Keystone rodent interactions: prairie dogs and kangaroo rats structure the biotic composition of a desertified grassland

Understanding the interactive effects of multiple keystone species where they co-occur may have important consequences for regional biodiversity. Additionally, understanding how the impacts of keystone species vary across different ecosystems is important for effectively guiding conservation and management. We conducted a large-scale field study in northern Mexico where the geographic distributions of black-tailed prairie dogs Cynomys ludovicianus and banner-tailed kangaroo rats Dipodomys spectabilis overlap. These species are considered both keystones and ecosystem engineers of grassland environments, but little is known about their separate and interacting roles in desertified systems where they co-occur. Our research evaluated 1) the independent impacts of black-tailed prairie dogs and banner-tailed kangaroo rats in a desertified annual grassland, and 2) their interactive effects on grassland community structure and biodiversity. Prairie dogs and kangaroo rats differentially affected vegetation structure, plant cover, species composition, and species richness across multiple spatial and temporal scales. The interactive effects of these keystone species resulted in enhanced landscape heterogeneity and biodiversity. Our results demonstrate the importance of prairie dogs and kangaroo rats in desertified grasslands, and have important implications for understanding the interactive effects and context-dependency of keystone species.     

Arthropods of a semi-natural grassland in an urban environment: the John F. Kennedy International Airport,New York

Semi-natural grassland habitat fragments, such as those found on airports, might be important for arthropod conservation and biodiversity in urban ecosystems. The objectives of this study were to: (1) describe the arthropod communities present within the grasslands on the John F. Kennedy International Airport and (2) assess spatial and temporal variation in those arthropod communities. We collected arthropods using a vacuum sampler during 2003 and using sweep-net collection methods during 2003 and 2004. During 2003, a total of 1,467 arthropods, representing 17 orders and 68 families were found in vacuum samples. A total of 3,784 arthropods, representing 12 orders and 94 families were collected in sweep-net samples during 2003. In 2004, a total of 3,281 arthropods, representing 12 orders and 85 families were collected in sweep-net samples. Hemiptera, Orthoptera, and Diptera were the most abundant taxa, accounting for 47, 18, and 14% of all arthropods captured, respectively. We found evidence of spatial and temporal variation in arthropod abundance, in particular as noted by fluctuations in Orthoptera: Acrididae and Hemiptera: Auchenorrhyncha. Hemipteran family diversity was also influenced by habitat type. Grassland habitats on airfields, although influenced by anthropogenic factors (e.g., mowing), have the potential to provide abundant and diverse arthropod communities and might serve as a refugium for such species within urban ecosystems.     

Environmental gradients determine the potential for ecosystem engineering effects

Understanding processes that determine biodiversity is a fundamental challenge in ecology. At the landscape scale, physical alteration of ecosystems by organisms, called ecosystem engineering, enhances biodiversity worldwide by increasing heterogeneity in resource conditions and enhancing species coexistence across engineered and non‐engineered habitats. Engineering–diversity relationships can vary along environmental gradients due to changes in the amount of physical structuring created by ecosystem engineering, but it is unclear how this variation is influenced by the responsiveness of non‐structural abiotic properties to engineering. Here we show that environmental gradients determine the capacity for engineering to alter resource availability and species diversity, independent of the magnitude of structural change produced by engineering. We created an experimental rainfall gradient in an arid grassland where rodents restructure soils by constructing large, long‐lasting burrows. We found that greater rainfall increased water availability and productivity in both burrow and inter‐burrow habitats, causing a decline in local (alpha) plant diversity within both of these habitats. However, increased rainfall also resulted in greater differences in soil resources between burrow and inter‐burrow habitats, which increased species turnover (beta diversity) across habitats and stabilized landscape‐level (gamma) diversity. These responses occurred regardless of rodent presence and without changes in the extent of physical alteration of soils by rodents. Our results suggest that environmental gradients can influence the effects of ecosystem engineering in maintaining biodiversity via resource heterogeneity and species turnover. In an era of rapid environmental change, accounting for this interaction may be critical to conservation and management.     

Positive interactions between desert granivores: localized facilitation of harvester ants by kangaroo rats

Facilitation, when one species enhances the environment or performance of another species, can be highly localized in space. While facilitation in plant communities has been intensely studied, the role of facilitation in shaping animal communities is less well understood. In the Chihuahuan Desert, both kangaroo rats and harvester ants depend on the abundant seeds of annual plants. Kangaroo rats, however, are hypothesized to facilitate harvester ants through soil disturbance and selective seed predation rather than competing with them. I used a spatially explicit approach to examine whether a positive or negative interaction exists between banner-tailed kangaroo rat (Dipodomys spectabilis) mounds and rough harvester ant (Pogonomyrmex rugosus) colonies. The presence of a scale-dependent interaction between mounds and colonies was tested by comparing fitted spatial point process models with and without interspecific effects. Also, the effect of proximity to a mound on colony mortality and spatial patterns of surviving colonies was examined. The spatial pattern of kangaroo rat mounds and harvester ant colonies was consistent with a positive interspecific interaction at small scales (<10 m). Mortality risk of vulnerable, recently founded harvester ant colonies was lower when located close to a kangaroo rat mound and proximity to a mound partly predicted the spatial pattern of surviving colonies. My findings support localized facilitation of harvester ants by kangaroo rats, likely mediated through ecosystem engineering and foraging effects on plant cover and composition. The scale-dependent effect of kangaroo rats on abiotic and biotic factors appears to result in greater founding and survivorship of young colonies near mounds. These results suggest that soil disturbance and foraging by rodents can have subtle impacts on the distribution and demography of other species.     

Environmental DNA metabarcoding of wild flowers reveals diverse communities of terrestrial arthropods

Terrestrial arthropods comprise the most species‐rich communities on Earth, and grassland flowers provide resources for hundreds of thousands of arthropod species. Diverse grassland ecosystems worldwide are threatened by various types of environmental change, which has led to decline in arthropod diversity. At the same time, monitoring grassland arthropod diversity is time‐consuming and strictly dependent on declining taxonomic expertise. Environmental DNA (eDNA) metabarcoding of complex samples has demonstrated that information on species compositions can be efficiently and non‐invasively obtained. Here, we test the potential of wild flowers as a novel source of arthropod eDNA. We performed eDNA metabarcoding of flowers from several different plant species using two sets of generic primers, targeting the mitochondrial genes 16S rRNA and COI. Our results show that terrestrial arthropod species leave traces of DNA on the flowers that they interact with. We obtained eDNA from at least 135 arthropod species in 67 families and 14 orders, together representing diverse ecological groups including pollinators, parasitoids, gall inducers, predators, and phytophagous species. Arthropod communities clustered together according to plant species. Our data also indicate that this experiment was not exhaustive, and that an even higher arthropod richness could be obtained using this eDNA approach. Overall, our results demonstrate that it is possible to obtain information on diverse communities of insects and other terrestrial arthropods from eDNA metabarcoding of wild flowers. This novel source of eDNA represents a vast potential for addressing fundamental research questions in ecology, obtaining data on cryptic and unknown species of plant‐associated arthropods, as well as applied research on pest management or conservation of endangered species such as wild pollinators.     

Mechanisms for the keystone status of kangaroo rats: graminivory rather than granivory?

Graminivory by kangaroo rats (Dipodomys spp.) was investigated as a potential mechanism for the keystone role of these rodents in the dynamics of desert grasslands. Experiments confirmed that Ord's kangaroo rats (Dipodomys ordii) cut and consumed a large proportion of the tillers of three Chihuahuan Desert tussock-forming grass species. Field observations indicated that the characteristically cut grass tillers were absent from all-rodent and medium-sized kangaroo rat exclosures, but were frequent in large-sized kangaroo rat and rabbit exclosures, indicating that the medium-sized kangaroo rats (D. ordii, D. merriami) were responsible for grass cutting. Tiller waste as a percentage of peak standing crop ranged from 7% in grassland habitats to 0.7% in Flourensia cernua shrubland. Of the 13 species of perennial, tussock-forming grasses measured, only one, Muhlenbergia porteri, had no tillers cut by kangaroo rats. This study demonstrates that the keystone role of kangaroo rats in Chihuahuan Desert grassland ecosystems is probably the result of their graminivory. Received: 28 October 1996 / Accepted: 26 February 1997     

The arthropod,but not the vertebrate host or its environment,dictates bacterial community composition of fleas and ticks

Bacterial community composition in blood-sucking arthropods can shift dramatically across time and space. We used 16S rRNA gene amplification and pyrosequencing to investigate the relative impact of vertebrate host-related, arthropod-related and environmental factors on bacterial community composition in fleas and ticks collected from rodents in southern Indiana (USA). Bacterial community composition was largely affected by arthropod identity, but not by the rodent host or environmental conditions. Specifically, the arthropod group (fleas vs ticks) determined the community composition of bacteria, where bacterial communities of ticks were less diverse and more dependent on arthropod traits—especially tick species and life stage—than bacterial communities of fleas. Our data suggest that both arthropod life histories and the presence of arthropod-specific endosymbionts may mask the effects of the vertebrate host and its environment.     

Dietary niche differentiation among three species of invasive rodents (Rattus rattus, R. exulans, Mus musculus)

The diets of sympatric rodents partially define their realized niches. Identifying items in stomachs of introduced rodents helps determine rodents’ trophic positions and species most at risk of consumption. In the Hawaiian Islands, which lacked rodents prior to human arrival, three rodents (Rattus rattus or black rat, R. exulans or Pacific rat, Mus musculus or house mouse) commonly coexist in native habitats where they consume a wide range of plants and animals. These three rodent species were trapped in montane forest for 2.5 years; their stomach contents were analyzed to determine short-term diets (n = 12–95 indiv. per species), and isotopic fractions of δ¹⁵N and δ¹³C in their bone collagen were analyzed to further estimate their trophic positions (n = 11–20 indiv. per species). For all three species, >75 % of individuals had plants and >90 % had arthropods in their stomachs, and significant differences in mean relative abundances were found for food items in stomachs among all three rodents. Rodents may be dispersing some native and non-native seeds, including the highly invasive Clidemia hirta. Most identifiable arthropods in rodent stomachs were non-native, and no stomachs contained birds, snails, or lizards. The δ¹⁵N and δ¹³C signatures were consistent with trophic feeding differences revealed from stomach contents. Dietary niche differentiation by coexisting rodent species is evident in this forest, with Pacific rats being intermediate between the mostly carnivorous house mouse and the mostly herbivorous black rat; such findings can help forecast rodent impacts and direct management efforts in ecosystems where these invasive animals coexist.     

Redundant or complementary? Impact of a colonizing species on community structure and function

Recent studies suggest that species with similar functional traits will have similar effects on ecosystems, but evidence for redundancy of species impacts is limited. Here we use a long‐term experiment to gain insight into functional relationships within a desert rodent community. Experimental removal of kangaroo rats, Dipodomys spp., coupled with the recent, serendipitous colonization of a single species of large pocket mouse Chaetodipus baileyi yielded treatments that differed in the diversity of large granivorous rodents present. We evaluated functional overlap of C. baileyi and the other resident large granivores (i.e. the kangaroo rats) by comparing total energy use of granivorous rodents and total abundance and species richness of small granivores across treatments before and after the arrival of C. baileyi. We found that C. baileyi almost completely compensated for the changes in these key ecosystem‐level properties caused by kangaroo rat removal, but it differentially impacted the population dynamics of individual small granivorous rodent species. Thus, its effects were largely complementary, rather than redundant, to those of the missing kangaroo rats. Although short‐term or single‐measure analyses may suggest redundancy, our results support the longstanding dictum that niches of coexisting species are often similar but rarely, if ever, identical.     

Promotion of exotic weed establishment by endangered giant kangaroo rats (Dipodomys ingens) in a California grassland

Giant kangaroo rats (Dipodomys ingens) continually modify their burrow precincts by digging tunnels, clipping plants, and other activities. In the valley grasslands of the Carrizo Plain Natural Area (San Luis Obispo County, California), this chronic disturbance to soil and vegetation promoted the establishment of exotic ruderal and early successional plant species. Erodium cicutarium, Bromus madritensis ssp. rubens, and other Mediterranean annuals were found to constitute a very large proportion of the vegetation on giant kangaroo rat precincts. When vegetation on precincts was compared with the vegetation in less disturbed intermediate areas located between precincts, species richness, cover and frequency of exotic plants were significantly greater on precincts. The reverse was found for native species. In addition, exotic species encountered in this study had significantly larger seeds than did native species, suggesting that these granivorous kangaroo rats preferentially cache large weed seeds on their precincts. Since the kangaroo rats depend on exotic plants for food and the exotic plants depend upon the kangaroo rats to disturb their habitat continually, the weed-kangaroo rat relationship is mutualistic. This strong relationship may also inhibit population growth of native grassland plants which occupy disturbed habitats but have difficulty competing with exotic weeds for resources. From a conservation perspective, this mutualism presents an intractable management dilemma. Restoration of valley grasslands where endangered giant kangaroo rats occur, to conditions where native species dominate, may be impossible.     

Parasitic and phoretic arthropods of the elephant-eared and the Santa Cruz kangaroo rats

The parasitic and phoretic arthropods of the elephant-eared kangaroo rat (Dipodomys elephantinus) and Santa Cruz kangaroo rat (D. venustus) are reported; most of these represent new host records. Thirteen of 14 (93%) of D. elephantinus and 11 of 12 (92%) of D. venustus had 11 and nine arthropod species, respectively. Larval and nymphal stages of the tick Dermacentor occidentalis were the most prevalent parasite (77%) on D. elephantinus whereas the mesostigmatid mite Androlaelaps fahrenholzi was the most prevalent (56%) on D. venustus. The arthropod fauna of these two closely related rodents were similar with seven of the 14 arthropod species occurring on both host species. Two species of the host specific listrophorid mite of the genus Geomylichus were found on both hosts.     

Interactive disturbance effects of two disparate ecosystem engineers in North American shortgrass steppe

Disturbances such as fire, grazing, and soil mixing by animals interact to shape vegetation in grassland ecosystems. Animal-generated disturbances are unique in that they arise from a suite of behaviors that are themselves subject to modification by external factors. The manner in which co-occurring animal taxa interact to alter vegetation is a function of their respective behaviors, which shape the characteristics (e.g., the magnitude or extent) of their disturbances. To determine whether prairie dogs (Cynomys ludovicianus) and harvester ants (Pogonomyrmex occidentalis) interactively alter vegetation structure and heterogeneity on the Colorado shortgrass steppe, we characterized the size, dispersion, and vegetation of prairie dog burrow mounds and ant nests (located on and off prairie dog colonies) and vegetation growing beyond mound and nest perimeters. Ants located on prairie dog colonies engineered significantly larger nests and disturbed nearly twice as much total soil area as their off-colony counterparts. Ant nests were overdispersed both on and off prairie dog colonies, while prairie dog mounds were randomly dispersed. Where harvester ants and prairie dogs co-occur, the overdispersed pattern of on-colony ant nests is in effect "overlaid" onto the random pattern of prairie dog mounds, resulting in a unique, aggregated pattern of soil disturbance. Ant nests on prairie dog colonies had significantly less vegetation and lower plant species diversity than did prairie dog mounds, while off-colony nests were similar to mounds. These results suggest that ant nests are more highly disturbed when located on prairie dog colonies. Beyond nests proper, ants did not appear to alter vegetation in a manner distinct from prairie dogs. As such, the interactive effects of prairie dogs and ants on vegetation arise mainly from the disturbance characteristics of mounds and nests proper.     

Effects of habitat fragmentation and black-tailed prairie dogs on urban avian diversity

Urbanization and habitat fragmentation have the potential to influence bird communities. In addition, these phenomena, as well as ongoing lethal control measures, have also greatly reduced the range of the black-tailed prairie dog (Cynomys ludovicianus) since the beginning of the 20th century. Although prairie dogs are highly interactive species that can influence avian communities, few studies have investigated whether these interactions persist in urban settings. Our goal was to investigate the relative impacts of habitat fragmentation and prairie dogs on bird communities within an urban matrix. We performed bird surveys on 20 habitat fragments (10 colonized by prairie dogs, 10 uncolonized by prairie dogs) distributed throughout the Denver metropolitan area, and calculated Shannon–Weiner diversity and richness of all birds and native species, as well as total counts of grassland birds and raptors. Diversity, richness, and counts of many species increased with increasing fragment connectivity, and decreased on fragments isolated for longer periods of time. Avian diversity and richness did not differ between fragments with and without prairie dogs, suggesting that this element of the ecological role of prairie dogs is not fully retained in urban habitat. Future studies of the role of prairie dogs as keystone species in urban systems should include other taxa as well as consider the influence of the urban matrix surrounding prairie dog habitat. Our results emphasize that conservation of urban avian diversity should focus on landscape connectivity as well as local habitat features.     

Partitioning the effects of an ecosystem engineer: kangaroo rats control community structure via multiple pathways

1.?Ecosystem engineers impact communities by altering habitat conditions, but they can also have strong effects through consumptive, competitive and other non-engineering pathways. 2.?Engineering effects can lead to fundamentally different community dynamics than non-engineering effects, but the relative strengths of these interactions are seldom quantified. 3.?We combined structural equation modelling and exclosure experiments to partition the effects of a keystone engineer, the giant kangaroo rat (Dipodomys ingens), on plants, invertebrates and vertebrates in a semi-arid California grassland. 4.?We separated the effects of burrow creation from kangaroo rat density and found that kangaroo rats increased the diversity and abundance of other species via both engineering and non-engineering pathways. 5.?Engineering was the primary factor structuring plant and small mammal communities, whereas non-engineering effects structured invertebrate communities and increased lizard abundance. 6.?These results highlight the importance of the non-engineering effects of ecosystem engineers and shed new light on the multiple pathways by which strong-interactors shape communities.     

荒漠啮齿动物群落对开垦干扰的响应及其种群生态对策

开垦对功能相对脆弱的荒漠生态系统是重要的干扰,这种干扰往往导致栖息地破碎化,并对动植物群落产生强烈影响。作为荒漠生态系统的重要成分,啮齿动物群落受到开垦干扰后对环境的响应及其群落中种群的生态对策,是荒漠生态系统生物多样性及其功能维持稳定的重要基础。2006～2011年,采用标志重捕法对内蒙古阿拉善荒漠区未开垦和开垦草地啮齿动物群落格局及其不同生态对策种群的数量组成进行了专门研究。目的（1）明确开垦干扰下啮齿动物群落格局时间尺度变化;（2）验证假设：人为干扰区（开垦区）啮齿动物群落中r?对策者占据优势,未干扰区（未开垦区）以K?对策者为主;（3）依据啮齿动物群落中不同生态对策种群的数量组成来判断群落所受干扰的程度。结果表明,开垦干扰降低了啮齿动物群落多样性,改变了群落中不同生态对策种群的数量组成,种群以r?对策者为优势;未开垦区啮齿动物群落中以K?对策种群为主。开垦区啮齿动物群落受到严重干扰。     

Prairie dog presence affects occurrence patterns of disease vectors on small mammals

Wildlife disease is recognized as a burgeoning threat to imperiled species and aspects of host and vector community ecology have been shown to have significant effects on disease dynamics. The black‐tailed prairie dog is a species of conservation concern that is highly susceptible to plague, a flea‐transmitted disease. Prairie dogs (Cynomys) alter the grassland communities in which they exist and have been shown to affect populations of small rodents, which are purported disease reservoirs. To explore potential ecological effects of black‐tailed prairie dogs on plague dynamics, we quantified flea occurrence patterns on small mammals in the presence and absence of prairie dogs at 8 study areas across their geographic range. Small mammals sampled from prairie dog colonies showed significantly higher flea prevalence, flea abundance, and relative flea species richness than those sampled from off‐colony sites. Successful plague transmission likely is dependent on high prevalence and abundance of fleas that can serve as competent vectors. Prairie dogs may therefore facilitate the maintenance of plague by increasing flea occurrence on potential plague reservoir species. Our data demonstrate the previously unreported ecological influence of prairie dogs on vector species assemblages, which could influence disease dynamics.     

Rapid Decline of a Grassland System and Its Ecological and Conservation Implications

One of the most important conservation issues in ecology is the imperiled state of grassland ecosystems worldwide due to land conversion, desertification, and the loss of native populations and species. The Janos region of northwestern Mexico maintains one of the largest remaining black-tailed prairie dog (Cynomys ludovicianus) colony complexes in North America and supports a high diversity of threatened and endangered species. Yet, cattle grazing, agriculture, and drought have greatly impacted the region. We evaluated the impact of human activities on the Janos grasslands, comparing changes in the vertebrate community over the last two decades. Our results reveal profound, rapid changes in the Janos grassland community, demonstrating large declines in vertebrate abundance across all taxonomic groups. We also found that the 55,000 ha prairie dog colony complex has declined by 73% since 1988. The prairie dog complex has become increasingly fragmented, and their densities have shown a precipitous decline over the years, from an average density of 25 per ha in 1988 to 2 per ha in 2004. We demonstrated that prairie dogs strongly suppressed woody plant encroachment as well as created open grassland habitat by clearing woody vegetation, and found rapid invasion of shrubland once the prairie dogs disappeared from the grasslands. Comparison of grasslands and shrublands showed markedly different species compositions, with species richness being greatest when both habitats were considered together. Our data demonstrate the rapid decline of a grassland ecosystem, and documents the dramatic loss in biodiversity over a very short time period concomitant with anthropogenic grassland degradation and the decline of a keystone species.     

Arthropods and biofuel production systems in North America

Abstract Biomass harvest may eventually be conducted on over 100 000 000 ha of US crop and forest lands to meet federally-mandated targets for renewable biofuels. Such large-scale land use changes could profoundly impact working landscapes and the arthropod communities that inhabit them. We review the literature on dedicated biofuel crops and biomass harvest from forests to look for commonalities in arthropod community responses. With expanded biofuel production, existing arthropod pests of biofuel crops will likely become more important and new pests will emerge. Beneficial arthropods will also be influenced by biofuel crop habitats, potentially altering the distribution of pollination and pest control services to the surrounding landscape. Production of biofuel crops including initial crop selection, genetic improvement, agronomic practices, and harvest regimes will also influence arthropod communities. In turn, arthropods will impact the productivity and species composition of biomass production systems. Some of these processes have the potential to cause landscape-level changes in arthropod community dynamics and insect-vectored plant diseases. Finally, changes in arthropod populations and their spatiotemporal distribution in the landscape will have impacts on consumers of insects at higher trophic levels, potentially influencing their population and community dynamics and producing feedbacks to arthropod communities. Given that dedicated biofuel crops and intensified biomass harvest from forests are still relatively uncommon in North America, as they increase, we anticipate ‘predictably unpredictable’ shifts in arthropod communities and the ecosystem services and functions they support. We suggest that research on arthropod dynamics within biofuel crops, their spillover into adjacent habitats, and implications for the sustainability of working landscapes are critical topics for both basic and applied investigations.     

Role of arthropod communities in bioenergy crop litter decomposition†

The extensive land use conversion expected to occur to meet demands for bioenergy feedstock production will likely have widespread impacts on agroecosystem biodiversity and ecosystem services, including carbon sequestration. Although arthropod detritivores are known to contribute to litter decomposition and thus energy flow and nutrient cycling in many plant communities, their importance in bioenergy feedstock communities has not yet been assessed. We undertook an experimental study quantifying rates of litter mass loss and nutrient cycling in the presence and absence of these organisms in three bioenergy feedstock crops—miscanthus (Miscanthus x giganteus), switchgrass (Panicum virgatum), and a planted prairie community. Overall arthropod abundance and litter decomposition rates were similar in all three communities. Despite effective reduction of arthropods in experimental plots via insecticide application, litter decomposition rates, inorganic nitrogen leaching, and carbon–nitrogen ratios did not differ significantly between control (with arthropods) and treatment (without arthropods) plots in any of the three community types. Our findings suggest that changes in arthropod faunal composition associated with widespread adoption of bioenergy feedstock crops may not be associated with profoundly altered arthropod‐mediated litter decomposition and nutrient release.