Mycorrhiza modulates aboveground tri‐trophic interactions to the fitness benefit of its host plant

1. Arbuscular mycorrhiza (AM), the association of AM fungi and plant roots, may alter morphological and physiological attributes of aboveground plant parts and thereby influence plant‐associated organisms such as herbivores and their natural enemies, predators and parasitoids. 2. The interactions between AM and the players of aboveground tri‐trophic systems have mainly been considered in isolation from each other. The effects of AM on aboveground herbivore–carnivore population dynamics and the consequences to plant fitness are unknown. 3. We explored AM‐induced compensatory mechanisms for AM‐promoted proliferation of the herbivorous spider mite, Tetranychus urticae Koch, on whole bean plants, Phaseolus vulgaris L. Vegetative and reproductive plant growth, AM fungal colonisation levels, and mite densities were assessed on spider mite‐infested plants colonised or not by the AM fungus Glomus mosseae Nicol. & Gerd, and harbouring the natural enemy of the spider mites, the predatory mite Phytoseiulus persimilis Anthias‐Henriot or not. 4. AM symbiosis modulated the aboveground tri‐trophic system to the fitness benefit of the plant. AM‐increased plant productivity outweighed the fitness decrease due to AM‐promoted herbivory: at similar vegetative growth, mycorrhizal plants produced more seeds than non‐mycorrhizal plants. 5. AM‐increased spider mite population levels were compensated for by enhanced population growth of the predators and increased plant tolerance to herbivory. 6. AM‐enhanced predator performance looped back to the AM fungus and stabilised its root colonisation levels, providing the first experimental evidence of a mutually beneficial interaction between AM and an aboveground third trophic level natural enemy.     

Arbuscular mycorrhiza enhances preference of ovipositing predatory mites for direct prey‐related cues

Most terrestrial plants are associated with arbuscular mycorrhizal fungi but research on the effects of arbuscular mycorrhizal symbiosis on aboveground plant‐associated organisms is scarcely expanded to tri‐trophic systems. The arbuscular mycorrhizal fungus Glomus mosseae Nicol. & Gerd. enhances fitness of the two‐spotted spider mite Tetranychus urticae Koch and its natural enemy, the predatory mite Phytoseiulus persimilis Athias‐Henriot, via changes in host plant and prey quality, respectively. In the present study, it is hypothesized that gravid P. persimilis are able to recognize arbuscular mycorrhiza‐enhanced prey quality and behave accordingly. In two experiments, on leaf arenas and in cages, P. persimilis is given a choice between prey patches deriving from mycorrhizal and non‐mycorrhizal bean plants (Phaseolus vulgaris L.) as feeding and oviposition sites. The use of cages allows the manipulation of distinct patch components acting as possible cues to guide predator foraging and oviposition behaviours, such as eggs produced and traces (webbing and faeces) left by the spider mite females. Both experiments show that P. persimilis preferentially resides close to prey fed on mycorrhizal plants. The cage experiment reveals that P. persimilis uses direct prey‐related cues, mainly derived from eggs, to discern prey quality and preferentially oviposits close to prey from mycorrhizal plants. This is the first study to document that predators recognize arbuscular mycorrhiza‐induced changes in herbivorous prey quality via direct prey‐related cues.     

Responses of belowground communities to large aboveground herbivores: Meta‐analysis reveals biome‐dependent patterns and critical research gaps

The importance of herbivore–plant and soil biota–plant interactions in terrestrial ecosystems is amply recognized, but the effects of aboveground herbivores on soil biota remain challenging to predict. To find global patterns in belowground responses to vertebrate herbivores, we performed a meta‐analysis of studies that had measured abundance or activity of soil organisms inside and outside field exclosures (areas that excluded herbivores). Responses were often controlled by climate, ecosystem type, and dominant herbivore identity. Soil microfauna and especially root‐feeding nematodes were negatively affected by herbivores in subarctic sites. In arid ecosystems, herbivore presence tended to reduce microbial biomass and nitrogen mineralization. Herbivores decreased soil respiration in subarctic ecosystems and increased it in temperate ecosystems, but had no net effect on microbial biomass or nitrogen mineralization in those ecosystems. Responses of soil fauna, microbial biomass, and nitrogen mineralization shifted from neutral to negative with increasing herbivore body size. Responses of animal decomposers tended to switch from negative to positive with increasing precipitation, but also differed among taxa, for instance Oribatida responded negatively to herbivores, whereas Collembola did not. Our findings imply that losses and gains of aboveground herbivores will interact with climate and land use changes, inducing functional shifts in soil communities. To conceptualize the mechanisms behind our findings and link them with previous theoretical frameworks, we propose two complementary approaches to predict soil biological responses to vertebrate herbivores, one focused on an herbivore body size gradient, and the other on a climate severity gradient. Major research gaps were revealed, with tropical biomes, protists, and soil macrofauna being especially overlooked.     

Influence of presence and spatial arrangement of belowground insects on host‐plant selection of aboveground insects: a field study

Abstract 1. Several studies have shown that above‐ and belowground insects can interact by influencing each others growth, development, and survival when they feed on the same host‐plant. In natural systems, however, insects can make choices on which plants to oviposit and feed. A field experiment was carried out to determine if root‐feeding insects can influence feeding and oviposition preferences and decisions of naturally colonising foliar‐feeding insects. 2. Using the wild cruciferous plant Brassica nigra and larvae of the cabbage root fly Delia radicum as the belowground root‐feeding insect, naturally colonising populations of foliar‐feeding insects were monitored over the course of a summer season. 3. Groups of root‐infested and root‐uninfested B. nigra plants were placed in a meadow during June, July, and August of 2006 for periods of 3 days. The root‐infested and the root‐uninfested plants were either dispersed evenly or placed in clusters. Once daily, all leaves of each plant were carefully inspected and insects were removed and collected for identification. 4. The flea beetles Phyllotreta spp. and the aphid Brevicoryne brassicae were significantly more abundant on root‐uninfested (control) than on root‐infested plants. However, for B. brassicae this was only apparent when the plants were placed in clusters. Host‐plant selection by the generalist aphid M. persicae and oviposition preference by the specialist butterfly P. rapae, however, were not significantly influenced by root herbivory. 5. The results of this study show that the presence of root‐feeding insects can affect feeding and oviposition preferences of foliar‐feeding insects, even under natural conditions where many other interactions occur simultaneously. The results suggest that root‐feeding insects play a role in the structuring of aboveground communities of insects, but these effects depend on the insect species as well as on the spatial distribution of the root‐feeding insects.     

Field evidence for indirect interactions between foliar‐feeding insect and root‐feeding nematode communities on Nicotiana tabacum

Abstract 1. As herbivory often elicits systemic changes in plant traits, indirect interactions via induced plant responses may be a pervasive feature structuring herbivore communities. Although the importance of this phenomenon has been emphasised for herbivorous insects, it is unknown if and how induced responses contribute to the organisation of other major phytoparasitic taxa. 2. Survey and experimental field studies were used to investigate the role of plants in linking the dynamics of foliar‐feeding insects and root‐feeding nematodes on tobacco, Nicotiana tabacum. 3. Plant‐mediated interactions between insects and nematodes could largely be differentiated by insect feeding guild, with positive insect–nematode interactions predominating with leaf‐chewing insects (caterpillars) and negative interactions occurring with sap‐feeding insects (aphids). For example, insect defoliation was positively correlated with the abundance of root‐feeding nematodes, but aphids and nematodes were negatively correlated. Experimental field manipulations of foliar insect and nematode root herbivory also tended to support this outcome. 4. Overall, these results suggest that plants indirectly link the dynamics of divergent consumer taxa in spatially distinct ecosystems. This lends support to the growing perception that plants play a critical role in propagating indirect effects among a diverse assemblage of consumers.     

Fertilisers and insect herbivores: a meta‐analysis

Despite the importance of a thorough understanding of the effect of synthetic fertiliser on insect population dynamics, existing literature is conflicting and an area of intense debate. Here, a categorical random‐effects meta‐analysis and a vote count meta‐analysis are employed to examine the effects of nitrogen (N), phosphorus (P), potassium (K) and NPK fertiliser on insect population dynamics. In agreement with the general consensus, insects were found to respond positively, overall, to fertilisers. Sucking insects showed a much stronger response to fertilisers than chewing insects. The environment in which a study is conducted can have a marked effect on insect responses to fertiliser, with natural environments showing the potential for buffering effects of nitrogen fertilisers in particular. As well as highlighting the potential shortfall in the amount of research investigating particularly the effects of potassium and phosphorus, this study provides an invaluable flag post in the ongoing research investigating fertiliser effects on ecosystems.     

Interactions among plants,bacteria, and fungi reduce extracellular enzyme activities under long‐term N fertilization

Atmospheric nitrogen (N) deposition has enhanced soil carbon (C) stocks in temperate forests. Most research has posited that these soil C gains are driven primarily by shifts in fungal community composition with elevated N leading to declines in lignin degrading Basidiomycetes. Recent research, however, suggests that plants and soil microbes are dynamically intertwined, whereby plants send C subsidies to rhizosphere microbes to enhance enzyme production and the mobilization of N. Thus, under elevated N, trees may reduce belowground C allocation leading to cascading impacts on the ability of microbes to degrade soil organic matter through a shift in microbial species and/or a change in plant–microbe interactions. The objective of this study was to determine the extent to which couplings among plant, fungal, and bacterial responses to N fertilization alter the activity of enzymes that are the primary agents of soil decomposition. We measured fungal and bacterial community composition, root–microbial interactions, and extracellular enzyme activity in the rhizosphere, bulk, and organic horizon of soils sampled from a long‐term (>25 years), whole‐watershed, N fertilization experiment at the Fernow Experimental Forest in West Virginia, USA. We observed significant declines in plant C investment to fine root biomass (24.7%), root morphology, and arbuscular mycorrhizal (AM) colonization (55.9%). Moreover, we found that declines in extracellular enzyme activity were significantly correlated with a shift in bacterial community composition, but not fungal community composition. This bacterial community shift was also correlated with reduced AM fungal colonization indicating that declines in plant investment belowground drive the response of bacterial community structure and function to N fertilization. Collectively, we find that enzyme activity responses to N fertilization are not solely driven by fungi, but instead reflect a whole ecosystem response, whereby declines in the strength of belowground C investment to gain N cascade through the soil environment.     

Above‐ and belowground insect herbivores mediate the impact of nitrogen eutrophication on the soil food web in a grassland ecosystem

Insect herbivores are important drivers of ecosystem processes in grasslands, and can mediate the grassland's response to environmental change. For example, recent evidence shows that above‐ and belowground herbivory, individually and in combination, can modify how a plant community responds to nitrogen (N) eutrophication, an important driver of global change. However, knowledge about how such effects extend to the associated soil food web is lacking. In a mesocosm experiment, we investigated how communities of soil nematodes – an abundant and functionally important group of soil organisms – responded to above‐ and belowground insect herbivory at contrasting N levels. We found that the strongest influence of above‐ and belowground herbivory on the nematode community appeared at elevated N. The abundance of root‐feeding nematodes increased when either above‐ or belowground insect herbivores were present at elevated N, but when applied together the two herbivore types cancelled out one another's effect. Additionally, at elevated N aboveground herbivory increased the abundance of fungal‐feeders relative to bacterial‐feeders, which indicates changes in decomposition pathways induced by N and herbivory. Belowground herbivory increased the abundance of omnivorous nematodes. The shifts in both the herbivorous and detrital parts of the soil food web demonstrate that above‐ and belowground herbivory does not only mediate the response of the plant community to N eutrophication, but in extension also the soil food web sustained by the plant community. We conclude that feedbacks between effects of above‐ and belowground herbivory mediate the response of the grassland ecosystem to N eutrophication.     

Localized and non‐localized effects of arbuscular mycorrhizal symbiosis on accumulation of osmolytes and aquaporins and on antioxidant systems in maize plants subjected to total or partial root drying

The arbuscular mycorrhizal (AM) symbiosis alters host plant physiology under drought stress, but no information is available on whether or not the AM affects respond to drought locally or systemically. A split‐root system was used to obtain AM plants with total or only half root system colonized as well as to induce physiological drought affecting the whole plant or non‐physiological drought affecting only the half root system. We analysed the local and/or systemic nature of the AM effects on accumulation of osmoregulatory compounds and aquaporins and on antioxidant systems. Maize plants accumulated proline both, locally in roots affected by drought and systemically when the drought affected the whole root system, being the last effect ampler in AM plants. PIPs (plasma membrane intrinsic proteins) aquaporins were also differently regulated by drought in AM and non‐AM root compartments. When the drought affected only the AM root compartment, the rise of lipid peroxidation was restricted to such compartment. On the contrary, when the drought affected the non‐AM root fraction, the rise of lipid peroxidation was similar in both root compartments. Thus, the benefits of the AM symbiosis not only rely in a lower oxidative stress in the host plant, but it also restricts locally such oxidative stress.     

Laboratory experiments imply the conditionality of mycorrhizal benefits for Salix repens: role of pH and nitrogen to phosphorus ratios

Responses of one arbuscular mycorrhizal fungus (Glomus mosseae) and two ectomycorrhizal fungi (Hebeloma leucosarx, Paxillus involutus) to a range of substrate conditions were investigated in the laboratory. Non-mycorrhizal controls were also included. Substrate conditions included three levels of nitrogen – phosphorus ratios, ranging from N limitation to P limitation (N/P ratio 5.4, 16.2, 48.6), and three pH's, ranging from acidic to alkaline (pH 4, 5.5, 7), in a full factorial experiment. Plant parameters (carbon gain, N and P-content, root length) were significantly affected by fungus, soil pH and soil N/P, and their interactions. Mycorrhizal benefits by ectomycorrhizal fungi (EcMF) were generally larger than by the arbuscular mycorrhizal fungi (AMF), when assessed by above-ground parameters. Glomus mosseae, despite low colonization, had a much larger positive effect on root length than those EcMF. Hebeloma leucosarx and P. involutus were equally effective, despite differences in proportional colonization. Hebeloma leucosarx was able to expand niche width of S. repens towards alkaline conditions. Results are discussed in the framework of a dune successional gradient from young, calcareous, humus-poor towards old, acidic, humus-rich soils.     

Effects of tail autotomy on survival,growth and territory occupation in free‐ranging juvenile geckos (Oedura lesueurii)

Abstract Many animals autotomize their tails to facilitate escape from predators. Although tail autotomy can increase the likelihood of surviving a predatory encounter, it may entail subsequent costs, including reduced growth, loss of energy stores, a reduction in reproductive output, loss of social status and a decreased probability of survival during subsequent encounters with predators. To date, few studies have investigated the potential fitness costs of tail autotomy in natural populations. I investigated whether tail loss influenced survival, growth and territory occupation of juvenile velvet geckos Oedura lesueurii in a population where predatory snakes were common. During the 3‐year mark–recapture study, 32% of juveniles voluntarily autotomized their tails when first captured. Analysis of survival using the program mark showed that voluntary tail autotomy did not influence the subsequent survival of juvenile geckos. Survival was age‐dependent and was higher in 1‐year‐old animals (0.98) than in hatchlings (0.76), whereas recapture probabilities were time‐dependent. Growth rates of tailed and tailless juveniles were very similar, but tailless geckos had slow rates of tail regeneration (0.14 mm day⁻¹). Tail autotomy did not influence rock usage by geckos, and both tailed and tailless juveniles used few rocks as diurnal retreat sites (means of 1.64 and 1.47 rocks, respectively) and spent long time periods (85 and 82 days) under the same rocks. Site fidelity may confer survival advantages to juveniles in populations sympatric with ambush foraging snakes. My results show that two potential fitness costs of tail autotomy – decreased growth rates and a lower probability of survival – did not occur in juveniles from this population. However, compared with juveniles, significantly fewer adult geckos (17%) voluntarily autotomized their tails during capture. Because adults possess large tails that are used for lipid storage, the energetic costs of tail autotomy are likely to be much higher in adult than in juvenile O. lesueurii.     

Histories of host shifts and cospeciation among free‐living parasitoids of Rhagoletis flies

Host shifts by specialist insects can lead to reproductive isolation between insect populations that use different hosts, promoting diversification. When both a phytophagous insect and its ancestrally associated parasitoid shift to the same novel host plant, they may cospeciate. However, because adult parasitoids are free living, they can also colonize novel host insects and diversify independent of their ancestral host insect. Although shifts of parasitoids to new insect hosts have been documented in ecological time, the long‐term importance of such shifts to parasitoid diversity has not been evaluated. We used a genus of flies with a history of speciation via host shifting (Rhagoletis [Diptera: Tephritidae]) and three associated hymenopteran parasitoid genera (Diachasma, Coptera and Utetes) to examine cophylogenetic relationships between parasitoids and their host insects. We inferred phylogenies of Rhagoletis, Diachasma, Coptera and Utetes and used distance‐based cophylogenetic methods (ParaFit and PACo) to assess congruence between fly and parasitoid trees. We used an event‐based method with a free‐living parasitoid cost model to reconstruct cophylogenetic histories of each parasitoid genus and Rhagoletis. We found that the current species diversity and host–parasitoid associations between the Rhagoletis flies and parasitoids are the primary result of ancient cospeciation events. Parasitoid shifts to ancestrally unrelated hosts primarily occur near the branch tips, suggesting that host shifts contribute to recent parasitoid species diversity but that these lineages may not persist over longer time periods. Our analyses also stress the importance of biologically informed cost models when investigating the coevolutionary histories of hosts and free‐living parasitoids.     

Responses of plant community mycorrhization to anthropogenic influence depend on the habitat and mycorrhizal type

Anthropogenic impact represents a major pressure on ecosystems, yet little is known about how it affects symbiotic relationships, such as mycorrhizal symbiosis, which plays a crucial role in ecosystem functioning. We analyzed the effects of three human impact types – increasing urbanity, introduction of alien plant species (alienness) and modifications in plant species distribution ranges (as a proxy for naturalness) – on plant community overall mycorrhization (including arbuscular, ecto‐, ericoid and orchid mycorrhizal plants) and arbuscular mycorrhization (indicating the degree of forming mycorrhizal symbiosis at plant community level using the relative abundance of mycorrhizal and arbuscular mycorrhizal plants, respectively). The study was carried out in three habitat types, each dominated by a distinct mycorrhizal type – ectomycorrhizal woodlands, ericoid mycorrhizal heathlands and arbuscular mycorrhizal grasslands – at the regional scale in the Netherlands. The response of community mycorrhization and arbuscular mycorrhization to anthropogenic influence showed contrasting patterns, depending on the specific aspect of human impact. Community mycorrhization responded negatively to urbanity and positively to increasing alienness, while arbuscular mycorrhization showed the reverse trend. More natural heathlands were found to be more mycorrhizal and less arbuscular mycorrhizal. The strongest responses were detected in woodlands and heathlands, while mycorrhization in grasslands was relatively insensitive to human impact. Our study highlights the importance of considering mycorrhizal symbiosis in understanding and quantifying the effects of anthropogenic influence on plant communities, especially in woodlands and heathlands.     

Dosage and duration effects of nitrogen additions on ectomycorrhizal sporocarp production and functioning: an example from two N‐limited boreal forests

1. Although it is well known that nitrogen (N) additions strongly affect ectomycorrhizal (EM) fungal community composition, less is known about how different N application rates and duration of N additions affect the functional role EM fungi play in the forest N cycle.
2. We measured EM sporocarp abundance and species richness as well as determined the δ¹⁵N in EM sporocarps and tree foliage in two Pinus sylvestris forests characterized by short- and long-term N addition histories and multiple N addition treatments. After 20 and 39 years of N additions, two of the long-term N addition treatments were terminated, thereby providing a unique opportunity to examine the temporal recovery of EM sporocarps after cessation of high N loading.
3. In general, increasing N availability significantly reduced EM sporocarp production, species richness, and the amount of N retained in EM sporocarps. However, these general responses were strongly dependent on the application rate and duration of N additions. The annual addition of 20 kg·N·ha⁻¹ for the past 6 years resulted in a slight increase in the production and retention of N in EM sporocarps, whereas the addition of 100 kg·N·ha⁻¹·yr⁻¹ during the same period nearly eliminated EM sporocarps. In contrast, long-term additions of N at rates of ca. 35 or 70 kg·N·ha⁻¹·yr⁻¹ for the past 40 years did not eliminate tree carbon allocation to EM sporocarps, although there was a decrease in the abundance and a shift in the dominant EM sporocarp taxa. Despite no immediate recovery, EM sporocarp abundance and species richness approached those of the control 20 years after terminating N additions in the most heavily fertilized treatment, suggesting a recovery of carbon allocation to EM sporocarps after cessation of high N loading.
4. Our results provide evidence for a tight coupling between tree carbon allocation to and N retention in EM sporocarps and moreover highlight the potential use of δ¹⁵N in EM sporocarps as a relative index of EM fungal sink strength for N. However, nitrogen additions at high dosage rates or over long time periods appear to disrupt this feedback, which could have important ramifications on carbon and nitrogen dynamics in these forested ecosystems.

     

Aromatic residues in RNase T stack with nucleobases to guide the sequence‐specific recognition and cleavage of nucleic acids

RNase T is a classical member of the DEDDh family of exonucleases with a unique sequence preference in that its 3′‐to‐5′ exonuclease activity is blocked by a 3′‐terminal dinucleotide CC in digesting both single‐stranded RNA and DNA. Our previous crystal structure analysis of RNase T‐DNA complexes show that four phenylalanine residues, F29, F77, F124, and F146, stack with the two 3′‐terminal nucleobases. To elucidate if the π–π stacking interactions between aromatic residues and nucleobases play a critical role in sequence‐specific protein–nucleic acid recognition, here we mutated two to four of the phenylalanine residues in RNase T to tryptophan (W mutants) and tyrosine (Y mutants). The Escherichia coli strains expressing either the W mutants or the Y mutants had slow growth phenotypes, suggesting that all of these mutants could not fully substitute the function of the wild‐type RNase T in vivo. DNA digestion assays revealed W mutants shared similar sequence specificity with wild‐type RNase T. However, the Y mutants exhibited altered sequence‐dependent activity, digesting ssDNA with both 3′‐end CC and GG sequences. Moreover, the W and Y mutants had reduced DNA‐binding activity and lower thermal stability as compared to wild‐type RNase T. Taken together, our results suggest that the four phenylalanine residues in RNase T not only play critical roles in sequence‐specific recognition, but also in overall protein stability. Our results provide the first evidence showing that the π−π stacking interactions between nucleobases and protein aromatic residues may guide the sequence‐specific activity for DNA and RNA enzymes.     

Bottom‐up effects of glucosinolate variation on aphid colony dynamics in wild cabbage populations

1. There is an ongoing debate about the relative importance of top‐down and bottom‐up regulation of herbivore dynamics in the wild. Secondary metabolites, produced by plants, have negative effects on survival and growth of some herbivore species, causing bottom‐up regulation of population dynamics. Herbivore natural enemies may use plant secondary metabolites as cues to find their prey, but their survival and reproduction can also be influenced by the upward cascade of secondary metabolites through the food web. Thus plant chemistry might also affect herbivore populations by mediating top‐down regulation. 2. We investigated the influence of heritable variation in aliphatic glucosinolates, a class of secondary metabolites produced by Brassica plants, on the relative importance of top‐down and bottom‐up regulation of Brevicoryne brassicae (mealy cabbage aphid) colonies in natural Brassica oleracea (wild cabbage) populations. We manipulated natural enemy pressure on plants differing in their glucosinolate profiles, and monitored aphid colony growth and disperser production. 3. Aphid colony sizes were significantly smaller on plants producing sinigrin, compared with plants producing alternative aliphatic glucosinolates. Aphid natural enemy numbers correlated with aphid colony size, but there was no additional effect of the plants' chemical phenotype on natural enemy abundance. Furthermore, experimental reduction of natural enemy pressure had no effect on aphid colony size or production of winged dispersers. 4. Our results provide evidence for glucosinolate‐mediated, bottom‐up regulation of mealy cabbage aphid colonies in natural populations, but we found no indication of top‐down regulation. We emphasise that more studies of these processes should focus on tritrophic interactions in the wild.     

Arthropod food webs in organic and conventional wheat farming systems of an agricultural long‐term experiment: a stable isotope approach

• 1 Agricultural intensification not only alters the structure of arthropod communities, but also may affect biotic interactions by altering the availability of basal resources. We analyzed variations in stable isotope ratios (¹⁵N/¹⁴N and ¹³C/¹²C) of fertilizers, plants, prey and generalist predators in organic and conventional farming systems in a long‐term agricultural experiment [DOK trial (bioDynamic, bioOrganic, Konventionell)]. Two basal resources with pronounced differences in carbon isotope signatures, wheat litter (C₃ plant) and maize litter (C₄ plant), were used to uncover differences in food web properties between the two farming systems (conventional versus organic).
• 2 Predators incorporated significantly higher proportions of carbon from wheat sources in organically managed fields, suggesting that they were more closely linked to wheat‐consuming prey in this system. The δ¹⁵N values of three predaceous species were more than 2‰ greater in summer than in spring.
• 3 The results obtained suggest that generalist predators consumed higher proportions of herbivore prey in the organic system and that starvation and intraguild predation rates increased in some predator species with time.
• 4 Because the effects of farming system and sampling date on predators were species‐specific, conserving a diverse natural enemy community including species with different phenologies and sensitivities to management practices may, in the long term, be a good strategy for maintaining high pest suppression throughout the growing season.

     

Co‐occurrence dynamics of endangered Lower Keys marsh rabbits and free‐ranging domestic cats: Prey responses to an exotic predator removal program

The Lower Keys marsh rabbit (Sylvilagus palustris hefneri) is one of many endangered endemic species of the Florida Keys. The main threats are habitat loss and fragmentation from sea‐level rise, development, and habitat succession. Exotic predators such as free‐ranging domestic cats (Felis catus) pose an additional threat to these endangered small mammals. Management strategies have focused on habitat restoration and exotic predator control. However, the effectiveness of predator removal and the effects of anthropogenic habitat modifications and restoration have not been evaluated. Between 2013 and 2015, we used camera traps to survey marsh rabbits and free‐ranging cats at 84 sites in the National Key Deer Refuge, Big Pine Key, Florida, USA. We used dynamic occupancy models to determine factors associated with marsh rabbit occurrence, colonization, extinction, and the co‐occurrence of marsh rabbits and cats during a period of predator removal. Rabbit occurrence was positively related to freshwater habitat and patch size, but was negatively related to the number of individual cats detected at each site. Furthermore, marsh rabbit colonization was negatively associated with relative increases in the number of individual cats at each site between survey years. Cat occurrence was negatively associated with increasing distance from human developments. The probability of cat site extinction was positively related to a 2‐year trapping effort, indicating that predator removal reduced the cat population. Dynamic co‐occurrence models suggested that cats and marsh rabbits co‐occur less frequently than expected under random conditions, whereas co‐detections were site and survey‐specific. Rabbit site extinction and colonization were not strongly conditional on cat presence, but corresponded with a negative association. Our results suggest that while rabbits can colonize and persist at sites where cats occur, it is the number of individual cats at a site that more strongly influences rabbit occupancy and colonization. These findings indicate that continued predator management would likely benefit endangered small mammals as they recolonize restored habitats.