Population dynamics of an infaunal polychaete: The effect of predators and an adult-recruit interaction

The effect of predation by fish and wading shore birds on the population dynamics of a nereid polychaete (Ceratonereis pseudoerythraeensis Hutchings & Turvey) was studied. The species occurs in high densities on the site studied probably owing to high nutrient input from a nearby sewage treatment farm. Predators were excluded from experimental areas with wire mesh cages. The effects of cage structures on predator behaviour, algal deposition and sediment depth and composition were studied, and the possibility that C. pseudoerythraeensis might migrate in or out of caged areas was experimentally tested. These effects appeared to be of minimal importance. Analyses of size classes of C. pseudoerythraeensis showed that the density of adult worms in control areas decreased relative to caged areas. This was attributed to predation, mainly by flounder and curlew sandpipers. Recruitment of juvenile C. pseudoerythraeensis was greater in control than caged treatments. The hypothesis that increased adult density decreases juvenile recruitment was confirmed by manipulating the densities of adults. The adult-recruit interaction effect apparently counter-balanced losses due to predators, so that if only the total densities of the polychaetes had been studied no effect of predation would have been apparent.     

Intraguild interactions between generalist predators and an introduced parasitoid of Glycaspis brimblecombei (Homoptera: Psylloidea)

Studies were conducted to evaluate potential impacts of generalist predators on the biological control of Glycaspis brimblecombei Moore (Homoptera: Psylloidea), a pest of eucalyptus trees in California, and its introduced parasitoid Psyllaephagus bliteus (Hymenoptera: Encyrtidae). Based on the results of the monitoring populations of G. brimblecombei and their natural enemies in inland and coastal California in the field, P. bliteus or Anthocoris nemoralis (Fabricius) (Heteroptera: Anthocoridae), alone or both species together were released into cages with G. brimblecombei to simulate predatory interference on the introduced parasitoid in the laboratory. Although coastal sites had higher densities of natural enemies as were percent parasitism and predation, the mean number of G. brimblecombei did not vary between inland and coastal sites. P. bliteus or A. nemoralis significantly reduced the psyllid densities in cages. However, when both species were together, the presence of A. nemoralis increased the parasitoid mortality relative to the mortality observed in the parasitoid-alone treatment. Moreover, the increase in parasitoid mortality was followed by the decrease in mortality of the psyllids. The current study also indicated that predation risk of parasitized hosts varies depending on the developmental stages of the psyllids.     

Prey or play: interactions between walruses and seabirds

Several anecdotal reports indicate that walruses (Odobenus rosmarus) occasionally attack seabirds, which potentially impacts local bird populations. However, the manner in which walruses interact with seabirds and the motivational basis of such interactions have not been investigated. Here, we describe and characterize the behaviour of wild Pacific walruses (O. r. divergens) directed at seabirds in water near the summer haulout in the Chukchi Sea. Although most walruses showed no interest in seabirds nearby, some individuals intentionally approached them both alone and in groups. A total of 74 seabird encounters for 71 individually identified walruses were registered. Behavioural analysis based on detailed observations, photography and video recording showed that the most common types of walrus behaviour toward a bird were approach by surfacing and splash, approach by surfacing and hit and attack from below. Immature individuals initiated 82% of encounters. The motivation to approach a bird was low in adult individuals, with the majority of encounters involving adults initiated by males. Walrus encounters with live birds showed a very low rate of bird kill. Encounters with dead birds were followed by further manipulations with bird carcasses, which included both the consumption of bird soft tissue and object play taking the form of drop–catch behaviour. In addition eight cases of the object-oriented play with a bird carcass in a group of walruses were observed. Object play in wild walruses is reported for the first time. Our results indicate that in seabird encounters, walruses display diverse behavioural patterns, not limited to predatory responses.     

Nest‐site characteristics,breeding success and competitive interactions between two recently sympatric apex predators

An influential period in avian life‐cycles is the annual breeding season, when competition over suitable nesting sites and territories is a key factor that can determine fitness and distribution, especially for species that are highly selective in their nesting habitats. We analysed nest‐site characteristics, breeding success and competitive interactions between two apex predator populations. Whereas the Short‐toed Eagle Circaetus gallicus has nested in the Judean Foothills (Israel) for a long time, the Long‐legged Buzzard Buteo rufinus has only invaded the nesting habitat of the Short‐toed Eagle during their breeding season in the last two decades. These two recently sympatric species have similar nesting ecology and frequently use the same nests. They are therefore expected to compete over nesting sites and territories. We analysed interspecific interactions between these two species by combining information from comprehensive observational, experimental, GIS analysis and remote sensing data, deriving 65 variables to characterize the nest‐sites used and the breeding success in 381 breeding attempts over four consecutive breeding seasons. To assess interspecific and intraspecific territorial behaviour and aggressiveness, stuffed Long‐legged Buzzards and Short‐toed Eagles were presented close to nests. Nest‐site characteristics overlapped substantially between species, and Long‐legged Buzzards occupied 21% of all Short‐toed Eagle nests. Intraspecific aggression rates among Long‐legged Buzzards were higher than their interspecific aggression rates with Short‐toed Eagles and also higher than intraspecific aggression among Short‐toed Eagles. Long‐legged Buzzard and Short‐toed Eagle breeding densities (1.59 ± 0.11 and 2.96 ± 0.11 pairs per 10 km², respectively) are likely to be the highest across their respective breeding distributions, with a maximum productivity of 0.96 ± 0.01 and 0.56 ± 0.05 (young fledged/breeding pair) for Long‐legged Buzzard and Short‐toed Eagle, respectively. Intraspecific interactions among both species play an important role in determining their breeding success and the spatial distribution of nesting sites. Our results suggest that interspecific competition over nesting sites and territories between both species, and the potential dominance of Long‐legged Buzzard, has both direct and indirect impacts on the spatial and demographic distribution of Short‐toed Eagles due to the recent establishment of Long‐legged Buzzard territories in the Judean breeding area.     

Spatial-temporal patterns in intra-annual gray whale foraging: Characterizing interactions between predators and prey in Clayquot Sound, British Columbia, Canada

In Clayquot Sound, British Columbia, gray whales (Eschrichtius robustus) forage primarily on mysids (Family Mysideae) and also on crab larvae (Family Porcellanidae) that are constrained to specific habitat, which relate to bathymetric depths. In this paper we characterize the interactions of gray whales and their prey by analyzing fine scale spatial‐temporal patterns in foraging gray whale distribution within a season. Kernel density estimators are applied to two seasons (1998 and 2002) of high‐resolution data on foraging by gray whales. By partitioning data from each foraging season into several time periods (12 in 1998 and 11 in 2002), using a temporal autocorrelation function, and generating kernel density estimated surfaces for each time period, it is possible to identify discrete areas of increasing and declining foraging effort. Our results indicate that gray whales forage on mysids throughout a season and opportunistically forage on crab larvae. The episodic crab larvae feeding may reduce, but not eliminate, pressure to mysid populations enabling mysids to reassemble swarms and continue to support gray whale foraging in the latter part of the season. Results suggest that when managing marine environments, gray whale populations require multiple and connected habitats for summer foraging.     

Effects of nutrients and predators on an old-field food chain: interactions of top-down and bottom-up processes

In theory, selection favours predators that select prey in order to maximise reproductive success. We studied the association between preference and performance of the generalist predator Orius laevigatus with respect to two prey species: spider mites ( Tetranychus urticae ) and western flower thrips ( Frankliniella occidentalis ). Under ample prey supply, the predators had higher maximum reproductive success (measured as intrinsic population growth rate r ) on thrips than on spider mites; hence thrips represent a higher prey quality to the bugs. This was at odds with the observed preference of the predatory bug for plants (patches) with high densities of spider mites to plants with moderate densities of thrips in release-recapture experiments. Thus, prey quality does not suffice to explain the preference of predators for plants with prey. The quality of a patch as an oviposition site (i.e. the number of eggs produced on a patch per bug per day) also did not match preference patterns. Hence, patch preference was not correlated to prey quality or oviposition rate on prey patches. However, patch productivity, i.e. the total number of offspring surviving until adulthood that can be produced by one female on a patch, was correlated with preference. This was further tested by offering the predators a choice between plants with high densities of spider mites and plants with high densities of thrips in an independent set of release-recapture experiments. These two types of prey patches were found equivalent in terms of patch productivity. Indeed, the predators showed no preference for either of the two types of patches, which is in agreement with our predictions. This suggests that the predatory bugs select patches based on patch productivity rather than on prey quality or oviposition rate on a patch.     

Large- and small-scale effects of habitat structure on rates of predation: how percent coverage of seagrass affects rates of predation and siphon nipping on an infaunal bivalve

Landscape ecology, predominantly a terrestrial discipline, considers the effect of large-scale (tens of meters to kilometers) spatial patterns of habitats on ecological processes such as competition, predation, and flow of energy. In this study, a landscape-ecology approach was applied to a marine soft-sediment environment to examine rates of predation and transfer of secondary production in and around vegetated habitats. Seagrass beds naturally occur in a variety of spatial configurations from patches 1–10s of meters across with interspersed unvegetated sediments (i.e., patchy coverage) to more continuous coverage with little or no bare sediment. I designed experiments to address how percent coverage of seagrass in a 100-m² area of seafloor, and the spatial arrangement (degree of patchiness or fragmentation) of an equal area (100 m²) of vegetation affected predation (lethal) and siphon nipping (sublethal) intensity on an infaunal bivalve, Mercenaria mercenaria (hard clam). Measures of seagrass density and biomass with different percent coverage of seagrass were also made. When clams were placed in both the vegetated and unvegetated portions of the seafloor nearly twice as many clams were recovered live with 99% seagrass cover than with 23% seagrass cover, while survivorship was intermediate with 70% cover. Cropping of clam siphons from both the vegetated and unvegetated sediments was also affected by the amount of seagrass cover in a 100-m² area of seafloor: mean adjusted siphon weights were approximately 76% heavier from the 99% seagrass cover treatment than from the 70% or 23% cover treatments. Survivorship of clams placed within an equal area of seagrass in very patchy, patchy, and continuous spatial configurations was 40% higher in the continuous seagrass treatment than in either of the two patchy treatments. This study demonstrates that transfer of secondary production in the form of predation and cropping on an infaunal organism is altered as the percent cover of seagrass changes. While large-scale changes in the amount and spatial patterning of vegetation may affect habitat utilization patterns and foraging HGLoopbehavior, increased seagrass density and biomass with increased percent coverage of seagrass limit any conclusions concerning predator foraging behavior and feeding success in response to patch shapes and sizes. Instead, local changes in seagrass characteristics provide the most compelling explanation for the observed results.     

Lethal interactions among vertebrate top predators: a review of concepts,assumptions and terminology

Lethal interactions among large vertebrate predators have long interested researchers because of ecological and conservation issues. Research focusing on lethal interactions among vertebrate top predators has used several terms with a broad sense, and also introduced new terminology. We analysed the published literature with reference to the main underlying concepts and the use of terminology and its ecological context. The most frequently used terms in the literature were ‘predation’, ‘intraguild predation’, ‘interference competition’, and ‘interspecific killing’. Most studies presented evidence of the killing of the victim (77%), but information regarding its consumption was not given in 48% of cases. More than half of the analysed studies (56%) had no solid information on the degree of competition between interacting species. By reviewing definitions and their underlying assumptions, we demonstrate that lethal interactions among large vertebrate predators could be designated using four terms—‘predation’, ‘intraguild predation’, ‘interspecific competitive killing’, and ‘superpredation’—without the need to employ additional terminology that may increase confusion and misuse. For a correct framework of these lethal interactions it is critical to assess if the kill is consumed, if the victim is indeed a competitor of the killer, and if the prey is a high‐order predator. However, these elements of the framework are simultaneously the most common constraints to studies of lethal interactions, since they often require a great effort to obtain. The proper use of terms and concepts is fundamental to understanding the causes behind lethal interactions and, ultimately, what is actually happening in these complex interactions.     

Anurans as prey: an exploratory analysis and size relationships between predators and their prey

The vertebrate predators of post-metamorphic anurans were quantified and the predator–prey relationship was investigated by analysing the relative size of invertebrate predators and anurans. More than 100 vertebrate predators were identified (in more than 200 reports) and classified as opportunistic, convenience, temporary specialized and specialized predators. Invertebrate predators were classified as solitary non-venomous, venomous and social foragers according to 333 reviewed reports. Each of these categories of invertebrate predators was compared with the relative size of the anurans, showing an increase in the relative size of the prey when predators used special predatory tactics. The number of species and the number of families of anurans that were preyed upon did not vary with the size of the predator, suggesting that prey selection was not arbitrary and that energetic constraints must be involved in this choice. The relatively low predation pressure upon brachycephalids was related to the presence of some defensive strategies of its species. This compounding review can be used as the foundation for future advances in vertebrate predator–prey interactions.     

No relevant cardiac, pharmacokinetic or safety interactions between roflumilast and inhaled formoterol in healthy subjects: an open-label, randomised, actively controlled study

Background

Roflumilast is an oral, selective phosphodiesterase 4 inhibitor with anti-inflammatory effects in chronic obstructive pulmonary disease (COPD). The addition of roflumilast to long-acting bronchodilators improves lung function in patients with moderate-to-severe COPD. The present study investigated drug-drug interaction effects between inhaled formoterol and oral roflumilast.

Methods

This was a single-centre (investigational clinic), open, randomised, multiple-dose, parallel-group study. In Regimen A, healthy men were treated with roflumilast (500 μg tablet once daily; Day 2-18) and concomitant formoterol (24 μg twice daily; Day 12-18). In Regimen B, healthy men were treated with formoterol (24 μg twice daily; Day 2-18) and concomitant roflumilast (500 μg once daily; Day 9-18). Steady-state plasma pharmacokinetics of roflumilast, roflumilast N-oxide and/or formoterol (C_max and AUC_0-τ) as well as pharmacodynamics - blood pressure, transthoracic impedance cardiography (ZCG), 12-lead digital electrocardiography, peripheral blood eosinophils, and serum glucose and potassium concentrations - were evaluated through Day 1 (baseline), Day 8 (Regimen B: formoterol alone) or Day 11 (Regimen A: roflumilast alone), and Day 18 (Regimen A and B: roflumilast plus formoterol). Blood and urine samples were taken for safety assessment at screening, pharmacokinetic profiling days and Day 19. Adverse events were monitored throughout the study.

Results

Of the 27 subjects enrolled, 24 were evaluable (12 in each regimen). No relevant pharmacokinetic interactions occurred. Neither roflumilast nor formoterol were associated with significant changes in cardiovascular parameters as measured by ZCG, and these parameters were not affected during concomitant administration. Formoterol was associated with a slight increase in heart rate and a corresponding shortening of the QT interval, without changes in the heart rate-corrected QTc interval. There were small effects on the other pharmacodynamic assessments when roflumilast and formoterol were administered individually, but no interactions or safety concerns were seen after concomitant administration. No severe or serious adverse events were reported, and no adverse events led to premature study discontinuation.

Conclusions

No clinically relevant pharmacokinetic or pharmacodynamic interactions were found when oral roflumilast was administered concomitantly with inhaled formoterol, including no effect on cardiac repolarisation. Roflumilast was well tolerated.

Trial Registration

Clinicaltrials.gov NCT00940329     

The role of semiochemicals in tritrophic interactions between the spruce bark beetle Ips typographus, its predators and infested spruce

Abstract:  Semiochemical interactions between the spruce bark beetle Ips typographus , its predators Medetera setiventris , Thanasimus formicarius and Thanasimus femoralis , and the host Norway spruce, Picea abies , were studied in the field. The chemicals S - cis -verbenol, 2-methyl-3-buten-2-ol, ipsdienol, (+)- α -pinene, (−)- α -pinene, (±)- α -pinene, limonene, camphor and their naturally occuring mixtures were used as trap baits in a multiple-choice design that allowed for comparison of their attractivity for the focal species. Medetera was attracted to both the prey aggregation pheromone and its multifunctional component, ipsdienol. On the contrary, both Thanasimus species responded predominantly to ipsdienol and less to the prey aggregation pheromone. In the case of I. typographus , the attractivity of aggregation pheromone seems to be increased by the addition of a mixture of monoterpenic tree volatiles, and by addition of ipsdienol. Bark beetles and predators showed species-specific responses to volatile mixtures representing different stages of tree decay and different stages of bark beetle colony establishment. These responses correlates with the optimal foraging habitat of each species. None of the predator species responded to 2-methyl-3-buten-2-ol, a substantial component of I. typographus pheromonal bouquet, thus it is hypothesized that only substances of monoterpenic origin attract predators.     

Electrostatic calculations for an ion channel. I. Energy and potential profiles and interactions between ions

The electrostatic energy profile of one, two, or three ions in an aqueous channel through a lipid membrane is calculated. It is shown that the previous solution to this problem (based on the assumption that the channel is infinitely long) significantly overestimates the electrostatic energy barrier. For example, for a 3-A radius pore, the energy is 16 kT for the infinite channel and 6.7 kT for an ion in the center of a channel 25 A long. The energy as a function of the position of the ion is also determined. With this energy profile, the rate of crossing the membrane (using the Nernst-Planck equation) was estimated and found to be compatible with the maximum conductance observed for the gramicidin A channel. The total electrostatic energy (as a function of position) required to place two or three ions in the channel is also calculated. The electrostatic interaction is small for two ions at opposite ends of the channel and large for any positioning of the three ions. Finally, the gradient through the channel of an applied potential is calculated. The solution to these problems is based on solving an equivalent problem in which an appropriate surface charge is placed on the boundary between the lipid and aqueous regions. The magnitude of the surface charge is obtained from the numerical solution for a system of coupled integral equations.     

Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids

1. Most communities of insect herbivores are unlikely to be structured by resource competition, but they may be structured by apparent competition mediated by shared natural enemies. 2. The potential of three guilds of natural enemies (parasitoids, fungal entomopathogens and predators) to influence aphid community structure through indirect interactions is assessed. Based on the biology, we predicted that the scope for apparent competition would be greatest for the predator and least for the parasitoid guilds. 3. Separate fully quantitative food webs were constructed for 3 years for the parasitoid guild, 2 years for the pathogen guild and for a single year for the predator guild. The webs were analysed using standard food web statistics designed for binary data, and using information-theory-based metrics that make use of the full quantitative data. 4. A total of 29 aphid, 24 parasitoid, five entomopathogenic fungi and 13 aphid specialist predator species were recorded in the study. Aphid density varied among years, and two species of aphid were particularly common in different years. Omitting these species, aphid diversity was similar among years. 5. The parasitoid web showed the lowest connectance while standard food web statistics suggested the pathogen and predator webs had similar levels of connectance. However, when a measure based on quantitative data was used the pathogen web was intermediate between the other two guilds. 6. There is evidence that a single aphid species had a particularly large effect on the structure of the pathogen food web. 7. The predator and pathogen webs were not compartmentalized, and the vast majority of parasitoids were connected in a single large compartment. 8. It was concluded that indirect effects are most likely to be mediated by predators, a prediction supported by the available experimental evidence.     

Gut bacteria may be involved in interactions between plants, herbivores and their predators: microbial biosynthesis of N-acylglutamine surfactants as elicitors of plant volatiles

N-Acylamino acids are dominant and widespread constituents of insect oral secretions (regurgitants), serving the insect as biosurfactants in the digestive process. During feeding the conjugates may be introduced into damaged leaves and contribute there to the elicitation of plant defenses such as the induction of volatile biosynthesis. From gut segments of Spodoptera exigua, Mamestra brassicae and Agrotis segetum 23 bacterial strains were isolated, ten of which were able to synthesise typical lepidopteran N-acylamino acids from externally added precursors. Four strains, Providencia rettgeri, Ochrobactrum spec., Myroides odoratus and Acinetobacter sp. genospecies 11 were identified on the basis of their 16 S rDNA. The organisms displayed a very broad substrate tolerance, since fatty acids of different chain length and different degree of saturation were converted into N-acylamino acids. Moreover, most of the proteinogenic amino acids, but not glutamic and aspartic acid, were used as substrates. The dominant occurrence of fatty acids conjugated with glutamine may result from a preferred transport of glutamine from the hemolymph into the gut of the insects. The involvement of bacteria in the biosynthesis of compounds which play a pivotal role in the interaction of plants, herbivores and their predators adds a new trophic level to this complex network of interactions. Due to their short generation cycle and the ease of adaptation endosymbiontic bacteria may have an outstanding importance for the coevolution of plant-insect interactions.     

Three-way interactions between mosquito population,viral strain and temperature underlying chikungunya virus transmission potential

Interactions between pathogens and their insect vectors in nature are under the control of both genetic and non-genetic factors, yet most studies on mosquito vector competence for human pathogens are conducted in laboratory systems that do not consider genetic and/or environmental variability. Evaluating the risk of emergence of arthropod-borne viruses (arboviruses) of public health importance such as chikungunya virus (CHIKV) requires a more realistic appraisal of genetic and environmental contributions to vector competence. In particular, sources of variation do not necessarily act independently and may combine in the form of interactions. Here, we measured CHIKV transmission potential by the mosquito Aedes albopictus in all combinations of six worldwide vector populations, two virus strains and two ambient temperatures (20°C and 28°C). Overall, CHIKV transmission potential by Ae. albopictus strongly depended on the three-way combination of mosquito population, virus strain and temperature. Such genotype-by-genotype-by-environment (G × G × E) interactions question the relevance of vector competence studies conducted with a simpler set of conditions. Our results highlight the need to account for the complex interplay between vectors, pathogens and environmental factors to accurately assess the potential of vector-borne diseases to emerge.     

Differential BBB interactions of three ingestive peptides: obestatin, ghrelin, and adiponectin

Endogenous compounds, including ingestive peptides, can interact with the blood-brain barrier (BBB) in different ways. Here we used in vivo and in vitro techniques to examine the BBB permeation of the newly described satiety peptide obestatin. The fate of obestatin in blood and at the BBB was contrasted with that of adiponectin. By the sensitive multiple time-regression method, obestatin appeared to have an extremely fast influx rate to the brain whereas adiponectin did not cross the BBB. HPLC analysis, however, showed the obestatin result to be spurious, reflecting rapid degradation. Absence of BBB permeation by obestatin and adiponectin was in contrast to the saturable transport of human ghrelin reported previously. As a positive control, ghrelin showed saturable binding and endocytosis in RBE4 cerebral microvessel endothelial cells. By comparison, obestatin lacked specific binding and endocytosis, and the small amount internalized showed rapid intracellular degradation before the radioactivity was released by exocytosis. The differential interactions of obestatin, adiponectin, and ghrelin with the BBB illustrate their distinctive physiological interactions with the CNS.     

Indirect interactions in a rice ecosystem: density dependence and the interplay between consumptive and non‐consumptive effects of predators

1. Density‐ and trait‐mediated indirect interactions (DMIIs and TMIIs, respectively) in food chains play crucial roles in community structure and processes. However, factors affecting the relative strength of these interactions are poorly understood, including in widespread and important freshwater rice ecosystems. 2. We studied the strength of DMIIs and TMIIs in a food chain involving a predator (the Reeve’s turtle Chinemys reevesii), its herbivorous prey (the apple snail Pomacea canaliculata) and a plant (rice Oryza sativa) in outdoor containers simulating rice fields. We also evaluated consumptive and non‐consumptive effects of the predator on the snail. We removed a fixed proportion of snails every 2 days to simulate prey consumption and introduced a caged turtle that was fed daily with snails to simulate non‐consumptive effects. 3. Direct consumptive effects increased growth of the remaining snails and their per capita feeding rate. Moreover, consumptive and non‐consumptive effects, and their interaction, affected the proportion of snails buried in the soil. This interaction was presumably because increasing food availability per snail induced their self‐burying behaviour. 4. Both DMIIs and TMIIs affected the number of rice plants remaining, whereas their interaction term was not significant. 5. In summary, density dependence and interactions between consumptive and non‐consumptive effects influenced snail growth and behaviour, respectively. However, no cascading effects of these complicated interactions on rice plants were detected.     

Local adaptation,evolutionary potential and host–parasite coevolution: interactions between migration,mutation, population size and generation time

Local adaptation of parasites to their sympatric hosts has been investigated on different biological systems through reciprocal transplant experiments. Most of these studies revealed a local adaptation of the parasite. In several cases, however, parasites were found to be locally maladapted or neither adapted nor maladapted. In the present paper, we try to determine the causes of such variability in these results. We analyse a host–parasite metapopulation model and study the effect of several factors on the emergence of local adaptation: population sizes, mutation rates and migration rates for both the host and the parasite, and parasite generation time. We show that all these factors may act on local adaptation through their effects on the evolutionary potential of each species. In particular, we find that higher numbers of mutants or migrants do, in general, promote local adaptation. Interestingly, shorter parasite generation time does not always favour parasite local adaptation. When genetic variability is limiting, shorter generation time, via an increase of the strength of selection, decreases the capacity of the parasite to adapt to an evolving host.