The effect of population density on the reproduction ofTrichogramma japonicum Ashmead (Hymenoptera: Trichogrammatidae)

When a fixed number of the hosts, the eggs of the almond moth were exposed experimentally to various numbers of the parasites, Trichogramma japonicum, the following changes were observed with increasing parasite density:

1. The percentage of parasitism rises and approaches to 100 with gradually diminishing rate.
2. The number of parasite progeny increases and reaches a maximum, then decreases gradually.
3. The number of eggs laid per parasite female decreases gradually.
4. The proportion of hyperparasitized hosts progressively rises. The frequency distribution of parasite eggs in a host is of an intermediate type between random and uniform.
5. The competition among parasite larvae becomes severe. The progressive rise in mortality, the declining percentage of females in progeny and the emergence of stunted adults at the higher densities are observed.

In connection with both the nature of the parasitizing behaviour of adult and that of the competition among larvae, the nature of the density effect on the parasite population was discussed.     

Regulatory processes and population cyclicity in laboratory populations ofAnagasta Kühniella (Zeller) (Lepidoptera: Phycitidae). III. The development of population models

1. Life table data for interactions between Anagasta kühniella and its ichneumon parasite Venturia canescens in two room ecosystems (A & B) have been analyzed in an attempt to explain and model each room situation. The life table data have been presented in the form of a graphical key-factor analysis, and have been further analyzed by an investigation of the density relationships between the different mortalities and the Angasta densities upon which the mortalities act.
2. In room A (1.2 gm food per container), the parasites were present throughout the interaction. Egg and early larval mortality (k₁) appeared to be directly density-dependent and was the sole stabilizing influence when introduced into the model for room A. The area of discovery of the parasite was relatively constant and its mean value was used to calculate parasitism (k₃) in the model. All other mortalities were density-independent and treated as being constant at their mean values. The model predicts a series of oscillations of decreasing amplitude which are somewhat similar to those observed in the Anagasta population during the early stages of the interaction. The observed mean densities of host and parasite were very close to those predicted.
3. In room B, the parasites were absent for the first 8 generations (1- 2gm food per container). Model B₁ covers this period and includes a direct density-dependent component describing changes in k₁, the remaining mortalities being constant. The observed mean densities approximate to the calculated densities. The parasites were present from the ninth generation and after the eleventh generation the food per container was increased to 7.2 gm. Model B₂ covers the period in room B from generation 11. The most important component of k₁ after the parasites were established is a delayed density-dependent one which appeared to be due to wounding of very small larvae by the probing activities of the parasites. Since the changes in k₁ could not be suitably predicted, the observed values were used in model B₂. This delayed component was not detected in room A due to the relatively small range of parasite densities in room A compared with the 600-fold change in densities in room B. The calculated area of discovery for the parasite population in each generation was found to vary inversely with searching parasite density, and this ‘interference relationship’ was used in the submodel for parasitism. Again, this relationship was not detected in room A due to the much smaller range of parasite densities there. Model B₂ gives oscillations in host and parasite populations arising from parasitism being a delayed density-dependent mortality. The correspondence with the observed oscillations is partly due to the actual k₁-values being used and partly because the submodel for parasitism adequately describes the observed changes in k₃. The tendency for these oscillations to decrease in amplitude is due to both the damping effect of parasite interference and the direct density-dependent component of k₁.

     

Differences in egg wastage by superparasitism,contrastingVenturia (=Nemeritis) canescens searching singly versus searching in groups

A statistical and graphic study is presented of the wastage of eggs by Venturia (=Nemeritis) canescens when searching singly and in groups of 10 among hosts at four different host densities in laboratory universes as described byHuffaker andMatsumoto (preceding paper of this journal). The host insect was the fluour moth Anagasta kühniella and the host densities used were 10, 30, 100 and 200 per universe. Intensity of egg wastage due to superparasitim varied significantly according to host density, and between the two parasite densities employed, 1 and 10, using both F-tests and chi-square tests. Plots of k-factor analysis on this egg wastage showed high negative correlations with host density, and the raw data for single parasites was well represented by a parabola while that for the grouped parasites departed from this relationship only at the lowest host density.     

Functional response to host density in a parasitic wasp,with reference to population regulation

1. The functional response to, and preference for, the host density in a parasite were examined experimentally using an icheumon wasp, Exidechthis canescens, and its host Cadra cautella under controlled conditions.
2. Wasps were more active in host-searching at higher than lower host densities. Percent parasitism increased rapidly with initial increments in host density and then tended to increase more slowly at higher host densities. A sigmoid functional response curve is indicated, which implies that the parasite is able to control its host even at low densities.
3. Wasps actively selected areas of high host density in which to concentrate host-searching behavior.
4. Host-searching by E. canescens is stimulated by the odor of the host when present, and by food in which hosts have developed but have been removed.
5. Both the functional response and the host-density preference of the parasite are mediated by its host-searching behavior. This relationship is discussed in the context of population regulation.

     

Effect of temperature and parasite density on three species ofAphytis (Hymenoptera: Aphelinidae), parasitising California red scale

Summary Three species ofAphytis parasites of California red scale,Aonidiella aurantii (Maskell) were each confined at different densities with approximately equal numbers of scale insects at several constant temperatures to determine the effect of these factors on progeny production and distribution and the search rate. Egg location on the host body by the parasites was unaffected by temperature or parasite density.A. melinus laid its eggs both dorsally and ventrally in equal proportions whileA. lingnanensis andA. chrysomphali laid their eggs ventrally. Progeny production byA. melinus andA. lingnanensis increased at the higher temperature; that ofA. chrysomphali did not. Unlike the other species,A. chrysomphali failed to oviposit at 32°C. Although increasing parasite density reduced progeny production in bothA. melinus andA. lingnanensis, they were able to maintain an almonst constant search rate. This was due to their ability to distribute their eggs among the hosts more regularly at the higher parasite densities. While the mechanism of this process is easy to understand forA. melinus which behaved as a gregarious parasite, it is unclear forA. lingnanensis, which is almost a solitary parasite. The progeny production and the search rate ofA. chrysomphali dropped significantly with increasing parasite density.     

On the capacity of macroparasites to control insect populations

A graphical model of the population dynamics of macroparasites and their hosts is developed. Three principal means by which the parasites can be regulated are considered: reduction in host density as a result of parasite-induced host mortality, reduction in host density as a result of parasite-induced host sterility, and competition among parasites within multiply-infected hosts. The means by which parasites are regulated has a major effect on the degree to which they can depress host population densities. In particular, a parasite that sterilizes its host is expected to reduce host density more than one that causes an equivalent decline in host fitness through increased mortality. A special case of the model is developed for herbivorous insects that, in the absence of parasites, are limited by larval food resources. Parasites that are regulated via parasite-induced host sterility will control the insect populations below the level set by larval resources if the threshold host density for the parasites (N(T)) is less than the ratio of carrying capacity to net reproductive rate of the insects (K/R). Data are presented showing that all three means of parasite regulation, but especially parasite-induced host sterility, can operate in Howardula aoronymphium, a nematode parasite of mycophagous Drosophila flies. Data from a field cage experiment show that, if these nematodes are regulated primarily via reductions in host density due to this sterility, the parameters N(T), K, and R are such that Howardula is likely to play an important role in controlling Drosophila populations. However, this conclusion must be tempered by the fact that these nematodes also cause increased host mortality and experience within-host competition, making the conditions for parasite control of the flies more stringent.     

Temporal and spatial variation of larval parasitism in non-outbreaking populations of a folivorous moth

In order to assess the role of parasitoids in the regulation of non-outbreaking populations of Epirrita autumnata, a geometrid lepidopteran with outbreaking populations in northern Europe, we examined the temporal and spatial variation of larval parasitism in southwestern Finland during 6 successive years. The study was carried out on two spatial scales, among trees within sites of about 1 ha and among sites separated by distances of 2–10 km, using experimental and observational approaches respectively. The overall percent parasitism was independent of host density on both spatial scales, while temporally it fluctuated only little. Of the two main parasitoids, the commoner one, Protapanteles immunis, showed a variable response to host density on the larger spatial scale and negative density dependence on the smaller scale. Temporally, parasitism caused by this species was independent of host density. Another parasitoid, Phobocampe bicingulata, showed positive density dependence on the smaller spatial scale and had a variable response on the larger scale, but exhibited negative density dependence over time. The results of this study caution against drawing conclusions concerning population regulation on the grounds of spatial density dependence alone. Larval parasitoids apparently do not maintain low densities in the E. autumnata populations studied. However, they may suppress E. autumnata densities to a level low enough for density-dependent mortality factor(s) to become regulating. Among other mortality factors of E. autumnata, pupal predation has been found to be temporally positively density-dependent. Received: 19 October 1999 / Accepted: 10 January 2000     

Structure,organization, and response of a species-rich parasitoid community to host leafminer population dynamics

The parasitoid community dynamics of an agromyzid honeysuckle leafminer, Chromatomyia suikazurae (Agromyzidae, Diptera) were studied between 1981 and 1990 in a natural forest in Kyoto, Japan. The parasitoid fauna composed three koinobionts (all larval-pupal solitary parasitoids) and 22 idiodiont species (11 larval solitary, nine pupal solitary and one pupal gregarious). The parasitoid community was dominated by early-attacking oligophagous braconid koinobionts at early periods, but was gradually displaced by late-attacking polyphagous eulophid idiobionts. Accordingly, the diversity index of the parasitoid community peaked at an intermediate point in the intra-generational succession. The succeeding attack-in-waves by the late-attacking idiobionts greatly reduced not only the survival rates of early-attacking parasitoid larvae but also the survival rates of hosts. The density-dependence observed in the host pupal mortality was thought to result from density-dependent host-switching by a keystone polyphagous pupal idiobiont parasitoid, Chrysocharis pubens, whereas high host pupal mortality was potentially attained by an early-attacking koinobiont braconid. Supposed aggregation of polyphagous parasitoids at high host density resulted in intense within-host competition and in an increase of host-feeding attack, both of which contributed to low emergence rates of parasitoids at high host densities. Parasitoid emergence rates were also reduced at low host densities, probably by inter- and intra-specific hyperparasitism among oligophagous parasitoids for limited hosts. The regulation effects of the species-rich parasitoid community upon the host population dynamics are thought to derive from succeeding attack-in-waves by polyphagous late-attacking idiobionts, especially by the keystone species.     

Crowding and disease: effects of host density on response to infection in a butterfly–parasite interaction

Abstract. 1. Hosts experiencing frequent variation in density are thought to benefit from allocating more resources to parasite defence when density is high (‘density‐dependent prophylaxis’). However, high density conditions can increase intra‐specific competition and induce physiological stress, hence increasing host susceptibility to infection (‘crowding‐stress hypothesis’). 2. We studied monarch butterflies (Danaus plexippus) and quantified the effects of larval rearing density on susceptibility to the protozoan parasite Ophryocystis elektroscirrha. Larvae were inoculated with parasite spores and reared at three density treatments: low, moderate, and high. We examined the effects of larval density on parasite loads, host survival, development rates, body size, and wing melanism. 3. Results showed an increase in infection probability with greater larval density. Monarchs in the moderate and high density treatments also suffered the greatest negative effects of parasite infection on body size, development rate, and adult longevity. 4. We observed greater body sizes and shorter development times for monarchs reared at moderate densities, and this was true for both unparasitised and parasite‐treated monarchs. We hypothesise that this effect could result from greater larval feeding rates at moderate densities, combined with greater physiological stress at the highest densities. 5. Although monarch larvae are assumed to occur at very low densities in the wild, an analysis of continent‐wide monarch larval abundance data showed that larval densities can reach high levels in year‐round resident populations and during the late phase of the breeding season. Treatment levels used in our experiment captured ecologically‐relevant variation in larval density observed in the wild.     

Functional response to host density by the egg parasiteTrichogramma pretiosum

The effect of host density on parasitism byTrichogramma pretiosum Riley was studied by exposing groups of 150, 300, 600 or 1200 eggs of potato tuber moth to 2, 4 or 8 female parasites per group. The parasite exhibited a type 2 functional response. As host density increasedT. pretiosum parasitised more hosts, but at a decreasing rate. The attack coefficient (a′) decreased as parasite density increased, whereas the handling time (T _h ) remained almost constant. The search rate (a) decreased with increasing host density.T. pretiosum responded to increasing host density by increasing the number of its encounters with hosts and the number of hosts it parasitised only up to host density of 300 when the parasite density was 2 and up to host density of 600 when the parasite densities were greater and then remained almost constant. The observed incidence of parasitism was higher than that expected on the assumption that the parasites behaved the same at higher host densities as at the lowest. When parasite density was raised from 2 to 8 females per group the percentage of female progeny fell from about 73 to about 48%. A 2-fold increase in the number of female progeny was observed when parasite density was reduced from 8 to 2 and also when the host density was raised from 150 to 1200 eggs.     

Effects of parasite density and host availability on progeny production byBiosteres (Opius) longicaudatus, [Hym.: Braconidae], a parasite ofAnastrepha suspensa [Dip.: Tephritidae]

Progeny production ofBiosteres (Opius) longicaudatus Ashmead, a larvalpupal parasite of the Caribbean fruit fly,Anastrepha suspensa (Loew) was affected by host availability, previous ovipositional experience, and parasite density and age. Parasitization rates were evaluated in 24.5 cm³ ovipositional cages at parasite densities of 25, 125, and 250 male-female pairs by exposingB. longicaudatus adults to (a) 500A. suspensa larvae for a 24 h period or (b)ad libitum host larvae for each of the 14 days following eclosion. The mean numbers of parasite progeny produced at the 25, 125, and 250 densities were 1076, 1896, and 2038, respectively. The number of progeny produced per surviving female parasite was inversely proportional to the adult parasite density and relatively more female progeny were produced as the adult parasites aged. Host mortality was significantly higher among parasitized larvae. Maximum rearing efficiency was achieved at the 125 density.     

Bottom–up regulation of parasite population densities in freshwater ecosystems

Theory predicts the bottom–up coupling of resource and consumer densities, and epidemiological models make the same prediction for host–parasite interactions. Empirical evidence that spatial variation in local host density drives parasite population density remains scarce, however. We test the coupling of consumer (parasite) and resource (host) populations using data from 310 populations of metazoan parasites infecting invertebrates and fish in New Zealand lakes, spanning a range of transmission modes. Both parasite density (no. parasites per m²) and intensity of infection (no. parasites per infected hosts) were quantified for each parasite population, and related to host density, spatial variability in host density and transmission mode (egg ingestion, contact transmission or trophic transmission). The results show that dense and temporally stable host populations are exploited by denser and more stable parasite populations. For parasites with multi‐host cycles, density of the ‘source’ host did not matter: only density of the current host affected parasite density at a given life stage. For contact‐transmitted parasites, intensity of infection decreased with increasing host density. Our results support the strong bottom–up coupling of consumer and resource densities, but also suggest that intraspecific competition among parasites may be weaker when hosts are abundant: high host density promotes greater parasite population density, but also reduces the number of conspecific parasites per individual host.     

Regulatory processes and population cyclicity in laboratory populations ofAnagasta kühniella (Zeller) (Lepidoptera: Phycitidae)

AsMatsumoto andHuffaker (1973) concluded that their initial universe size was too small for the proper separation of the effects of host density and dispersion on parasite performance, a larger universe of 38 1/2″ (length) ×38 1/2″ (width) ×3″ (height) was used. When individual parasites were exposed to fixed densities and dispersion patterns of host, they displayed an overall decrease in the parasitization rate when compared to the small universe. In all cases aHolling -type response resulted. When a group of 10 parasites per test was employed a Nicholsonian type of response resulted. In an experimentally confined space, the parasites displayed a mutual behavioral interference resulting in emigration which accelerated as the parasite density increased.     

Regulatory processes and population cyclicity in laboratory populations ofAnagasta kühniella (Zeller) (lepidoptera: Phycitidae) V. Host finding and parasitization in a “small” universe by an entomophagous parasite,Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae)

Summary Host finding by the entomophagous parasite,Venturia canescens (Grav.), parasitizingAnagasta kühniella (Zeller) was studied. Studies utilizing fixed densities and dispersion patterns of the hosts where no choice of density groupings was offered showed that within the experimental conditions used, host density relationships were more important than dispersion. Decreasing the time hosts were exposed to a parasite from 72 hours to 24 hours did not alter the overall parasitization. In both cases progressively less hosts were parasitized as host density increased, which exemplified aHolling-type of response. However, when host densities were varied within the same universe, independent of dispersion patterns, and the parasites were given a “choice” of host densities to attack, an increasing percentage of hosts in the higher host density groups were parasitized; thus a density-dependent behavioral response was exhibited. These studies were conducted as a partial fulfillment in the Ph. D. program of one of us (B. M. Matsumoto) and form a part of a broad investigation into the processes operating in the dynamics of arthropod populations under grants toC. B. Huffaker from the U. S. Public Health Service, National Institutes of Health and the U. S. Department of Agriculture.     

Infections with immunogenic trypanosomes reduce tsetse reproductive fitness: potential impact of different parasite strains on vector population structure

The parasite Trypanosoma brucei rhodesiense and its insect vector Glossina morsitans morsitans were used to evaluate the effect of parasite clearance (resistance) as well as the cost of midgut infections on tsetse host fitness. Tsetse flies are viviparous and have a low reproductive capacity, giving birth to only 6-8 progeny during their lifetime. Thus, small perturbations to their reproductive fitness can have a major impact on population densities. We measured the fecundity (number of larval progeny deposited) and mortality in parasite-resistant tsetse females and untreated controls and found no differences. There was, however, a typanosome-specific impact on midgut infections. Infections with an immunogenic parasite line that resulted in prolonged activation of the tsetse immune system delayed intrauterine larval development resulting in the production of fewer progeny over the fly's lifetime. In contrast, parasitism with a second line that failed to activate the immune system did not impose a fecundity cost. Coinfections favored the establishment of the immunogenic parasites in the midgut. We show that a decrease in the synthesis of Glossina Milk gland protein (GmmMgp), a major female accessory gland protein associated with larvagenesis, likely contributed to the reproductive lag observed in infected flies. Mathematical analysis of our empirical results indicated that infection with the immunogenic trypanosomes reduced tsetse fecundity by 30% relative to infections with the non-immunogenic strain. We estimate that a moderate infection prevalence of about 26% with immunogenic parasites has the potential to reduce tsetse populations. Potential repercussions for vector population growth, parasite-host coevolution, and disease prevalence are discussed.     

Ovipositional response ofVenturia canescens (Grav.) (Hymenoptera: Ichneumonidae) to various host and parasite densities

Summary Ovipositional response inVenturia canescens (Grav.) parasitizingAnagasta kühniella (Zeller) is analyzed for all combinations of five parasite densities (2, 5, 10, 25, and 50), four host densities (25, 50, 100, and 200), and three floor area universe sizes (76 cm², 160 cm², and 345 cm²). Over this range, no mutual interference (as measured by decreasing parasite fecundity) was observed, althoughNicholson’s area of discovery decreased significantly with parasite density increase as a result of a non-Poisson distribution of parasite eggs; use of this parameter is therefore not a suitable means of determining if mutual interference is present. Other parameters studied, and for which significant correlations were obtained, include mean parasite eggs per host, percentage parasitization, percentage of parasite eggs wasted, and negative binomialk approximations. This study was conducted as part of a broad investigation into the processes operating in the dynamics of arthropod populations under a grant toC. B. Huffaker by the U.S. Public Health Service, National Institutes of Health.     

Nutritional availability and larval density dependence in Aedes aegypti

1. Density dependence is the effect of density on population growth. Density dependence is an aggregate term for a suite of complex interactions between animals and their environment. 2. Mechanistic studies of density dependence in mosquito ecology are sparse, and the role of environmental factors is poorly understood. 3. Two empirical study designs were compared to consider the interaction between nutritional availability and density in Aedes aegypti. First, larvae were fed per capita. Second, larvae were fed a fixed amount of food unadjusted for the number of individuals; therefore, at higher densities, individuals received less per capita. 4. Survivorship, wing length, and development rate were lower at high densities when larvae were fed a fixed, unadjusted amount of food. The opposite was observed when food was adjusted per capita, suggesting that high densities may be beneficial for larval development when per capita nutrition is held constant 5. These results demonstrate that negative associations between Ae. aegypti larval density and larval development are a manifestation of decreased per capita nutrient uptake at high densities. 6. Population regulation is a proportional response to environmental variability in Ae. aegypti. Increased survivorship at high densities when larvae were fed per capita demonstrates that nutritional availability is not the only mechanism of density dependence in mosquitoes. Further studies should characterise density dependence in mosquitoes by using mechanistic study designs across diverse environmental conditions.     

Strong density-dependent survival and recruitment regulate the abundance of a coral reef fish

Debate on the control of population dynamics in reef fishes has centred on whether patterns in abundance are determined by the supply of planktonic recruits, or by post-recruitment processes. Recruitment limitation implies little or no regulation of the reef-associated population, and is supported by several experimental studies that failed to detect density dependence. Previous manipulations of population density have, however, focused on juveniles, and there have been no tests for density-dependent interactions among adult reef fishes. I tested for population regulation in Coryphopterus glaucofraenum, a small, short-lived goby that is common in the Caribbean. Adult density was manipulated on artificial reefs and adults were also monitored on reefs where they varied in density naturally. Survival of adult gobies showed a strong inverse relationship with their initial density across a realistic range of densities. Individually marked gobies, however, grew at similar rates across all densities, suggesting that density-dependent survival was not associated with depressed growth, and so may result from predation or parasitism rather than from food shortage. Like adult survival, the accumulation of new recruits on reefs was also much lower at high adult densities than at low densities. Suppression of recruitment by adults may occur because adults cause either reduced larval settlement or reduced early post-settlement survival. In summary, this study has documented a previously unrecorded regulatory mechanism for reef fish populations (density-dependent adult mortality) and provided a particularly strong example of a well-established mechanism (density-dependent recruitment). In combination, these two compensatory mechanisms have the potential to strongly regulate the abundance of this species, and rule out the control of abundance by the supply of recruits.     

Effects of crowding on populations of Aedes albifasciatus larvae under laboratory conditions

Aedes (Ochlerotatus) albifasciatus(Macquart 1838) (Diptera: Culicidae) is a neotropical flood water mosquito, incriminated as the main vector of the western equine encephalitis virus, and which affects beef and milk production in central Argentina. The short time required to hatch and develop from egg to adult, usually in temporary pools, suggests a strategy which allows for exploitation of transient pools, thus evading predation and interspecific competition. Under these conditions intra specific competition could represent a major density-dependent source of larval mortality, but the relative importance of density-dependent regulation of mosquito populations has generated controversy. Therefore we examined the effects of larval density on basic population characteristics of Ae. albifasciatusin the laboratory. Larvae were obtained by synchronous hatching of eggs laid by field-trapped females. Emerging larvae (L1) were used to build cohorts of different initial densities, kept in plastic trays with 400 ml of distilled water, and food supplied daily during the first 10 days (0.1 g per larvae day^–1). Age-specific development time and specific and relative mortality were estimated, and their relation to initial larval density was assessed through linear and non-linear regressions and correlation analysis. First hatching was registered 3 h after flooding the eggs. Higher levels of pre-adult mortality were detected in groups with higher densities. Specific mortality and average time to enter a stage of L1 to L3 could directly be related to initial larval density, but no significant relations were found for L4 and pupae. Results suggest that crowding could be a factor capable of regulating the density of natural populations of Ae. albifasciatus.