Host Growth Rate Research Articles

The scaling of total parasite biomass with host body mass

The selective pressure exerted by parasites on their hosts will to a large extent be influenced by the abundance or biomass of parasites supported by the hosts. Predicting how much parasite biomass can be supported by host individuals or populations should be straightforward: ultimately, parasite biomass must be controlled by resource supply, which is a direct function of host metabolism. Using comparative data sets on the biomass of metazoan parasites in vertebrate hosts, we determined how parasite biomass scales with host body mass. If the rate at which host resources are converted into parasite biomass is the same as that at which host resources are channelled toward host growth, then on a log–log plot parasite biomass should increase with host mass with a slope of 0.75 when corrected for operating temperature. Average parasite biomass per host scaled with host body mass at a lower rate than expected (across 131 vertebrate species, slope = 0.54); this was true independently of phylogenetic influences and also within the major vertebrate groups separately. Since most host individuals in a population harbour a parasite load well below that allowed by their metabolic rate, because of the stochastic nature of infection, it is maximum parasite biomass, and not average biomass, that is predicted to scale with metabolic rate among host species. We found that maximum parasite biomass scaled isometrically (i.e., slope = 1) with host body mass. Thus, larger host species can potentially support the same parasite biomass per gram of host tissues as small host species. The relationship found between maximum parasite biomass and host body mass, with its slope greater than 0.75, suggests that parasites are not like host tissues: they are able to appropriate more host resources than expected from metabolically derived host growth rates.

Establishment success of sooty beech scale insects, Ultracoelostoma sp., on different host tree species in New Zealand

The sooty beech scale insect (Ultracoelostoma sp.) (Hemiptera: Margarodidae) exhibits a highly patchy distribution at local and regional scales. A major factor driving this common distributional phenomenon in other phloem-feeding insects is aggregation and local adaptation. The aim of this study was to determine if Ultracoelostoma was locally adapted to its natal host trees, by contrasting the establishment rates of first instar “crawlers” in reciprocal transfers to natal versus novel hosts. Although there are two closely-related species of sooty beech scale insect, the morphological characters of crawlers in this study were intermediate between those of U. assimile and U. brittini. However, all of the voucher specimens examined had consistent morphology, indicating that they belong to one species which we refer to as Ultracoelostoma sp. Reciprocal transfers of crawlers were carried out between individual red beech (Nothofagus fusca), as well as between mountain beech (N. solandri) and red beech trees, to ascertain if insects had become locally adapted to their individual host tree or to host species. In total, 480 crawlers were placed in enclosures on their natal and novel host trees, of which only 32 (6.7 %) became established. No evidence for local adaptation, either to individual host trees or to host tree species, was found. There was also no difference in crawler establishment between natal and novel hosts. However, crawlers originating from mountain beech trees had significantly higher establishment rates on both natal mountain beech and novel red beech hosts, than did crawlers originating from red beech trees. The superior ability of mountain beech crawlers to become established, even on novel red beech trees, suggests that scale insects on mountain beech trees have higher individual fitness (possibly due to maternal effects mediated by differences in host nutritional quality, defensive compounds or growth rate). This increased fitness may result in crawlers being better provisioned to search for appropriate establishment sites. The results of this study indicate that beech scale insects perform better on mountain beech at this site, although crawlers did not preferentially establish on mountain beech.

Host physiological status determines phage-like particle distribution in the lysate

Bacteriophage morphotype diversity and latent period duration upon induction were correlated with the host population growth. The prophages of the lysogenic Vibrio sp. (DSM14379) were induced with mitomycin C in a batch culture with different salinity, substrate concentration or composition, and at different temperatures. Under all experimental conditions, phages were induced and a population of different complete and incomplete phage-like particles was observed in the lysate. Under favorable growth conditions, the phage-like particle community in the lysate was overpopulated with phage tail-like rigid rods. The number of rods was reduced in samples with low organic carbon concentration, samples with 8% and 10% NaCl, and samples induced at 40 and 43 degrees C. Although all lysates contained all phage-like particle-size fractions, their relative abundances varied. Up to a fivefold difference in phage-like particle size was observed in lysates. Size distribution of phage-like particles changed along temperature, salinity and organic carbon gradients. Results also indicated that the latent period of the induced phage-like particle population converged to approximately 90 min above a growth rate of 1.0 h(-1). At lower host growth rates, the latent period generally increased. However, at 40 and 43 degrees C and at low peptone-yeast extract concentration in the growth medium, the latent period remained short. We propose that different host physiological conditions influence organic matter composition upon prophage induction and may thus affect virus-controlled flow of the energy and carbon in the ecosystem.

Effects of asymmetric dispersal and environmental gradients on the stability of host–parasitoid systems

We consider host–parasitoid systems spatially distributed on a row of patches connected by dispersal. We analyze the effects of dispersal frequency, dispersal asymmetry, number of patches and environmental gradients on the stability of the host–parasitoid interactions. To take into account dispersal frequency, the hosts and parasitoids are allowed to move from one patch to a neighboring patch a certain number of times within a generation. When this number is high, aggregation methods can be used to simplify the proposed initial model into an aggregated model describing the dynamics of both the total host and parasitoid populations. We show that as the number of patches increases less asymmetric parasitoid dispersal rates are required for stability. We found that the ‘CV2>1 rule’ is a valid approximation for stability if host growth rate is low, otherwise the general condition of stability we establish should be preferred. Environmental variability along the row of patches is introduced as gradients on host growth rate and parasitoid searching efficiency. We show that stability is more likely when parasitoids move preferentially towards patches where they have high searching efficiency or when hosts go mainly to patches where they have a low growth rate.

Ant species confer different partner benefits on two neotropical myrmecophytes

The dynamics of mutualistic interactions involving more than a single pair of species depend on the relative costs and benefits of interaction among alternative partners. The neotropical myrmecophytes Cordia nodosa and Duroia hirsuta associate with several species of obligately symbiotic ants. I compared the ant partners of Cordia and Duroia with respect to two benefits known to be important in ant-myrmecophyte interactions: protection against herbivores provided by ants, and protection against encroaching vegetation provided by ants. Azteca spp., Myrmelachista schumanni, and Allomerus octoarticulatus demerarae ants all provide the leaves of Cordia and Duroia some protection against herbivores. However, Azteca and Allomerus provide more protection than does Myrmelachista to the leaves of their host plants. Although Allomerus protects the leaves of its hosts, plants occupied by Allomerus suffer more attacks by herbivores to their stems than do plants occupied by other ants. Relative to Azteca or Allomerus, Myrmelachista ants provide better protection against encroaching vegetation, increasing canopy openness over their host plants. These differences in benefits among the ant partners of Cordia and Duroia are reflected in the effect of each ant species on host plant size, growth rate, and reproduction. The results of this study show how mutualistic ant partners can differ with respect to both the magnitude and type of benefits they provide to the same species of myrmecophytic host.

Parasites grow larger in faster growing fish hosts

Parasites depend on host-derived energy for growth and development, and so are potentially affected by the host's ability to acquire nutrients under competitive foraging scenarios. Although parasites might be expected to grow faster in hosts that are better at acquiring nutrients from natural ecosystems, it is also possible that the most competitive hosts are better at countering infections, if they have an improved immune response or are able to limit the availability of nutrients to parasites. I first quantified the ability of uninfected three-spined sticklebacks Gasterosteus aculeatus to compete in groups for sequentially-presented food items, and then exposed either the best or worst competitors to infective stages of the cestode Schistocephalus solidus. Fish were subsequently raised in their original groups, under competitive feeding regimes, for 96 days, after which fish and parasite growth was determined. Unexpectedly, pre-exposure host competitive ability had no effect on susceptibility to infection, or on post-infection growth rate. Furthermore, despite a 120-fold variation in parasite mass at the end of the study, pre-infection competitive ability was not related to parasite growth. The closest predictor of parasite mass was body size-corrected host growth rate, indicating that the fastest growing fish developed the largest parasites. Faster growing hosts therefore apparently provide ideal environments for growing parasites. This finding has important implications for ecology and aquaculture.

The impact of tree and stand characteristics on spruce beetle (Coleoptera: Scolytidae) induced mortality of white spruce in the Copper River Basin, Alaska

I examined the relationships between individual and stand-level characteristics of white spruce, Picea glauca (Moench) Voss, and the incidence of spruce beetle, Dendroctonus rufipennis Kirby, induced mortality. The study region, in the Kennicott Valley of the Copper River Basin, Alaska, has contained an active spruce beetle epidemic since 1989. I investigated the relationship among the individual traits of host age, size (diameter at breast height, DBH), and growth rate (basal area increment, BAI) and mortality from the spruce beetle. I also examined the effects of stand density, mean DBH, and mean BAI on percent mortality within plots. Survival was higher for younger, smaller, and faster-growing trees. However, the effect of age is not significant when included in a logistic regression model examining the effect of individual host traits on host survival. Mortality increased with increasing DBH and decreasing BAI, and there was a significant interaction between DBH and BAI. While the proportion of individuals killed by the spruce beetle significantly differed between stands, I found no significant relationships between stand-level characteristics and mortality rate. This research suggests that the individual traits of host size and growth rate, as well as their interaction are the best predictors of susceptibility to spruce beetle-induced mortality in this system.

Cockle Cerastoderma edule population mortality: role of the digenean parasite Himasthla quissetensis

Infection patterns of the digenean trematode Himasthla quissetensis in its second inter- mediate host, the edible cockle Cerastoderma edule, and the impact of this parasite on cockle popula- tions were quantified. A 2 yr transplant experiment and a 4 yr survey were conducted in Arcachon Bay, a coastal lagoon on the Atlantic SW coast of France. Cockles free of H. quissetensis were trans- planted at La Canelette, a station where cockles were usually highly infected. Infection began in May, when the water temperature reached 17°C and stopped in November (12°C). There was no new infec- tion between November and April. Monthly surveys at 2 stations, Arguin and La Canelette, confirmed that cockle infection by H. quissetensis occurred during the warmer period of the year. Only cockles with a shell length > 8 mm became infected; therefore, cockle growth rate, which differed at the 2 sta- tions, was also a key factor explaining infection phenology. In winter, the mean parasite abundance of H. quissetensis in cockles decreased at both stations. The mortality rate of parasites in cockles was very low, with no seasonal pattern, and did not explain this winter decrease. Consequently, the decrease of H. quissetensis was interpreted as mortality of heavily infected cockles. At Arguin, where the cockle population was characterised by moderate abundance, high growth rate and short lifespan, cockle mortality amounted to 93% during the first year of benthic life, with no significant contribution of parasites; in the following year (Year 2), cockle mortality was 85%, with 28% due to H. quissetensis infection. At La Canelette, the cockle population, characterised by low abundance and low growth rate, suffered almost 100% mortality in the first year, with no contribution by parasites, which started to infect cockles in the second year only; the remaining cockles had a long lifespan (up to 5 yr), and >46% of their mortality was linked to H. quissetensis infection. It is concluded that both host growth rate and water temperature are important factors in the initiation of parasite infection and that the intensity of infection and its effect on host mortality closely depend on host growth and environmental factors.

Gregarious Oviposition and Clutch Size Adjustment by a Heliconius Butterfly1

ABSTRACTFemale Heliconius hewitsoni butterflies were found to aggregate during oviposition, producing multi‐parent egg clutches. This behavior occurred when host plants were locally plentiful, indicating that females chose to oviposit gregariously. Collective clutch size correlated with host growth rate and with the number of females contributing to a clutch. Eggs did not positively bias host plant growth. Collective clutch size adjustment may represent a mechanism for facilitating larval aggregation while reducing intraspecific competition.

Ectoparasitism in marsh tits: costs and functional explanations

Among hole-nesting birds, the blood-sucking hen flea is a common parasite affecting both nestlings and parents. By adding fleas to marsh tit (Parus palustris) nests, I aimed to investigate the effect of fleas on nestling growth rate and parental effort as well as evaluating a potential mechanism by which fleas affect nestlings (i.e., resting metabolic rate; RMR). Nestlings from flea-infested broods were lighter than nestlings from control broods. This reduced growth rate was evident as soon as 3 days after adding extra fleas to the nest, but the reduction did not increase after this initial drop in mass. Parents did not alter their feeding frequency in response to the manipulation; thus the small size of nestlings in manipulated nests seems to be directly caused by the fleas. Mass-specific RMR was significantly higher in nestlings from flea-infested nests compared to nestlings from control nests. I used the results to evaluate the suggested mechanisms for parasite-related decrease in host growth rate. The increase in RMR and the very rapid reduction in nestling growth rate after experimental addition of fleas can be explained by an immune reaction, mainly by the innate immune system, to substances in the saliva of the fleas. (Less)

Coexistence in a Competitive Parasitoid-host System

The main objective of this work is to determine the conditions for coexistence and competitive exclusion in a discrete model for a community of three species: a stage-structured host and two competing parasitoids sharing the same host developmental stage. Coexistence of the community of the species is found to depend on the host life history parameters in the first place, and on competitive ability and parasitoid efficiency in the second place. In particular, parasitoids equilibrium densities are defined by the size of the refuge. Extinction is expected with low growth rate and with low adult survival. Host life histories are also associated with oscillations in population density, and depending on the combination of host adult survival from one generation to the next and host growth rate, the minimum of fluctuations approaches zero, implying a higher potential risk of extinction because of stochastic factors. Our results suggest that equally reduced survival of parasitoids in hosts parasitized by both species determines extinction of the parasitoid with lower population density, in contrast to the case when both parasitoids benefit with 50% of all doubly parasitized hosts, leading to the hypothesis that a community where competitors in multiparasitized hosts die, easily becomes extinct. Competitive exclusion is expected for highly asymmetric competitive interactions, independent of population densities, allowing us to hypothesize that coexistence of competitors in systems with limited resources and refuges is associated with a clearly defined competitive hierarchy.

HOST GROWTH CONDITIONS REGULATE THE PLASTICITY OF HORIZONTAL AND VERTICAL TRANSMISSION IN HOLOSPORA UNDULATA, A BACTERIAL PARASITE OF THE PROTOZOAN PARAMECIUM CAUDATUM

A parasite might be prohibited from investing simultaneously in horizontal (infection of new hosts) and vertical (infection of the current host's offspring) transmission because of developmental, physiological, or evolutionary costs and constraints. Rather, these constraints may select for adaptive phenotypic plasticity, where the parasite uses the transmission pathway that maximizes transmission in the current ecological and epidemiological conditions. By varying environmental conditions for the host's replication, we investigated the plasticity of vertical and horizontal transmission of Holospora undulata, a micronucleus-specific bacterial parasite of the protozoan Paramecium caudatum. We observed a negative correlation between the host's growth rate and the parasite's investment in horizontal transmission. In rapidly dividing hosts, the parasite remained in the reproductive stage and was passed on vertically to the daughter nuclei during mitotic division of the Paramecium. In contrast, at low or negative growth rates of the host, the parasite's reproductive forms differentiated into infectious forms, the agents of horizontal transmission. Furthermore, in treatments that were initiated with a high proportion of individuals harboring horizontally transmitted infectious forms, rapid replication resulted in a switch back from predominantly horizontal to almost exclusively vertical transmission. These results suggest a trade-off between the efficacies of vertical and horizontal transmission, with the parasite switching to horizontal transmission only if conditions for host replication, and thus vertical transmission, deteriorate.

Gregarious Oviposition and Clutch Size Adjustment by a Heliconius Butterfly1

Female Heliconius hewitsoni butterflies were found to aggregate during oviposition, producing multi-parent egg clutches. This behavior occurred when host plants were locally plentiful, indicating that females chose to oviposit gregariously. Collective clutch size correlated with host growth rate and with the number of females contributing to a clutch. Eggs did not positively bias host plant growth. Collective clutch size adjustment may represent a mechanism for facilitating larval aggregation while reducing intraspecific competition.

The Impact of Resource Limitation and the Phenology of Parasitoid Attack on the Duration of Insect Herbivore Outbreaks

Fluctuations in resource quality and quantity, and changes in mortality due to predators and parasites are thought to be of prime importance in the regular fluctuations of forest insects. We examine how food limitation and parasitoids with different phenologies of attack regulate the population cycles of insect hosts. Our analysis of the limit cycle of a model with a biologically realistic form of density dependence in the host yields two novel predictions. First, outbreaks will typically last for only 2 generations after parasitoids begin to reduce the host population below the maximum density. Second, host growth rate is important in determining cycle length only when parasitoids attack before the impacts of resource limitation affect the host. The robustness of these predictions are tested using a more general form of density dependence in the host, revealing that our predictions are valid as long as density dependence in the host is not too overcompensatory.

Geographical variations in infection by larval Anisakis simplex and Contracaecum osculatum (Nematoda, Anisakidae) in walleye pollock Theragra chalcogramma stocks off Hokkaido, Japan

: Stocks of walleye pollock Theragra chalcogramma collected from: (i) the Sea of Japan (off Rebun Island and Kumaishi); (ii) the Pacific coast (off Shikabe and eastern Hokkaido); and (iii) Nemuro Strait off Hokkaido, northern Japan, were examined for anisakid nematodes during December 1999 to February 2000, and the prevalence and abundance of Anisakis simplex and Contracaecum osculatum larvae were compared among the various sampling sites for fish of the same size and age. Anisakis simplex was generally more abundant than C. osculatum. Infection by A. simplex varied between the aforementioned stocks of walleye pollock as well as within stocks, whereby fish from off Rebun Island and Nemuro Strait were infected the most, followed by those from off the Pacific coast and Kumaishi. Infection by C. osculatum differed between the host stocks, and C. osculatum was the most abundant among the fish from Nemuro Strait. The infection variations seemed to be due to differences in host growth rate, host feeding habit, and the distribution of marine mammal final hosts. The results indicate that these two larval nematodes are useful biological indicators for the population study of walleye pollock in Japanese waters.

Effects of Escherichia coli physiology on growth of phage T7 in vivo and in silico.

Phage development depends not only upon phage functions but also on the physiological state of the host, characterized by levels and activities of host cellular functions. We established Escherichia coli at different physiological states by continuous culture under different dilution rates and then measured its production of phage T7 during a single cycle of infection. We found that the intracellular eclipse time decreased and the rise rate increased as the growth rate of the host increased. To develop mechanistic insight, we extended a computer simulation for the growth of phage T7 to account for the physiology of its host. Literature data were used to establish mathematical correlations between host resources and the host growth rate; host resources included the amount of genomic DNA, pool sizes and elongation rates of RNA polymerases and ribosomes, pool sizes of amino acids and nucleoside triphosphates, and the cell volume. The in silico (simulated) dependence of the phage intracellular rise rate on the host growth rate gave quantitatively good agreement with our in vivo results, increasing fivefold for a 2.4-fold increase in host doublings per hour, and the simulated dependence of eclipse time on growth rate agreed qualitatively, deviating by a fixed delay. When the simulation was used to numerically uncouple host resources from the host growth rate, phage growth was found to be most sensitive to the host translation machinery, specifically, the level and elongation rate of the ribosomes. Finally, the simulation was used to follow how bottlenecks to phage growth shift in response to variations in host or phage functions.

Parallel Acceleration of Evolutionary Rates in Symbiont Genes Underlying Host Nutrition

The overproduction of essential amino acids by Buchnera aphidicola, the primary bacterial mutualist of aphids, is considered an adaptation for increased production of nutrients that are lacking in aphids' diet of plant sap. Given their shared role in host nutrition, amino acid biosynthetic genes of Buchnera are expected to experience parallel changes in selection that depend on host diet quality, growth rate, and population structure. This study evaluates the hypothesis of parallel selection across biosynthetic pathways by testing for correlated changes in evolutionary rates at biosynthetic genes of Buchnera. Previous studies show fast evolutionary rates at tryptophan biosynthetic genes among Buchnera associated with the aphid genus Uroleucon and suggest reduced purifying selection on symbiont nutritional functions in this aphid group. Here, we test for parallel rate acceleration at other amino acid biosynthetic genes of Buchnera–Uroleucon, including those for leucine (leuABC) and isoleucine/valine biosynthesis (ilvC). Ratios of nonsynonymous to synonymous substitutions (dN/dS) were estimated using codon-based maximum-likelihood methods that account for the extreme AT compositional bias of Buchnera sequences. A significant elevation in dN/dS at biosynthetic loci but not at two housekeeping genes sampled (dnaN and tuf) suggests reduced host-level selection on biosynthetic capabilities of Buchnera–Uroleucon. In addition, the discovery of trpEG pseudogenes in Buchnera–U. obscurum further supports reduced selection on amino acid biosynthesis.

Parasite-induced variation in host morphology: brain-encysting trematodes in fathead minnows.

Metacercariae of the trematode Ornithodiplostomum ptychocheilus cause a conspicuous enlargement of the cranium of juvenile fathead minnows (Pimephales promelas). Minnows sampled from 2 naturally infected ponds in northern Alberta, Canada, had 12% higher and 7% wider craniums compared to fish from an adjacent, uninfected pond. We tested the prediction that cranial distortion was caused by encystment of metacercariae on the brains of slow-growing minnows in a factorial experiment. Juvenile fish were either exposed once to 120 cercariae or 3 times to 40 cercariae; they were then fed either a low- or high-quantity diet for 8 wk. Results showed that after controlling for host size, cranial heights were affected by infection regime and host diet but not by the infection x diet interaction. Cranial distortion was most prominent in minnows exposed once to cercariae, showing that the rapid, simultaneous growth of metacercariae interfered with the normal development of the cranium. Thus, the expression of the parasite-induced phenotype was context dependent, the result of factors associated with the dynamics of cercariae transmission and host growth rate.

A Parasitic Wasp (Eretmocerus mundus Mercet) Can Exploit Chemically Induced Delays in the Development Rates of Its Whitefly Host (Bemisia tabaci Genn.)

Sublethal plant defences, resulting in impaired growth of insect herbivores, may increase the impact of natural enemies upon those herbivores. This study examined whether such effects could be reproduced by chemically altering host growth rates. Fresh residues of piperonyl butoxide (a compound which slows growth in nymphs of the whitefly, Bemisia tabaci (Gennadius)) showed relatively little toxicity to adults and larvae of the parasitoid Eretmocerus mundus (Mercet), and once residues were 48 h old, they caused no discernible lethal or behavioral effects on adult wasps. Piperonyl butoxide had lethal effects on whitefly nymphs, but immature parasitoids continued to develop successfully in those hosts that survived. The hypothesis that slowing the growth rate of hosts might lead to increased parasitism by E. mundus was tested on large host populations in controlled temperature cabinets over two generations. On host populations of comparable size, highly significant increases in parasitism (7–8%, P < 0.0001) were observed. This work provides unique evidence that host growth rates can be artificially manipulated to confer advantage to parasitoids. The implications for biological control strategies and an understanding of plant allelochemical effects are discussed.

ClpP/ClpX-mediated degradation of the bacteriophage lambda O protein and regulation of lambda phage and lambda plasmid replication.

The O protein is a replication initiator that binds to the orilambda region and promotes assembly of the bacteriophage lambda replication complex. This protein, although protected from proteases by other elements of the replication complex, in a free form is rapidly degraded in the host, Escherichia coli, by the ClpP/ClpX protease. Nevertheless, the physiological role of this rapid degradation remains unclear. Here we demonstrate that the copy number of plasmids derived from bacteriophage lambda is significantly higher in wild-type cells growing in rich media than in slowly growing bacteria. However, lambda plasmid copy number in bacteria devoid of the ClpP/ClpX protease was not dependent on the bacterial growth rate and in all minimal media tested was comparable to that observed in wildtype cells growing in a rich medium. Contrary to lambda plasmid replication, the efficiency of lytic growth of bacteriophage lambda was found to be dependent on the host growth rate in both wild-type bacteria and clpP and clpX mutants. The activities of two major lambda promoters operating during the lytic development, p(R) and p(L), were found to be slightly dependent on the host growth rate. However, when p(R) activity was significantly decreased in the dnaA mutant, production of phage progeny was completely abolished at low growth rates. These results indicate that the O protein (whose level in E. coli cells depends on the activity of ClpP/ClpX protease) is a major limiting factor in the regulation of lambda plasmid replication at low bacterial growth rates. However, this protein seems to be only one of the limiting factors in the bacteriophage lambda lytic development under poor growth conditions of host cells. Therefore, it seems that the role of the rapid ClpP/ClpX-mediated proteolysis of the O protein is to decrease the efficiency of early DNA replication of the phage in slowly growing host cells.