Perturbation and abrupt shift in trophic control of biodiversity and productivity

Ecology is founded on the view that ecosystem properties like biodiversity and productivity change smoothly with changing environmental conditions. However, emerging theory predicts that environmental change may cause abrupt shifts to alternate states. In many ecosystems, top predators play a pivotal role in controlling plant productivity and diversity. Yet it remains uncertain if altering this control shifts systems to alternate states. I report on a test of the hypothesis that loss of predator control of ecosystem function causes abrupt state changes in diversity and productivity. In this meadow ecosystem, predators enhance plant diversity by causing a highly productive, competitively dominant plant species to be suppressed by herbivores. Experimental predator removal caused rapid proliferation of the competitively dominant plant. Moreover, temporally staggered predator reintroductions failed to restore the ecosystem. This loss of resilience confirmed that the ecosystem crossed a critical threshold and entrained into an alternate state.     

Frequency of prenatal loss in a macaque breeding colony

An accurate knowledge of the historical incidence of prenatal loss is essential for management of breeding colonies and for performing developmental toxicity studies in nonhuman primates. Data from the California Regional Primate Research Center indoor (timed-mated) and outdoor (random-mated) colonies of rhesus, cynomolgus, and bonnet macaques (Macaca mulatta, M. fascicularis, and M. radiata) were evaluated for a 10 year breeding period from 1984 to 1993. Pregnancy outcome data for the three species of macaques summarized in this report indicate that early pregnancy as well as term are vulnerable periods of gestation in terms of prenatal loss. Prematurity as well as twinning were additionally associated with elevated rates of loss during the prenatal or neonatal period. The incidence of pregnancy failure did not appear to be related to different housing/management conditions (i.e., indoor timed-mated vs. outdoor random-mated), parity, animal handling, shipping, or relocation. Some of the annual fluctuations in abortions could be related to disease outbreaks (e.g., measles, pneumonia) in the colony. These data will be invaluable in planning for research needs which focus on developmental biology and perinatology, and in interpreting the significance of abortions following exposure to experimental agents in small numbers of animals. © 1996 Wiley-Liss, Inc.     

Ultrafast evolution and loss of CRISPRs following a host shift in a novel wildlife pathogen, Mycoplasma gallisepticum

Measureable rates of genome evolution are well documented in human pathogens but are less well understood in bacterial pathogens in the wild, particularly during and after host switches. Mycoplasma gallisepticum (MG) is a pathogenic bacterium that has evolved predominantly in poultry and recently jumped to wild house finches (Carpodacus mexicanus), a common North American songbird. For the first time we characterize the genome and measure rates of genome evolution in House Finch isolates of MG, as well as in poultry outgroups. Using whole-genome sequences of 12 House Finch isolates across a 13-year serial sample and an additional four newly sequenced poultry strains, we estimate a nucleotide diversity in House Finch isolates of only ～2% of ancestral poultry strains and a nucleotide substitution rate of 0.8-1.2×10(-5) per site per year both in poultry and in House Finches, an exceptionally fast rate rivaling some of the highest estimates reported thus far for bacteria. We also found high diversity and complete turnover of CRISPR arrays in poultry MG strains prior to the switch to the House Finch host, but after the invasion of House Finches there is progressive loss of CRISPR repeat diversity, and recruitment of novel CRISPR repeats ceases. Recent (2007) House Finch MG strains retain only ～50% of the CRISPR repertoire founding (1994-95) strains and have lost the CRISPR-associated genes required for CRISPR function. Our results suggest that genome evolution in bacterial pathogens of wild birds can be extremely rapid and in this case is accompanied by apparent functional loss of CRISPRs.     

Detritivory: stoichiometry of a neglected trophic level

Previous syntheses have identified the key roles that phylogeny, body size, and trophic level play in determining arthropod stoichiometry. To date, however, detritivores have been largely omitted from such syntheses, despite their importance in nutrient cycling, biodiversity, and food web interactions. Here, we report on a compiled database of the allometry and nutritional stoichiometry (N and P) of detritivorous arthropods. Overall, both N and P content for detritivores varied among major phylogenetic lineages. Detritivore N content was similar to the N content of herbivores, but below that of predators. By contrast, detritivore P content was independent of trophic level. Contrary to previous reports, neither nutrient varied with body size. This analysis places detritivores in the context of related herbivores and predators, and as such, sets the stage for future investigations into the causes and consequences of elemental (mis)matches between detritivores and their detrital resources. Holly M. Martinson and Katie Schneider are co-first author.     

Defensive endosymbionts: a cryptic trophic level in community ecology

Maternally transmitted endosymbionts are widespread among insects, but how they are maintained within host populations is largely unknown. Recent discoveries show that some endosymbionts protect their hosts from pathogens or parasites. Spiroplasma, an endosymbiont of Drosophila neotestacea, protects female hosts from the sterilizing effects of parasitism by the nematode Howardula aoronymphium. Here, we show that Spiroplasma spreads rapidly within experimental populations of D. neotestacea subject to Howardula parasitism, but is neither strongly favored nor selected against in the absence of Howardula. In a reciprocal experiment, Howardula declined steadily to extinction in populations of Spiroplasma-infected flies, whereas in populations of uninfected flies, the prevalence of Howardula parasitism increased to c. 100%. Thus, Spiroplasma and Howardula exhibit effectively consumer-resource trophic dynamics. The recent spread of Spiroplasma in natural populations of D. neotestacea coincides with a decline in the prevalence of Howardula parasitism in the wild.     

Tree diversity alters the structure of a tri‐trophic network in a biodiversity experiment

Species and processes in ecosystems are part of multi‐trophic interaction networks. Plants represent the lowest trophic level in terrestrial ecosystems, and experiments have shown a stabilizing effect of plant diversity on higher trophic levels. Such evidence has been mainly collected in experimental grasslands. Forests are structurally more complex than grasslands and support the majority of the global biodiversity, but studies on multi‐trophic interaction networks are missing in experimental tree diversity gradients. In a forest diversity experiment in southeast China, we examined how tree diversity affects the structure of trophobiotic networks. Trophobioses are tri‐trophic interactions between plants, sap‐sucking Hemiptera and honeydew‐collecting ants that can be subdivided into a largely mutualistic Hemiptera–ant and an antagonistic plant–Hemiptera network. We inspected almost 7000 trees in 146 plots ranging from monocultures to 16 tree species mixtures and found 194 trophobioses consisting of 15 tree, 33 Hemiptera and 18 ant species. We found that tree diversity increased the proportion of trees harboring trophobioses. Consistent with the prediction that mutualistic and antagonistic networks respond differently to changing environments, we found that the generality index of the mutualistic Hemiptera–ant but not the antagonistic plant–Hemiptera network increased with tree diversity. High generality, maintained by high tree diversity, might correspond to higher functional stability. Hence, our results indicate that tree diversity could increase via bottom–up processes the robustness of ant–Hemiptera associations against changing environmental conditions. In turn, the plant–Hemiptera network was highly complementary, suggesting that host‐specific Hemiptera species may be vulnerable to co‐extinction if their host plants disappear. Based on our results, we provide possible future research directions to further disentangle the bottom–up effect of tree diversity on the structure of trophobiotic networks. Synthesis It is now widely accepted that plant diversity promotes ecosystem functionality and stability. However, it is still largely unknown how plant diversity affects interactions between trophic levels and if different interaction types are affected differently. Using a tri‐trophic study system consisting of plants, sap‐sucking Hemiptera, and ants we provide evidence that increasing local plant diversity stabilizes the mutualistic Hemiptera–ant but not the antagonistic plant–Hemiptera networks. Our results suggest that bottom–up effects of plant diversity on trophic interactions might generally depend on the type of interaction (mutualistic versus antagonistic) considered.     

The functional role of biodiversity in ecosystems: incorporating trophic complexity

Understanding how biodiversity affects functioning of ecosystems requires integrating diversity within trophic levels (horizontal diversity) and across trophic levels (vertical diversity, including food chain length and omnivory). We review theoretical and experimental progress toward this goal. Generally, experiments show that biomass and resource use increase similarly with horizontal diversity of either producers or consumers. Among prey, higher diversity often increases resistance to predation, due to increased probability of including inedible species and reduced efficiency of specialist predators confronted with diverse prey. Among predators, changing diversity can cascade to affect plant biomass, but the strength and sign of this effect depend on the degree of omnivory and prey behaviour. Horizontal and vertical diversity also interact: adding a trophic level can qualitatively change diversity effects at adjacent levels. Multitrophic interactions produce a richer variety of diversity-functioning relationships than the monotonic changes predicted for single trophic levels. This complexity depends on the degree of consumer dietary generalism, trade-offs between competitive ability and resistance to predation, intraguild predation and openness to migration. Although complementarity and selection effects occur in both animals and plants, few studies have conclusively documented the mechanisms mediating diversity effects. Understanding how biodiversity affects functioning of complex ecosystems will benefit from integrating theory and experiments with simulations and network-based approaches.     

Consequences of variation in plant defense for biodiversity at higher trophic levels

Antagonistic interactions between insect herbivores and plants impose selection on plants to defend themselves against these attackers. Although selection on plant defense traits has typically been studied for pairwise plant-attacker interactions, other community members of plant-based food webs are unavoidably affected by these traits as well. A plant trait might, for example, affect parasitoids and predators feeding on the herbivore. Consequently, defensive plant traits structure the diversity and composition of the complex community associated with the plant, and communities as a whole also feed back to selection on plant traits. Here, we review recent developments in our understanding of how plant defense traits structure insect communities and discuss how molecular mechanisms might drive community-wide effects.     

Arthropod biodiversity loss and the transformation of a tropical agro-ecosystem

The coffee (Coffea arabica) agro-ecosystem in the Central Valley of Costa Rica was formerly characterized by a high vegetational diversity. This complex system has been undergoing a major transformation to capital-intensive monocultural plantations where all shade trees are eliminated. In this study we examined the pattern of arthropod biodiversity loss associated with this transformation. Canopy arthropods were sampled in three coffee farms: a traditional plantation with many species of shade trees, a moderately shaded plantation with only Erythrina poeppigeana and coffee, and a coffee monoculture. An insecticidal fogging technique was used to sample both canopy and coffee arthropods. Data are presented on three major taxonomic groups: Coleoptera, non-formicid Hymenoptera, and Formicidae. Data demonstrate that the transformation of the coffee agro-ecosystem results in a significant loss of biological diversity of both canopy arthropods as well as arthropods living in coffee bushes. Percentage of species overlap was very small for all comparisons. Furthermore, species' richness on a per tree basis was found to be within the same order of magnitude as that reported for trees in tropical forests. If results presented here are generalizable, this means that conservation efforts to preserve biological diversity should also include traditional agro-ecosystems as conservation units.     

Causes of the species-area relationship by trophic level in a field-based microecosystem

Using a natural microecosystem, I test the contribution of the metapopulation effect to the species-area relationship, relative to that of the combined effects of habitat heterogeneity and sampling. The relative contributions were approximately equal, but with further relaxation of the fragmented community, the metapopulation effect is expected to increase. Predators had a greater slope to their species-area relationship than non-predators, and the habitat-plus-sampling effect was greater in predators than non-predators. This is the first attempt, to my knowledge, to quantify the causes of the species-area relationship.     

Valuing biodiversity and nature conservation at a local level

At a time where much of the discussion about major issues in nature conservation is necessarily undertaken at a global level, it is still important to consider the needs of the smaller organizations who do much of the grass roots work in the protection of wildlife and biodiversity. This study focuses on one such group, and examines how the contingent valuation method can be used to help to inform its decisions relating to the management of its portfolio of reserves in order to maximize benefits to its members. This paper argues that at a local level, where actions will not have significant global effects, contingent valuation methodology can inform decisions by assessing the value of additional reserves or particular conservation programmes to members in terms of their willingness to pay to acquire or implement them.     

Status of the long-tailed macaque Macaca fascicularis in Singapore and implications for management

The long-tailed macaque (Macaca fascicularis) population of the island-state of Singapore consists of ca. 1,218–1,454 individuals. About seventy percent of the population (ca. 1,027 individuals) is concentrated in both Bukit Timah and Central Catchment Nature Reserves, a system of reservoirs and forest reserves located in the center of Singapore. This core population resides mainly along perimeter forest areas of the reserve system, which is bordered by residential and recreational areas (e.g., parks and golf courses) and encircled by expressways. Periphery sub-populations (ca. 427 individuals) persist in forest fragments throughout Singapore mainland and on 5 offshore islands. Much of the Singaporean macaque population overlaps with human settlement and these commensal groups are mainly distributed close to roads, parks and residential areas. At least 70% of these groups are habituated to human presence and at least 50% to food provisioning. Moreover, commensal groups have more individuals and have higher infant:adult female ratios than non-commensal groups. The close association of habituated macaque groups living in human environments has led to increasing human-macaque conflict in Singapore. The overlap is also associated with human-induced population loss resulting from road accidents (2.4%); and trapping efforts (14%) aimed at ameliorating conflict issues. Consequently, it is important to better understand how humans are affecting macaque populations. In order to mitigate human-macaque conflict and at the same maintain a sustainable macaque population in Singapore, there is an urgent need for wildlife management strategies aimed at minimizing the extent of human–macaque conflict. Such strategies should include designing appropriate buffers around reserve areas, revised urban development plans, and managing the behavior of people interfacing with macaques.     

The decline of the trophic level concept

The development of the trophic level concept(1) is described and the causes of its failure as a predictive model in ecology are examined. A defence(2) of and modifications to the trophic level concept are reviewed. A trend towards taxonomic food web analysis is identified leading to models that are independent of the trophic level approach.     

Testing hypotheses of trophic level interactions: a boreal forest ecosystem

Models of community organization involve variations of the top-down (predator control) or bottom-up (nutrient limitation) hypotheses. Verbal models, however, can be interpreted in different ways leading to confusion. Therefore, we predict from first principles the range of possible trophic level interactions, and define mathematically the instantaneous effects of experimental perturbations. Some of these interactions are logically and biologically unfeasible. The remaining set of 27 feasible models is based on an initial assumption, for simplicity, of linear interactions between trophic levels. Many more complex and non-linear models are logically feasible but, for parsimony, simple ones are tested first. We use an experiment in the boreal forest of Canada to test predictions of instantaneous changes to trophic levels and distinguish between competing models. Seven different perturbations systematically removed each trophic level or, for some levels, supplemented them. The predictions resulting from the perturbations were concerned with the direction of change in biomass in the other levels. The direct effects of each perturbation produced strong top-down and bottom-up changes in biomass. At both the vegetation and herbivore levels top-down was stronger than bottom-up despite some compensatory growth stimulated by herbivory. The combination of experiments produced results consistent with two-way (reciprocal) interactions at each level. Indirect effects on one or two levels removed from the perturbation were either very weak or undetectable. Top-down effects were strong when direct but attenuated quickly. Bottom-up effects were less strong but persisted as indirect effects to higher levels. Although the 'pure reciprocal' model best fits our results for the boreal forest system different models may apply to different ecosystems around the world.