Discrete Cyclic di-GMP-Dependent Control of Bacterial Predation versus Axenic Growth in Bdellovibrio bacteriovorus

Bdellovibrio bacteriovorus is a Delta-proteobacterium that oscillates between free-living growth and predation on Gram-negative bacteria including important pathogens of man, animals and plants. After entering the prey periplasm, killing the prey and replicating inside the prey bdelloplast, several motile B. bacteriovorus progeny cells emerge. The B. bacteriovorus HD100 genome encodes numerous proteins predicted to be involved in signalling via the secondary messenger cyclic di-GMP (c-di-GMP), which is known to affect bacterial lifestyle choices. We investigated the role of c-di-GMP signalling in B. bacteriovorus, focussing on the five GGDEF domain proteins that are predicted to function as diguanylyl cyclases initiating c-di-GMP signalling cascades. Inactivation of individual GGDEF domain genes resulted in remarkably distinct phenotypes. Deletion of dgcB (Bd0742) resulted in a predation impaired, obligately axenic mutant, while deletion of dgcC (Bd1434) resulted in the opposite, obligately predatory mutant. Deletion of dgcA (Bd0367) abolished gliding motility, producing bacteria capable of predatory invasion but unable to leave the exhausted prey. Complementation was achieved with wild type dgc genes, but not with GGAAF versions. Deletion of cdgA (Bd3125) substantially slowed predation; this was restored by wild type complementation. Deletion of dgcD (Bd3766) had no observable phenotype. In vitro assays showed that DgcA, DgcB, and DgcC were diguanylyl cyclases. CdgA lacks enzymatic activity but functions as a c-di-GMP receptor apparently in the DgcB pathway. Activity of DgcD was not detected. Deletion of DgcA strongly decreased the extractable c-di-GMP content of axenic Bdellovibrio cells. We show that c-di-GMP signalling pathways are essential for both the free-living and predatory lifestyles of B. bacteriovorus and that obligately predatory dgcC- can be made lacking a propensity to survive without predation of bacterial pathogens and thus possibly useful in anti-pathogen applications. In contrast to many studies in other bacteria, Bdellovibrio shows specificity and lack of overlap in c-di-GMP signalling pathways.     

Prey bacteria shape the community structure of their predators

Although predator–prey interactions among higher organisms have been studied extensively, only few examples are known for microbes other than protists and viruses. Among the bacteria, the most studied obligate predators are the Bdellovibrio and like organisms (BALOs) that prey on many other bacteria. In the macroscopical world, both predator and prey influence the population size of the other''s community, and may have a role in selection. However, selective pressures among prey and predatory bacteria have been rarely investigated. In this study, Bacteriovorax, a predator within the group of BALOs, in environmental waters were fed two prey bacteria, Vibrio vulnificus and Vibrio parahaemolyticus. The two prey species yielded distinct Bacteriovorax populations, evidence that selective pressures shaped the predator community and diversity. The results of laboratory experiments confirmed the differential predation of Bacteriovorax phylotypes on the two bacteria species. Not only did Bacteriovorax Cluster IX exhibit the versatility to be the exclusive efficient predator on Vibrio vulnificus, thereby, behaving as a specialist, but was also able to prey with similar efficiency on Vibrio parahaemolyticus, indicative of a generalist. Therefore, we proposed a designation of versatilist for this predator. This initiative should provide a basis for further efforts to characterize the predatory patterns of bacterial predators. The results of this study have revealed impacts of the prey on Bacteriovorax predation and in structuring the predator community, and advanced understanding of predation behavior in the microbial world.     

Attracted to the enemy: Aedes aegypti prefers oviposition sites with predator-killed conspecifics

Oviposition habitat choices of species with aquatic larvae are expected to be influenced by both offspring risk of mortality due to predation, and offspring growth potential. Aquatic predators may indirectly influence growth potential for prey by reducing prey density and, for filter-feeding prey, by increasing bacterial food for prey via added organic matter (feces, partially eaten victims), creating the potential for interactive effects on oviposition choices. We tested the hypothesis that the mosquito Aedes aegypti preferentially oviposits in habitats with predatory Toxorhynchites larvae because of indirect effects of predation on chemical cues indicating bacterial abundance. We predicted that A. aegypti would avoid oviposition in sites with Toxorhynchites, but prefer to oviposit where bacterial food for larvae is abundant, and that predation by Toxorhynchites would increase bacterial abundances. Gravid A. aegypti were offered paired oviposition sites representing choices among: predator presence; the act of predation; conspecific density; dead conspecific larvae; and bacterial activity. A. aegypti preferentially oviposited in sites with Toxorhynchites theobaldi predation, and with killed conspecific larvae, but failed to detect preferences for other treatments. The antibiotic tetracycline eliminated the strongest oviposition preference. Both predation by Toxorhynchites and killed larvae increased bacterial abundances, suggesting that oviposition attraction is cued by bacteria. Our results show the potential for indirect effects, like trophic cascades, to influence oviposition choices and community composition in aquatic systems. Our results suggest that predators like Toxorhynchites may be doubly beneficial as biocontrol agents because of the attraction of ovipositing mosquitoes to bacterial by-products of Toxorhynchites feeding.     

Decomposing Predation: Testing for Parameters that Correlate with Predatory Performance by a Social Bacterium

Predator–prey interactions presumably play major roles in shaping the composition and dynamics of microbial communities. However, little is understood about the population biology of such interactions or how predation-related parameters vary or correlate across prey environments. Myxococcus xanthus is a motile soil bacterium that feeds on a broad range of other soil microbes that vary greatly in the degree to which they support M. xanthus growth. In order to decompose predator–prey interactions at the population level, we quantified five predation-related parameters during M. xanthus growth on nine phylogenetically diverse bacterial prey species. The horizontal expansion rate of swarming predator colonies fueled by prey lawns served as our measure of overall predatory performance, as it incorporates both the searching (motility) and handling (killing and consumption of prey) components of predation. Four other parameters—predator population growth rate, maximum predator yield, maximum prey kill, and overall rate of prey death—were measured from homogeneously mixed predator–prey lawns from which predator populations were not allowed to expand horizontally by swarming motility. All prey species fueled predator population growth. For some prey, predator-specific prey death was detected contemporaneously with predator population growth, whereas killing of other prey species was detected only after cessation of predator growth. All four of the alternative parameters were found to correlate significantly with predator swarm expansion rate to varying degrees, suggesting causal interrelationships among these diverse predation measures. More broadly, our results highlight the importance of examining multiple parameters for thoroughly understanding the population biology of microbial predation.     

Identifying inter‐ and intra‐guild feeding activity of an arthropod predator assemblage

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Assaying Predatory Feeding Behaviors in Pristionchus and Other Nematodes

This protocol provides multiple methods for the analysis and quantification of predatory feeding behaviors in nematodes. Many nematode species including Pristionchus pacificus display complex behaviors, the most striking of which is the predation of other nematode larvae. However, as these behaviors are absent in the model organism Caenorhabditis elegans, they have thus far only recently been described in detail along with the development of reliable behavioral assays ¹. These predatory behaviors are dependent upon phenotypically plastic but fixed mouth morphs making the correct identification and categorization of these animals essential. In P. pacificus there are two mouth types, the stenostomatous and eurystomatous morphs ², with only the wide mouthed eurystomatous containing an extra tooth and being capable of killing other nematode larvae. Through the isolation of an abundance of size matched prey larvae and subsequent exposure to predatory nematodes, assays including both "corpse assays" and "bite assays" on correctly identified mouth morph nematodes are possible. These assays provide a means to rapidly quantify predation success rates and provide a detailed behavioral analysis of individual nematodes engaged in predatory feeding activities. In addition, with the use of a high-speed camera, visualization of changes in pharyngeal activity including tooth and pumping dynamics are also possible.     

By their genes ye shall know them: genomic signatures of predatory bacteria

Predatory bacteria are taxonomically disparate, exhibit diverse predatory strategies and are widely distributed in varied environments. To date, their predatory phenotypes cannot be discerned in genome sequence data thereby limiting our understanding of bacterial predation, and of its impact in nature. Here, we define the ‘predatome,'' that is, sets of protein families that reflect the phenotypes of predatory bacteria. The proteomes of all sequenced 11 predatory bacteria, including two de novo sequenced genomes, and 19 non-predatory bacteria from across the phylogenetic and ecological landscapes were compared. Protein families discriminating between the two groups were identified and quantified, demonstrating that differences in the proteomes of predatory and non-predatory bacteria are large and significant. This analysis allows predictions to be made, as we show by confirming from genome data an over-looked bacterial predator. The predatome exhibits deficiencies in riboflavin and amino acids biosynthesis, suggesting that predators obtain them from their prey. In contrast, these genomes are highly enriched in adhesins, proteases and particular metabolic proteins, used for binding to, processing and consuming prey, respectively. Strikingly, predators and non-predators differ in isoprenoid biosynthesis: predators use the mevalonate pathway, whereas non-predators, like almost all bacteria, use the DOXP pathway. By defining predatory signatures in bacterial genomes, the predatory potential they encode can be uncovered, filling an essential gap for measuring bacterial predation in nature. Moreover, we suggest that full-genome proteomic comparisons are applicable to other ecological interactions between microbes, and provide a convenient and rational tool for the functional classification of bacteria.     

Killing of Escherichia coli by Myxococcus xanthus in Aqueous Environments Requires Exopolysaccharide-Dependent Physical Contact

Nutrient or niche-based competition among bacteria is a widespread phenomenon in the natural environment. Such interspecies interactions are often mediated by secreted soluble factors and/or direct cell–cell contact. As ubiquitous soil bacteria, Myxococcus species are able to produce a variety of bioactive secondary metabolites to inhibit the growth of other competing bacterial species. Meanwhile, Myxococcus spp. also exhibit sophisticated predatory behavior, an extreme form of competition that is often stimulated by close contact with prey cells and largely depends on the availability of solid surfaces. Myxococcus spp. can also be isolated from aquatic environments. However, studies focusing on the interaction between Myxococcus and other bacteria in such environments are still limited. In this study, using the well-studied Myxococcus xanthus DK1622 and Escherichia coli as model interspecies interaction pair, we demonstrated that in an aqueous environment, M. xanthus was able to kill E. coli in a cell contact-dependent manner and that the observed contact-dependent killing required the formation of co-aggregates between M. xanthus and E. coli cells. Further analysis revealed that exopolysaccharide (EPS), type IV pilus, and lipopolysaccharide mutants of M. xanthus displayed various degrees of attenuation in E. coli killing, and it correlated well with the mutants' reduction in EPS production. In addition, M. xanthus showed differential binding ability to different bacteria, and bacterial strains unable to co-aggregate with M. xanthus can escape the killing, suggesting the specific nature of co-aggregation and the targeted killing of interacting bacteria. In conclusion, our results demonstrated EPS-mediated, contact-dependent killing of E. coli by M. xanthus, a strategy that might facilitate the survival of this ubiquitous bacterium in aquatic environments.     

Antibiotic Production by Myxobacteria Plays a Role in Predation

Myxobacteria are predatory and are prolific producers of secondary metabolites. Here, we tested a hypothesized role that secondary metabolite antibiotics function as weapons in predation. To test this, a Myxococcus xanthus Δta1 mutant, blocked in antibiotic TA (myxovirescin) production, was constructed. This TA⁻ mutant was defective in producing a zone of inhibition (ZOI) against Escherichia coli. This shows that TA is the major M. xanthus-diffusible antibacterial agent against E. coli. Correspondingly, the TA⁻ mutant was defective in E. coli killing. Separately, an engineered E. coli strain resistant to TA was shown to be resistant toward predation. Exogenous addition of spectinomycin, a bacteriostatic antibiotic, rescued the predation defect of the TA⁻ mutant. In contrast, against Micrococcus luteus the TA⁻ mutant exhibited no defect in ZOI or killing. Thus, TA plays a selective role on prey species. To extend these studies to other myxobacteria, the role of antibiotic corallopyronin production in predation was tested and also found to be required for Corallococcus coralloides killing on E. coli. Next, a role of TA production in myxobacterial fitness was assessed by measuring swarm expansion. Here, the TA⁻ mutant had a specific swarm rate reduction on prey lawns, and thus reduced fitness, compared to an isogenic TA⁺ strain. Based on these observations, we conclude that myxobacterial antibiotic production can function as a predatory weapon. To our knowledge, this is the first report to directly show a link between secondary metabolite production and predation.     

Active predation,phylogenetic diversity,and global prevalence of myxobacteria in wastewater treatment plants

The operation of modern wastewater treatment plants (WWTPs) is driven by activated sludge microbiota, a complex assemblage of trophically interacting microorganisms. Microbial predation is crucial to fundamental understanding of how biological interactions drive microbiome structuring and functioning of WWTPs. However, predatory bacteria have received little attention regarding their diversity, activity, and ecological function in activated sludge, limiting the exploitation of food web interactions for wastewater microbiome engineering. Here, by using rRNA-stable isotope probing of activated sludge microbiota with ¹³C-labeled prey bacteria, we uncovered diverse as-yet-uncultivated putative predatory bacteria that actively incorporated ¹³C-biomass. Myxobacteria, especially Haliangium and the mle1-27 clade, were found as the dominant active predators, refreshing conventional views based on a few predatory isolates of Bdellovibrionota from WWTPs. The identified predatory bacteria showed more selective predation on prey compared with the protists dominated by ciliates, providing in situ evidence for inter-domain predation behavior divergence in activated sludge. Putative predatory bacteria were tracked over a two-year microbiome monitoring effort at a local WWTP, revealing the predominance of Myxococcota (6.5 ± 1.3%) over Bdellovibrionota (1.0 ± 0.2%) lineages. Phylogenetic analysis unveiled highly diverse myxobacteria inhabiting activated sludge and suggested a habitat filtering effect in global WWTPs. Further mining of a global activated sludge microbiome dataset revealed the prevalence of Myxococcota (5.4 ± 0.1%) species and potential impacts of myxobacterial predation on process performance. Collectively, our findings provided unique insights into the predating activity, diversity, and prevalence of Myxococcota species in activated sludge, highlighting their links with wastewater treatment processes via trophic regulation of enteric and functional bacteria.Subject terms: Microbial ecology, Biodiversity, Environmental microbiology, Microbial ecology, Environmental sciences     

Bdellovibrio Predation in the Presence of Decoys: Three-Way Bacterial Interactions Revealed by Mathematical and Experimental Analyses

Bdellovibrio bacteriovorus is a small, gram-negative, motile bacterium that preys upon other gram-negative bacteria, including several known human pathogens. Its predation efficiency is usually studied in pure cultures containing solely B. bacteriovorus and a suitable prey. However, in natural environments, as well as in any possible biomedical uses as an antimicrobial, Bdellovibrio is predatory in the presence of diverse decoys, including live nonsusceptible bacteria, eukaryotic cells, and cell debris. Here we gathered and mathematically modeled data from three-member cultures containing predator, prey, and nonsusceptible bacterial decoys. Specifically, we studied the rate of predation of planktonic late-log-phase Escherichia coli S17-1 prey by B. bacteriovorus HD100, both in the presence and in the absence of Bacillus subtilis nonsporulating strain 671, which acted as a live bacterial decoy. Interestingly, we found that although addition of the live Bacillus decoy did decrease the rate of Bdellovibrio predation in liquid cultures, this addition also resulted in a partially compensatory enhancement of the availability of prey for predation. This effect resulted in a higher final yield of Bdellovibrio than would be predicted for a simple inert decoy. Our mathematical model accounts for both negative and positive effects of predator-prey-decoy interactions in the closed batch environment. In addition, it informs considerations for predator dosing in any future therapeutic applications and sheds some light on considerations for modeling the massively complex interactions of real mixed bacterial populations in nature.     

Specialized Peptidoglycan Hydrolases Sculpt the Intra-bacterial Niche of Predatory Bdellovibrio and Increase Population Fitness

Bdellovibrio are predatory bacteria that have evolved to invade virtually all Gram-negative bacteria, including many prominent pathogens. Upon invasion, prey bacteria become rounded up into an osmotically stable niche for the Bdellovibrio, preventing further superinfection and allowing Bdellovibrio to replicate inside without competition, killing the prey bacterium and degrading its contents. Historically, prey rounding was hypothesized to be associated with peptidoglycan (PG) metabolism; we found two Bdellovibrio genes, bd0816 and bd3459, expressed at prey entry and encoding proteins with limited homologies to conventional dacB/PBP4 DD-endo/carboxypeptidases (responsible for peptidoglycan maintenance during growth and division). We tested possible links between Bd0816/3459 activity and predation. Bd3459, but not an active site serine mutant protein, bound β-lactam, exhibited DD-endo/carboxypeptidase activity against purified peptidoglycan and, importantly, rounded up E. coli cells upon periplasmic expression. A ΔBd0816 ΔBd3459 double mutant invaded prey more slowly than the wild type (with negligible prey cell rounding) and double invasions of single prey by more than one Bdellovibrio became more frequent. We solved the crystal structure of Bd3459 to 1.45 Å and this revealed predation-associated domain differences to conventional PBP4 housekeeping enzymes (loss of the regulatory domain III, alteration of domain II and a more exposed active site). The Bd3459 active site (and by similarity the Bd0816 active site) can thus accommodate and remodel the various bacterial PGs that Bdellovibrio may encounter across its diverse prey range, compared to the more closed active site that “regular” PBP4s have for self cell wall maintenance. Therefore, during evolution, Bdellovibrio peptidoglycan endopeptidases have adapted into secreted predation-specific proteins, preventing wasteful double invasion, and allowing activity upon the diverse prey peptidoglycan structures to sculpt the prey cell into a stable intracellular niche for replication.     

Measurement of Predation and Biofilm Formation under Different Ambient Oxygen Conditions Using a Simple Gasbag-Based System

Bdellovibrio bacteriovorus and Micavibrio aeruginosavorus are Gram-negative bacteria characterized by predatory behavior. The aim of this study was to evaluate the ability of the predators to prey in different oxygen environments. When placed on an orbital shaker, a positive association between the rate of aeration and predation was observed. To further examine the effects of elevated ambient oxygen levels on predation, a simple gasbag system was developed. Using the system, we were able to conduct experiments at ambient oxygen levels of 3% to 86%. When placed in gasbags and inflated with air, 50% O₂, and 100% O₂, positive predation was seen on both planktonic and biofilm-grown prey cells. However, in low-oxygen environments, predatory bacteria were able to attack only prey cells grown as biofilms. To further evaluate the gasbag system, biofilm development of Gram-positive and Gram-negative microorganisms was also measured. Although the gasbag system was found to be suitable for culturing bacteria that require a low-oxygen environment, it was not capable of supporting, with its current configuration, the growth of obligate anaerobes in liquid or agar medium.     

Widespread predatory abilities in the genus Streptomyces

The natural role of antibiotics in the ecology of Streptomyces is debated and still largely unknown. The predatory myxobacteria and many other genera of prokaryotic epibiotic and wolfpack predators across different taxa possess secondary metabolites with antimicrobial action, and these compounds have a role in predation. If all epibiotic predators are antibiotic producers, it is worth testing whether all antibiotic producers are predators too. We show here that Streptomyces are non-obligate epibiotic predators of other microorganisms and that predatory abilities are widespread in this genus. We developed a test for predatory activity which revealed that a large proportion of traditionally isolated Streptomyces strains and all oligophilic Streptomyces isolates show predatory activity. Those that did not show predatory ability on first challenge could do so after many generations of selection or acclimation. Using time-lapse photomicrography, we demonstrate that the growth of the tips of Streptomyces hyphae is accompanied by disappearance of cells of other bacteria in the vicinity presumably due to lysis. Predatory activity is restricted to surface growth and is not obligately associated with antibiotic production in conventional culture. However, some of the genes crucial to the regulation of secondary metabolite pathways are differentially expressed during predatory growth on different prey species as compared to saprophytic growth. Our findings strengthen the association between epibiotic predation and antibiotic production.     

Bacterial predator–prey dynamics in microscale patchy landscapes

Soil is a microenvironment with a fragmented (patchy) spatial structure in which many bacterial species interact. Here, we explore the interaction between the predatory bacterium Bdellovibrio bacteriovorus and its prey Escherichia coli in microfabricated landscapes. We ask how fragmentation influences the prey dynamics at the microscale and compare two landscape geometries: a patchy landscape and a continuous landscape. By following the dynamics of prey populations with high spatial and temporal resolution for many generations, we found that the variation in predation rates was twice as large in the patchy landscape and the dynamics was correlated over shorter length scales. We also found that while the prey population in the continuous landscape was almost entirely driven to extinction, a significant part of the prey population in the fragmented landscape persisted over time. We observed significant surface-associated growth, especially in the fragmented landscape and we surmise that this sub-population is more resistant to predation. Our results thus show that microscale fragmentation can significantly influence bacterial interactions.     

An Eye to a Kill: Using Predatory Bacteria to Control Gram-Negative Pathogens Associated with Ocular Infections

Ocular infections are a leading cause of vision loss. It has been previously suggested that predatory prokaryotes might be used as live antibiotics to control infections. In this study, Pseudomonas aeruginosa and Serratia marcescens ocular isolates were exposed to the predatory bacteria Micavibrio aeruginosavorus and Bdellovibrio bacteriovorus. All tested S. marcescens isolates were susceptible to predation by B. bacteriovorus strains 109J and HD100. Seven of the 10 P. aeruginosa isolates were susceptible to predation by B. bacteriovorus 109J with 80% being attacked by M. aeruginosavorus. All of the 19 tested isolates were found to be sensitive to at least one predator. To further investigate the effect of the predators on eukaryotic cells, human corneal-limbal epithelial (HCLE) cells were exposed to high concentrations of the predators. Cytotoxicity assays demonstrated that predatory bacteria do not damage ocular surface cells in vitro whereas the P. aeruginosa used as a positive control was highly toxic. Furthermore, no increase in the production of the proinflammatory cytokines IL-8 and TNF-alpha was measured in HCLE cells after exposure to the predators. Finally, injection of high concentration of predatory bacteria into the hemocoel of Galleria mellonella, an established model system used to study microbial pathogenesis, did not result in any measurable negative effect to the host. Our results suggest that predatory bacteria could be considered in the near future as a safe topical bio-control agent to treat ocular infections.     

Is It Necessary Managing Carnivores to Reverse the Decline of Endangered Prey Species? Insights from a Removal Experiment of Mesocarnivores to Benefit Demographic Parameters of the Pyrenean Capercaillie

Mesopredator control has long been used to alleviate the effect of elevated predation pressure on vulnerable, threatened or valuable species. However, the convenience of using mesopredator controls is technically questionable and scientifically-sound research is therefore required to evaluate the impact of predation on prey case by case. In this study we evaluated the effect of the alteration of terrestrial mesopredator dynamics on the demographic parameters of a relict capercaillie Tetrao urogallus aquitanicus population currently in decline for which the impact of predation has not previously been assessed. We used a six-year mesocarnivore removal experiment (2008–2013) together with seven-years of previous demographic information on capercaillies (1999–2007) within a before-after control-impact (BACI) design to evaluate the effect of mesocarnivore removal on capercaillie demographic parameters and on spatial behaviour of the most frequent predatory mesocarnivores of the capercaillie (Martes spp. and red fox Vulpes vulpes). Using a dynamic site-occupancy approach, the reduction of mesocarnivore population levels as a result of removal was clear for marten species, mainly during key months for capercaillie reproduction, but not for the red fox. Our results show that the breeding success of capercaillies was enhanced in areas where carnivores were removed and was inversely related to the occupation level of the studied mesocarnivores, although being only significant for Martes spp. Moreover, capercaillie predation rates were lower and adult survival seemingly higher in treatment during the removal phase. Cost-effective, long-term management interventions to ensure the recovery of this threatened capercaillie population are discussed in the light of the results. At our study area, the decision for implementing predation management should be included within a broader long-term conservation perspective. In this regard, a more feasible and sustainable management intervention in ecological and economic terms may be to balance the impact of mesocarnivores on capercaillies through the recovery of apex predators.     

Comparison of the predation capacities of two soil-dwelling predatory mites,Gaeolaelaps aculeifer and Stratiolaelaps scimitus (Acari: Laelapidae), on three thrips species

Soil-dwelling predatory mites are natural enemies of various soil pest insects and mites. Both Gaeolaelaps aculeifer (Canestrini) and Stratiolaelaps scimitus (Womersley) are commercialized natural enemies of thrips, but there is little information on the predation rate of these predatory mites on different thrips species. We compared their predation capacities on three thrips species, Frankliniella occidentalis, F. intonsa, and Thrips palmi, which are major pests of various horticultural plants. The predatory rate of G. aculeifer was higher than that of S. scimitus. Both predator species fed on more T. palmi thrips than F. occidentalis or F. intonsa thrips, which may be attributable to the smaller body size of T. palmi than the other thrips. Predation rates of female adults were 2.6–2.8 times higher than those of deutonymphs in both species. Predation rates were not separated according to the various developmental stages (i.e., second instar larva, pupa, or adult) of thrips; however, deutonymphs fed on fewer adults than larvae or pupae of F. occidentalis. Our results suggest that both G. aculeifer and S. scimitus are active predators that can prey during any of their developmental stages and on any species of thrips tested.     

An Analysis of Some Predatory Behaviour Patterns in Four Species of Carnivorous Marsupials (Dasyuridae), with Comparative Notes on the Eutherian Cat Felis catus

Two aspects of predatory behaviour in five species of carnivorous mammals were studied: four species (Dasyurus viverrinus, Dasyurus hallucatus, Dasyuroides byrnei and Phascogale tapoatafa) of a group of Australian marsupials, Dasyuridae, and an eutherian, the domestic cat, Felis catus. All data were collected from captive animals in laboratory conditions. Using sequences of predatory behaviour recorded on movie film, two aspects of predation were compared: (a) attack strategy, that is, the behavioural patterns leading up to biting the prey, and (2) head shaking movements used during killing. All individual predators of all species but Dasyuroides byrnei exhibited avoidance of attacking prey from the front. Indeed, two of the four individual Dasyuroides used not only did not avoid frontal attack but selected to do so even when attacks from the rear or side were possible (e.g., the prey sat unmoving in the centre of the enclosure). Frontal attacks by Dasyuroides involved the use of the forepaws to grasp and pin prey, and the directing of killing bites to the head. These two behaviour patterns are also present in the other three species of dasyurids. Therefore, the frontal attack employed by this species does not involve the use of novel behaviour patterns. Analysis of head shakes revealed two basic forms. From a downward pointing position the head was rotated in one of two ways: the snout traversed an arc in space, as seen in Felis catus and Dasyurus hallucatus, or the sagittal crest traversed an arc in space, as seen in the other three species of dasyurids. When the prey is held down by the forepaws, either form of head shake enhances penetration of the canines into the prey, whereas, when not held down by the forepaws, both forms of head shake can disorient prey, enabling subsequent killing bites to be applied.