Pea Aphid Populations Research Articles

Temperature effects on long‐term population dynamics in a parasitoid–host system

Long‐term environmental changes will likely alter the strengths of interactions between species and consequently their population dynamics, leading to changes in the stability of ecological systems. While an increasing number of empirical studies have shown that environmental changes can alter the strengths of species interactions, these studies are typically short (<1–2 generations) and therefore give only partial information about longer term population dynamics. To focus on longer term dynamics, we investigated population cycles of pea aphids and their most common parasitoid, Aphidius ervi, in Wisconsin, USA. Data collected over three years in alfalfa fields showed an apparent host–parasitoid population cycle. Furthermore, higher pea aphid population growth rates and increased parasitism were correlated with higher naturally occurring temperatures. While these effects were observed with seasonal fluctuations in temperature, they beg the question of how long‐term changes in mean annual temperature might change aphid–parasitoid population cycles, a question which we further pursued with laboratory experiments. To quantify temperature‐dependent demographic parameters, we used short‐term (<1 generation) experiments conducted at 20°C and 27°C. The higher temperature increased aphid and parasitoid development rates, adult aphid life span and fecundity, and parasitoid attack rates. We then conducted multi‐generation population‐level laboratory experiments to reveal the effects of temperature (20°C vs. 27°C) on population dynamics. We fit the resulting time series data using a nonlinear age‐structured state‐space model to estimate population‐level processes that could not be estimated in short‐term laboratory experiments. Using the model, we parsed out the demographic rates that had the largest impacts on aphid–parasitoid population cycles. This analysis showed that there were frequent contrasts in the effects of temperature operating through different demographic rates. For example, the temperature‐dependent increase in aphid development rate decreased cycle amplitude, while the increase in parasitoid attack rate increased cycle amplitude. There were also striking interactions among demographic rates. For example, the temperature‐dependent increase in aphid development rate could either increase or decrease the cycle period depending on the values of other demographic rates. Although these complexities make predictions difficult, overall they suggest that increasing long‐term mean temperature will decrease the period, increase the amplitude, and tend to destabilize pea aphid–A. ervi dynamics.

Inheritance patterns of secondary symbionts during sexual reproduction of pea aphid biotypes

Herbivorous insects frequently harbor bacterial symbionts that affect their ecology and evolution. Aphids host the obligatory endosymbiont Buchnera, which is required for reproduction, together with facultative symbionts whose frequencies vary across aphid populations. These maternally transmitted secondary symbionts have been particularly studied in the pea aphid, Acyrthosiphon pisum, which harbors at least 8 distinct bacterial species (not counting Buchnera) having environmentally dependent effects on host fitness. In particular, these symbiont species are associated with pea aphid populations feeding on specific plants. Although they are maternally inherited, these bacteria are occasionally transferred across insect lineages. One mechanism of such nonmaternal transfer is paternal transmission to the progeny during sexual reproduction. To date, transmission of secondary symbionts during sexual reproduction of aphids has been investigated in only a handful of aphid lineages and 3 symbiont species. To better characterize this process, we investigated inheritance patterns of 7 symbiont species during sexual reproduction of pea aphids through a crossing experiment involving 49 clones belonging to 9 host-specialized biotypes, and 117 crosses. Symbiont species in the progeny were detected with diagnostic qualitative PCR at the fundatrix stage hatching from eggs and in later parthenogenetic generations. We found no confirmed case of paternal transmission of symbionts to the progeny, and we observed that maternal transmission of a particular symbiont species (Serratia symbiotica) was quite inefficient. We discuss these observations in respect to the ecology of the pea aphid.

Does variation in host plant association and symbiont infection of pea aphid populations induce genetic and behaviour differentiation of its main parasitoid, Aphidius ervi?

The host-associated differentiation (HAD) hypothesis states that higher trophic levels in parasitic associations should exhibit similar divergence in case of host sympatric speciation. We tested HAD on populations of Aphidius ervi the main parasitoid of the pea aphid Acyrthosiphon pisum, emerging from host populations specialized on either alfalfa or red clover. Host and parasitoid populations were assessed for genetic variation and structure, while considering geography, host plant and host aphid protective symbionts Regiella insecticola and Hamiltonella defensa as potential covariables. Cluster and hierarchical analyses were used to assess the contribution of these variables to population structure, based on genotyping pea aphids and associated A. ervi with microsatellites, and host aphid facultative symbionts with 16S rDNA markers. Pea aphid genotypes were clearly distributed in two groups closely corresponding with their plant origins, confirming strong plant associated differentiation of this aphid in North America. Overall parasitism by A. ervi averaged 21.5 % across samples, and many parasitized aphids producing a wasp hosted defensive bacteria, indicating partial or ineffective protective efficacy of these symbionts in the field. The A. ervi population genetic data failed to support differentiation according to the host plant association of their pea aphid host. Potential for parasitoid specialization was also explored in experiments where wasps from alfalfa and clover aphids were reciprocally transplanted on alternate hosts, the hypothesis being that wasp behaviour and parasitic stages should be most adapted to their host of origin. Results revealed higher probability of oviposition on the alfalfa aphids, but higher adult emergence success on red clover aphids, with no interaction as expected under HAD. We conclude that our study provides no support for the HAD in this system. We discuss factors that might impair A. ervi specialization on its divergent aphid hosts on alfalfa and clover.

The potential for hyperparasitism to compromise biological control: Why don’t hyperparasitoids drive their primary parasitoid hosts extinct?

Predation or parasitism on species introduced as biological control agents is a common explanation for failure of biological control programs. Although there is clear evidence from some biological control programs that hyperparasitism can impact a parasitoid biological control agent, it is not clear whether hyperparasitoids have the potential to cause control failure. We performed glasshouse experiments using cages containing 48 plants to address whether the hyperparasitoid Asaphes suspensus can potentially eliminate a population of the primary parasitoid Aphidius ervi, a biological control agent of the pea aphid Acyrthosiphon pisum. Although As. suspensus has a low intrinsic rate of increase, only one-half that of A. ervi and one-third that of pea aphids, it was nonetheless capable of eliminating the A. ervi population within seven A. ervi generations. In contrast, in the absence of As. suspensus, A. ervi eliminated the pea aphid population. Field surveys, however, found that As. suspensus does not eliminate entire natural populations of A. ervi in lucerne crops, probably due to the high frequency of disturbance that favours high intrinsic rates of increase and short generation times. Nonetheless, the ability of As. suspensus to eliminate A. ervi in cages despite its low intrinsic rate of increase underscores the potential for hyperparasitism to disrupt biological control. Small populations are expected to be particularly susceptible to hyperparasitism, such as when releases of a new biological control agent are made.

Individual growth rates do not predict aphid population densities under altered atmospheric conditions

Altered atmospheric composition, associated with climate change, can modify herbivore population dynamics through CO2 and/or O3‐mediated changes in plant quality. Although pea aphid Acyrthosiphon pisum genotypes exhibit intraspecific variation in population growth in response to atmospheric composition, the proximate mechanisms underlying this variation are largely unknown. By rearing single (green, pink) and mixed (green + pink) pea aphid genotypes on red clover Trifolium pratense at the Aspen Free Air CO2 and O3 Enrichment (Aspen FACE) site, we assessed whether: (i) elevated CO2 and/or O3 concentrations alter aphid growth and development and (ii) individual aphid growth rates predict aphid population densities. We showed that growth and development of individual green and pink aphids were not influenced by CO2 and/or O3 concentrations when reared as individual or mixed genotypes. Individual growth rates, however, did not predict population densities. Reared as a single genotype, green pea aphid populations decreased in response to elevated CO2 concentrations, but not in response to elevated CO2 + O3 concentrations. Pink pea aphid populations reared as a single genotype were unaffected by augmented CO2 or O3. Populations of mixed genotypes, however, were reduced under elevated CO2 concentrations, irrespective of O3 concentrations. Herbivore population sizes may not readily be predicted from growth rates of individual organisms under atmospheric conditions associated with global climate change.

Assessing winter-survival of Pandora neoaphidis in soil with bioassays and molecular approaches

Pandora neoaphidis (Entomophthoromycotina, Entomophthorales) is a specific pathogen of aphids with a great potential for use in biological control. The development of effective biological control strategies requires detailed knowledge of its biology and ecology. However, little is known on the overwintering strategies of this fungus. It is believed that natural areas may play an important role for survival and soil may serve as an inoculum source for new populations in spring. This study aimed to investigate winter-survival of P. neoaphidis in topsoil layers in a field experiment by assessing fungal persistence and potential to infect and control pea aphid ( Acyrthosiphon pisum) populations in spring. For this purpose, a selected P. neoaphidis strain was introduced in the form of living infected pea aphids into caged plots containing defined pea aphid populations. Within 3 weeks the aphid populations decreased massively and a significant amount of P. neoaphidis inoculum accumulated on the soil providing optimal conditions for investigating the winter-survival of this fungus. Prevalence and pathogenicity of P. neoaphidis in plot soils were assessed from fall 2006 until spring 2007 using a combination of bioassay, quantitative PCR, and single nucleotide polymorphism genotyping approaches. Results indicated that the introduced strain did not survive the winter on the soil and that the strains present in the plots in the following spring were derived from outside the plots. However, the introduced strain had a beneficial effect on plant survival. The tools developed and applied in this study proved powerful and reliable for tracking specific target strains of P. neoaphidis in the environment.

Complex trait differentiation between host-populations of the pea aphid Acyrthosiphon pisum (Harris): implications for the evolution of ecological specialisation

Variation in traits affecting preference for, and performance on, new habitats is a key factor in the initiation of ecological specialisation and adaptive speciation. However, habitat and resource use also involves other traits whose influence on ecological and genetic divergence remains poorly understood. In the present study, we investigated the extent of variation of life-history traits among sympatric populations of the pea aphid Acyrthosiphon pisum, which shows several host races that are specialised on various plants of the family Fabaceae plants and is an established model for ecological speciation. First, we assessed the community structure of microbial partners within host populations of the pea aphid. The effect of these microbes on host fitness is uncertain, although there is growing evidence that they may modulate various important adaptive traits of their host such as plant utilisation and resistance against natural enemies. Second, we performed a multivariate analysis on several ecologically relevant features of host populations recorded in the present and previous studies (including microbial composition, colour morph, reproductive mode, and male dispersal phenotype), enabling the identification of correlations between phenotypic traits. We discuss the ecological significance of these associations of traits in relation to the habitat characteristics of pea aphid populations, and their consequences for the evolution of ecological specialisation and sympatric speciation.

Similar patterns of linkage disequilibrium and nucleotide diversity in native and introduced populations of the pea aphid, Acyrthosiphon pisum

BackgroundThe pea aphid, Acyrthosiphon pisum, is an emerging genomic model system for studies of polyphenisms, bacterial symbioses, host-plant specialization, and the vectoring of plant viruses. Here we provide estimates of nucleotide diversity and linkage disequilibrium (LD) in native (European) and introduced (United States) populations of the pea aphid. Because introductions can cause population bottlenecks, we hypothesized that U.S. populations harbor lower levels of nucleotide diversity and higher levels of LD than native populations.ResultsWe sampled four non-coding loci from 24 unique aphid clones from the U. S. (12 from New York and 12 from California) and 24 clones from Europe (12 alfalfa and 12 clover specialists). For each locus, we sequenced approximately 1 kb from two amplicons spaced ~10 kb apart to estimate both short range and longer range LD. We sequenced over 250 kb in total. Nucleotide diversity averaged 0.6% across all loci and all populations. LD decayed slowly within ~1 kb but reached much lower levels over ~10 kb. Contrary to our expectations, neither LD nor nucleotide diversity were significantly different between native and introduced populations.ConclusionBoth introduced and native populations of pea aphids exhibit low levels of nucleotide diversity and moderate levels of LD. The introduction of pea aphids to North America has not led to a detectable reduction of nucleotide diversity or increase in LD relative to native populations.

Predator avoidance behavior in the pea aphid: costs, frequency, and population consequences

Induced prey defenses can be costly. These costs have the potential to reduce prey survival or reproduction and, therefore, prey population growth. I estimated the potential for predators to suppress populations of pea aphids (Acyrthosiphon pisum) in alfalfa fields through the induction of pea aphid predator avoidance behavior. I quantified (1) the period of non-feeding activity that follows a disturbance event, (2) the effect of frequent disturbance on aphid reproduction, and (3) the frequency at which aphids are disturbed by predators. In combination, these three values predict that the disturbances induced by predators can substantially reduce aphid population growth. This result stems from the high frequency of predator-induced disturbance, and the observation that even brief disturbances reduce aphid reproduction. The potential for predators to suppress prey populations through induction of prey defenses may be strongest in systems where (1) predators frequently induce prey defensive responses, and (2) prey defenses incur acute survival or reproductive costs.

POPULATION DIFFERENTIATION AND GENETIC VARIATION IN HOST CHOICE AMONG PEA APHIDS FROM EIGHT HOST PLANT GENERA

Habitat choice plays a critical role in the processes of host range evolution, specialization, and ecological speciation. Pea aphid, Acyrthosiphon pisum, populations from alfalfa and red clover in eastern North America are known to be genetically differentiated and show genetic preferences for the appropriate host plant. This species feeds on many more hosts, and here we report a study of the genetic variation in host plant preference within and between pea aphid populations collected from eight genera of host plants in southeastern England. Most host-associated populations show a strong, genetically based preference for the host plant from which they were collected. Only in one case (populations from Vicia and Trifolium) was there little difference in the plant preference spectrum between populations. All populations showed a significant secondary preference for the plant on which all the aphid lines were reared: broad bean, Vicia faba, previously suggested to be a "universal host" for pea aphids. Of the total genetic variance in host preference within our sample, 61% could be attributed to preference for the collection host plant and a further 9% to systematic differences in secondary preferences with the residual representing within-population genetic variation between clones. We discuss how a combination of host plant preference and mating on the host plant may promote local adaptation and possibly ecological speciation, and whether a widely accepted host could oppose speciation by mediating gene flow between different populations.

Leaf surface wax and plant morphology of peas influence insect density

AbstractInsect predators and parasitoids adhere better, forage more effectively, and take more aphid prey on pea plants (Pisum sativumL.) (Leguminosae) with mutations that reduce the crystalline wax bloom on the plant surface. To assess the agronomic potential of this trait for pest management, abundance of pea aphids (Acyrthosiphon pisumL.) (Homoptera: Aphididae) and coccinellid predators, and percent parasitism of the aphids were evaluated on pea lines differing in wax bloom and plant architecture over two field seasons. Three pairs of pea lines were evaluated, each pair with a different architecture and differing within the pair in the amount of surface wax bloom (reduced or normal). The trials included plots treated with a narrow spectrum insecticide (pymetrozine) to reduce aphid populations and untreated controls. Reduced wax peas had significantly fewer aphids per plant in 2002 but not in 2003. Total natural enemy abundance was greater on reduced wax than on normal wax pea lines in both years of the study. Pymetrozine reduced aphid densities significantly in both years. Among the four pea lines evaluated for yield, seed yield per plant was affected by plant morphology and insecticide treatment. Yield was greatest on semileafless plants and on pymetrozine sprayed plots in both years. Yield of the reduced wax line in the semileafless background was similar to or exceeded yield in its normal wax sister line, suggesting that this morphological type was best for an agronomically viable reduced wax phenotype. Pea weevil (Bruchus pisorumL.) (Coleoptera: Bruchidae) damage to seed was overall more frequent on seeds from reduced wax varieties than from normal wax varieties. The results illustrate the trade‐offs associated with a reduced wax trait in peas but also show that certain combinations of reduced wax and gross morphology lead to reduced pea aphid populations and yields similar to those of normal wax peas.

Encounters between aphids and their predators: the relative frequencies of disturbance and consumption

AbstractEcologists may wish to evaluate the potential for predators to suppress prey populations through the costs of induced defensive behaviors as well as through consumption. In this paper, we measure the ratio of non‐consumptive, defense‐inducing encounters relative to consumptive encounters (henceforth the ‘disturbed : consumed ratio’) for two species of aphids and propose that these disturbed : consumed ratios can help evaluate the potential for behaviorally mediated prey suppression. For the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), the ratio of induced disturbances to consumption events was high, 30 : 1. For the cotton aphid, Aphis gossypii (Glover) (Homoptera: Aphididae), the ratio of induced disturbances to consumption events was low, approximately 1 : 14. These results indicate that the potential for predators to suppress pea aphid populations through induction of defensive behaviors is high, whereas the potential for predators to suppress cotton aphid populations through induced behaviors is low. In measuring the disturbed : consumed ratios of two prey species, this paper makes two novel points: it highlights the variability of the disturbed : consumed ratio, and it offers a simple statistic to help ecologists draw connections between predator–prey behaviors and predator–prey population dynamics.

Effects of Hydrophilic and Hydrophobic Kaolin-Based Particle Films on Pea Aphid (Homoptera: Aphididae) and Its Entomopathogen <I>Pandora neoaphidis</I> (Entomophthorales: Entomophthoraceae)

Hydrophobic and hydrophilic kaolin-based particle films are effective for control of insect pests in certain agricultural crops. How these products interact with potential biological control agents is not well documented. This study was conducted to evaluate the effects of the hydrophobic (M96-018) and hydrophilic (Surround WP) kaolin-based particle films (Engelhard Corporation, Iselin, NJ) on pea aphid, Acyrthosiphon pisum (Harris), on peas (Pisum spp.), and on the fungal aphid pathogen Pandora neoaphidis (Remaudière and Hennebert) Humber. Over two field seasons (2001 and 2002) in northern Idaho, applications of M96-018 significantly reduced the rate of pea aphid increase on pea, but Surround WP, tested only in 2001, did not reduce aphid population growth rate. Neither particle film treatment was as effective as a standard application of esfenvalerate (DuPont Asana). In the laboratory, particle films suppressed pea aphid populations by up to 30%. M96-018 seemed to have some repellent activity based on aphid distributions after treating plants. When applied along with P. neoaphidis conidia, M96-018 but not Surround WP caused higher percentage of infection mortality of pea aphids by P. neoaphidis than occurred on controls treated only with P. neoaphidis conidia. P. neoaphidis conidia deposited on glass slides coated with M96-018, produced more germ tubes and secondary conidia than those deposited on untreated glass slides or slides treated with Surround WP. This result suggests that greater infection of pea aphids on plants treated with M96-018 is in part a result of a direct enhancement of fungal germination by the particle film.

ESTIMATING FLUCTUATING VITAL RATES FROM TIME-SERIES DATA: A CASE STUDY OF APHID BIOCONTROL

Many ecological time series describe population dynamics. Indirectly, these data also provide information about the vital rates (e.g., birth rates, mortality rates) underlying these dynamics, but extracting this information from the data can be difficult. Here, we present a method for estimating fluctuating vital rates from ecological time series by using a model to re-code information in observed dynamics into information about unobserved vital rates. This model construction differs from most current models by replacing strong assumptions about the functional relationships dictating population dynamics with more conservative assumptions about how vital rates change with time. Thus, this method is a tool for analyzing time-series data that avoids strong assumptions about the mechanisms driving population dynamics. Our work is motivated by studying the biological control of pea aphids in alfalfa in south-central Wisconsin. Pea aphid populations are consistently held below economic threshold, although the source of this regulation is unclear. Here, we analyze monitoring data to understand the role that a specialist parasitoid plays in aphid biocontrol. Our modeling methodology allows us to estimate the vital rates that determine aphid dynamics (in particular, parasitism) without making arbitrary assumptions about the relationship between parasitism and aphid or parasitoid density. We find that, while parasitism depresses aphid population growth rate substantially, declines in aphid population growth rates do not coincide with increases in parasitism. Therefore, parasitism cannot be responsible for the density-dependent regulation of aphid populations observed in the field.

PREDATORS REDUCE PREY POPULATION GROWTH BY INDUCING CHANGES IN PREY BEHAVIOR

The ability of predators to reduce prey populations is generally ascribed to the consumption of prey individuals. However, predators may also induce behavioral changes in prey individuals, which can reduce prey survival and reproduction. Pea aphid populations are impacted by a variety of predators, many of which induce escape responses in individual aphids. We created disturbance-only predators (surgically manipulated predators that were unable to consume prey, but were still able to forage and interact with prey) and measured their ability to suppress aphid population growth over a six-day period. The greatest reduction in aphid population growth was caused by normal predators that were able to both consume and disturb aphids, but aphid population growth was also strongly reduced by nonconsumptive, disturbance-only predators. These field experiments are the first to show that predators reduce prey population growth partly through predator-induced changes in prey behavior, as well as through consumption of prey individuals.

Relative efficacy of some botanicals, detergent and kerosene in controlling the pea aphid Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) on grass pea Lathyrus sativus

Grass pea Lathyrus sativus L. plays a major role in the nutrition of many poor people in Ethiopia. However, the crop suffers heavy damage by pea aphids Acyrthosiphon pisum (Hemiptera: Aphididae). To test potentially more sustainable and harmless alternatives to the commonly used insecticides, some botanicals (neem, garlic and hot pepper), soap, kerosene and the aphicide pirimicarb, were tested for their efficacy against A. pisum at Wondata village, close to the town of Bahir Dar, in northwestern Ethiopia, from 1999 to 2002. After pirimicarb, hot pepper was consistently the most effective botanical in controlling the pea aphid in terms of both pea aphid population as well as grain yield. Compared to the untreated control, there was up to 83 and 55% lower aphid population on pirimicarb- and hot pepper-treated plots in the 2000/2001 cropping season, respectively. There was also up to 93 and 54% higher grain yield on plots treated with pirimicarb and hot pepper extract, respectively. Soap was less effective, while kerosene caused phytotoxicity. Infestation levels increased with advancing maturity of the crop, rising exceptionally suddenly and dramatically near crop maturity. Combined ANOVA over years and crop growth stages indicated that aphid populations varied with years and growth stages. In 2001/2002, aphid populations were higher and grain yields were lower compared with the other years. Percentage parasitism of aphids was significantly higher on pirimicarb-treated plots (~40%) than other treatments (<20%). Parasitism was essentially a late-season occurrence. Predator population, especially of ladybird beetles (Adonia spp.), was especially higher on hot pepper- and garlic-treated plots, and lowest on pirimicarb treated plots. Grain yield was positively correlated with level of aphid parasitism, ladybird beetle population and number of pods per plant, and strongly negatively correlated with aphid population. In conclusion, a fresh extract of hot pepper sprayed at the rate of 70 ml/4 m2 was selected for further research on rate, frequency and cost of application.

Effects of a simple plant morphological mutation on the arthropod community and the impacts of predators on a principal insect herbivore.

Plant features that enhance predator effectiveness can be considered extrinsic-resistance factors because they result in reduced insect herbivory. In this paper we test the hypothesis that reduced epicuticular wax (EW) in Pisum sativum L. is an extrinsic-resistance factor contributing to field resistance to Acyrthosiphon pisum (Harris). We monitored pea aphid populations in the field on reduced EW and normal EW near isolines of peas for two seasons and confirmed that aphid populations are lower on reduced EW peas than on normal EW peas. We also monitored predators within the canopies of the two pea lines to discover community level patterns in response to differences in EW. We found that while predator numbers were similar between the two lines, there were more syrphids on the normal EW peas, and a trend towards more coccinellids on reduced EW peas. We tested the impact of predators on pea aphids on the two EW lines by monitoring their population levels in cages that excluded predators, and in cages that allowed predators to enter. We found that pea aphid populations were similar on the two EW lines when predators were excluded. When predators were allowed access to the plants, pea aphid populations were reduced more on reduced EW peas than on normal EW peas. We also examined the intrinsic resistance to aphids in reduced EW peas with laboratory dual-choice tests comparing aphid response to reduced EW and normal EW peas, and found that walking, apterous aphids displayed no preference for one pea line over the other. Bioassays to measure growth and fecundity of the pea aphid on the two EW types in the greenhouse and in the field showed that intrinsic rate of increase, and other life table parameters, were not different for aphids on the two lines. Together these results support the hypothesis that reduced EW in peas is a predator-dependent extrinsic resistance factor. Genetically reducing EW bloom in peas and other waxy crop plants might improve the effectiveness of arthropod natural enemies of insect pests. More generally, the results show that a subtle change in plant morphology can substantially influence the impact of predators on insect herbivore populations. The benefit of extrinsic resistance to herbivory conferred by reduced EW may balance any benefits of a prominent EW bloom, thereby sustaining EW polymorphisms in some natural plant populations.

INTERACTIONS BETWEEN SPECIALIST AND GENERALIST NATURAL ENEMIES: PARASITOIDS, PREDATORS, AND PEA APHID BIOCONTROL

Most biological control systems involve a diverse community of natural enemies. We investigated how specialist and generalist natural enemies differ as biological control agents of pea aphids (Acyrthosiphon pisum), and how interactions among natural enemies affect successful control. In alfalfa, pea aphids are attacked by a specialist parasitoid wasp, Aphidius ervi, and a guild of generalist predators primarily made up of Nabis and Orius bugs, coccinellid and carabid beetles, and web-building spiders. In three field experiments, we manipulated the parasitoid, then the generalist predator guild, and finally both classes of natural enemy, and recorded resulting impacts on pea aphid population control. The parasitoid caused little immediate reduction in aphid population growth but caused a large decline after a delay corresponding to the generation time of the parasitoid. In contrast, the generalist guild caused an immediate decline in the aphid population growth rate. However, the generalists did not exert density-dependent control, so aphid densities continued to increase throughout the experiment. The third field experiment in which we simultaneously manipulated parasitoids and predators investigated the possibility of “nonadditive effects” on aphid control. Densities of parasitoid pupae were 50% lower in the presence of generalist predators, indicating intraguild predation. Nonetheless, the ratio of parasitoids to aphids was not changed, and the impact of the two types of natural enemies was additive. We constructed a stage-structured model of aphid, parasitoid, and predator dynamics and fit the model to data from our field experiments. The model supports the additivity of parasitoid and predator effects on aphid suppression but suggests that longer-term experiments (32 d rather than 20 d) would likely reveal nonadditive effects as predation removes parasitoids whose response to aphid densities occurs with a delay. The model allowed us to explore additional factors that could influence the additivity of parasitoid and predator effects. Aphid density-dependent population growth and predator immigration in response to aphid density would likely have little influence on the additivity between parasitism and predation. However, if a parasitoid were to show a strong Type II functional response, in contrast to A. ervi whose functional response is nearly Type I, interactions with predators would likely be synergistic. These analyses reveal factors that should be investigated in other systems to address whether parasitism and predation act additively on host densities. Corresponding Editor: E. Evans.

BAYESIAN ESTIMATION OF A DEMOGRAPHIC MATRIX MODEL FROM STAGE-FREQUENCY DATA

Demographic matrix models are standard tools for analyzing the dynamics of age- or stage-structured populations. Here, we present a method for estimating the average vital rates that parameterize a demographic matrix using a series of measurements of population size and structure (an “inverse problem” of demographic analysis). We join a deterministic, density-independent demographic matrix model with a stochastic observation model to write a likelihood function for the matrix parameters given the data. Adopting a Bayesian perspective, we combine this likelihood function with prior distributions for the model parameters to produce a joint posterior distribution for the parameters. We use a numerical technique (Markov chain Monte Carlo) to estimate and analyze the posterior distribution, and from this we calculate posterior distributions for functions of the demographic matrix, such as the population multiplication rate, stable stage distribution, and matrix sensitivities. Although measurements of population size and structure rarely contain enough information to estimate all the parameters in a matrix precisely, our analysis sheds light on the information that the data do contain about the vital rates by quantifying the precision of the parameter estimates and the correlations among them. Moreover, we show that matrix functions such as the population multiplication rate and matrix sensitivities can still be estimated precisely despite sizable uncertainty in the estimates of individual parameters, permitting biologically meaningful inference. We illustrate our approach for three populations of pea aphids (Acyrthosiphon pisum).

Population Dynamics of the Pea Aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae) on Field Pea ( Pisum sativum L.) in Northwestern Ethiopia

Once a minor pest, the pea aphid, Acyrthosiphon pisum (Harris) has recently become a major pest of field pea (Pisum sativum L.) in Ethiopia, particularly in the northwestern region. To determine the population dynamics of the pest, field experiments were carried out at Adet and Zema in northwestern Ethiopia in 1994, 1995 and 1996. Treatments were planting dates at 15-day intervals in May, June and July and sampling was carried out weekly until crop maturity. Combined ANOVA, over seasons and locations, showed significant effects of sowing dates, seasons and locations. Pea aphid populations increased and decreased with delay in planting at Adet and Zema, respectively. At Adet, peaks of weekly counts of aphid numbers were observed in August and seasonal totals of aphids on individual planting dates increased as planting was delayed. At Zema, peaks of weekly counts of aphid numbers were observed in mid-July (1996), late August and early September (1995) and mid-September (1994); peas planted on June 16 gave the lowest seasonal totals of aphids. Natural enemies (predators and parasitoids) appeared in considerable numbers in 1996 and these tended to increase as planting date was delayed. For most planting dates and years, weekly aphid populations showed positive correlation with maximum temperature, and negative correlation with minimum temperature and relative humidity. Increasing maximum temperature promoted the buildup of aphid populations while increased minimum temperature, rainfall and relative humidity suppressed it. Grain yield increased and decreased as planting date was delayed at Adet and Zema, respectively. From these results, it is recommended that planting of field peas should take place from mid- to late June at Adet and during the first week of June at Zema to obtain higher yields; by doing so a mean of 0.32 t/ha and 0.50 t/ha higher yield was obtained, respectively.