the forest understory were also very sensitive to clearcut temperatures due to relatively sparse understory foliage. An overall increase in forest diffusivity led to markedly higher temperatures close to the edge and a more even temperature distribution among height strata. In fragmented landscapes, total gap coverage and additivity from neighboring gaps strongly influenced forest temperatures. At low conductivities, heat flowed only into the forest close to the gaps and hence forest temperature increased almost linearly with gap area. However, at high conductivities, heat flowed far into the forest and forest temperature varied as a function of gap density in the surrounding neighborhood. Because of these additive effects, slight increases in total gap area led to disproportionate changes in the thermal profile of the landscape. These results have important implications for the conservation of forest ecosystems.