Regulation of aphid populations by aphidiid wasps: does parasitoid foraging behaviour or hyperparasitism limit impact?

Aphidiid parasitoids (Hymenoptera: Aphidiidae) of aphids generally exploit only a small percentage of the available host resources in the field. This limited impact on aphid populations has often been explained as a consequence of hyperparasitism. We propose that a wasp's reproductive strategy, as opposed to hyperparasitism, is the dominant factor in aphidiid population dynamics. A wasp's foraging efficiency and oviposition decisions are influenced by several variables, including searching behaviour between and within patches, host choice (as modified by the aphids' defensive behaviours), and plant structural complexity. Two broadly different patterns of host exploitation have evolved in aphidiid wasps in relation to ant-aphid mutualism. Firstly, in species that are exposed to predation and hyperparasitism, a female may leave a patch before all suitable hosts are parasitized. Because predators and hyperparasitoids tend to aggregate at high aphid or aphidiid densities, or in response to aphid honeydew, this strategy enables females to reduce offspring mortality by spreading the risk over several host patches. Secondly, in species that have evolved mechanisms to avoid aggression by mutualistic ants, females are able to exploit a hyperparasitoid-free resource space. Such species may concentrate their eggs in only a few aphid colonies, which are thus heavily exploited. Although hyperparasitism of species in the first group tends to reach high levels, its overall impact on aphid-aphidiid population dynamics is probably limited by the low average fecundity of most hyperparasitoids. We discuss the foraging patterns of aphidiid wasps in relation to aphid population regulation in general, and to classical biological control in particular. We argue that a parasitoid's potential to regulate the host population is largely determined by its foraging strategy. In an exotic parasitoid, a behavioural syndrome that has evolved and presumably is adaptive in a more diverse (native) environment may, in a more uniform (managed) environment, result in suboptimal patch-leaving and oviposition decisions, and possibly increased resource usage.     

Generalist and specialist predators that mediate permanence in ecological communities

 General dynamic models of systems with two prey and one or two predators are considered. After rescaling the equations so that both prey have the same intrinsic rate of growth, it is shown that there exists a generalist predator that can mediate permanence if and only if there is a population density of a prey at which its per-capita growth rate is positive yet less than its competitor’s invasion rate. In particular, this result implies that if the outcome of competition between the prey is independent of initial conditions, then there exists a generalist predator that mediates permanence. On the other hand, if the outcome of competition is contingent upon initial conditions (i.e., the prey are bistable), then there may not exist a suitable generalist predator. For example, bistable prey modeled by the Ayala–Gilpin (θ-Logistic) equations can be stabilized if and only if θ<1 for one of the prey. It is also shown that two specialist predators always can mediate permanence between bistable prey by creating a repelling heteroclinic cycle consisting of fixed points and limit cycles. Received 10 August 1996; received in revised form 21 March 1997     

Dispersion analyses and resource utilization of aphid parasitoids in a non-depletable environment

Dispersions and resource utilization of primary and secondary parasitoids developing in non-depletable primary host populations were determined for an aphid-parasitoid community occurring on strawberries. Analyses of dispersions based onGreen 's coefficient andLloyd 's Patchiness Index indicated parasitized aphids were highly aggregated initially, became less aggregated as density increased, and remained aggregated following collapse of the aphid populations. The “index of aggregation” values calculated usingTaylor 's Power Law concurred with results from the other indices, and the similarity of the regression coefficients from both seasons suggests that the index of aggregation may be characteristic for communities as well as species. Analysis withIwao 's regression of mean crowding on the mean generated similar results when population data were stratified temporally, and also indicated that the individual was the basic unit of the population. In a non-depletable environment, oviposition of individuals exhibiting an aggregated dispersion pattern within clumps of hosts provides primary parasitoids with a suitable trade-off between energy utilization or genetic potential, and losses associated with hyperparasitism.     

Refuge use by fish as a function of body weight changes

Refuge use provides a good model for the study of trade-offs between the benefits of predator avoidance and the costs of lost feeding opportunities. We manipulated the latter costs by subjecting similar-sized three-spine sticklebacks to 2 days of food deprivation followed by a 2-day re-feeding period and recorded associated changes in body weight and refuge use. Food deprivation resulted in a decrease and re-feeding in an increase in the duration of refuge use by fish. Emergence times of fish from the refuge were extremely variable (with a ratio of 1:127 between the shortest and the longest ones) but individual ranks were highly consistent between different days of testing, suggesting that emergence times were individually characteristic. Percentage weight change of fish in response to the experimental treatments also showed a high level of inter-individual variation ranging from 0–17%. A significant positive correlation was found between the percentage weight lost and the percentage decrease in emergence time from a refuge after food deprivation and similarly between the percentage weight gained and the percentage increase in refuge use after re-feeding. The relationship between energy turnover and behavioural strategies is discussed. Received: 13 December 1998 / Received in revised form: 2 May 1999 / Accepted: 7 June 1999     

Intra versus interspecific interactions of ladybeetles (Coleoptera: Coccinellidae) attacking aphids

Summary The nature and relative strengths of intra versus interspecific interactions among foraging ladybeetle larvae were studied experimentally by measuring short-term growth rates of predators and reductions in population sizes of prey in laboratory microcosms. In these microcosms, ladybeetle larvae foraged singly or as conspecific or heterospecific pairs, for pea aphids on bean plants over a two-day period. Similarly sized third instar larvae ofHippodamia convergens andH. tredecimpunctata, H. convergens andH. sinuata, andH. convergens andCoccinella septempunctata, were tested in experiments designed to ensure that paired larvae experienced moderate competition. Interspecific competition in these experiments did not differ significantly from intraspecific competition, in that an individual's weight gain did not depend on whether its competitor was heterospecific or conspecific. Furthermore, aphid populations were reduced equally by heterospecific and conspecific pairs. These results suggest that there is little or no difference between intra and interspecific interactions among larvae of these ladybeetles when two similarly sized individuals co-occur on a host plant. Thus, the species diversityper se of assemblages of ladybeetle larvae may have little influence over the short term on the reduction of aphid populations by ladybeetle predation.     

Intraguild predation and interference by the mealybug predator Cryptolaemus montrouzieri on the parasitoid Leptomastix dactylopii

The compatibility of the encyrtid parasitoid Leptomastix dactylopii with the coccinellid beetle Cryptolaemus montrouzieri against the citrus mealybug, Planococcus citri, is determined by the extent of intraguild predation and interference by the predator. We tested the preference of the adults and fourth-instar larvae of C. montrouzieri for healthy mealybugs and parasitized mealybugs harboring 1-, 4-, 7- and 14-day-old parasitoid larvae. The experiments were conducted in no-choice (only unparasitized mealybugs or parasitized mealybugs of one parasitoid age were offered at one time) and choice (unparasitized and parasitized mealybugs of a specific age were offered simultaneously) tests. Both the adults and larvae of C. montrouzieri fed on unparasitized and parasitized mealybugs but strongly discriminated against the hardened mummies (14 days old). We also investigated the influence of the presence of C. montrouzieri to the foraging effectiveness of L. dactylopii. The level of parasitism by L. dactylopii was reduced from about 13 to 6% when the number of the C. montrouzieri was increased from zero to four. We recommended that the releases of C. montrouzieri should be conducted 14 days after the releases of L. dactylopii to reduce intraguild predation on the parasitized mealybugs and to avoid interference with the foraging parasitoids.     

Foraging behaviour of a leafminer parasitoid in the field

Abstract. 1. The searching behaviour of the parasitoid Sympiesis sericeicornis Nees (Hymenoptera, Eulophidae) is analysed under field conditions.
2. Females were tracked when flying around the canopy of apple trees infested with the tentiform leafminer Phyllonorycter cydoniella (D. & S.)(Lepidoptera, Gracillariidae) and their behaviour studied at the level of a single mine and at the level of several mines on the same leaf (patch level).
3. The presence of mines is detected during flight. The foraging behaviour at the patch level is efficient: the female is able to distinguish the suitable from the unsuitable hosts and handle the suitable hosts first. Not all mines are visited before departure from the leaf and those left unvisited are exclusively mines without suitable hosts. The patch leaving rule is discussed.
4. An ethogram of the behaviour on the mine is constructed. Selected behavioural categories are analysed for different combinations of mine content and outcome of the visit to the mine. The assessment of the mine content is done in a differential way, quickly and without mistakes.
5. The results are discussed in the context of two environmental factors, wind speed and temperature, which reduce the available time for searching. They are also related to the growing percentage of unsuitable hosts during each host generation. Tentiform mines remain attractive for a long period of time, even after parasitism or emergence of the adult, and their examination reduces the rate of host discovery.     

Energy,predators and the behavior of feeding hummingbirds

Summary Current evidence suggests that many animals trade off energy gain against the risk of predation while feeding. In contrast, energetic considerations alone have proven successful in explaining and predicting the behaviour of feeding hummingbirds. This success may reflect the relative lack of natural predation on hummingbirds, but this study suggests that it may additionally reflect the lack of studies taking a predation perspective. In particular, when Anna's hummingbirds (Calypte anna) are faced with an obstructed view of their surroundings, they engage in behaviour suggestive of anti-predatory vigilance. In doing so, they voluntarily reduce their rate of energy intake. These birds also forgo better feeding opportunities that occur close to the ground, where observations suggest they are wary of opportunistic predators such as roadrunners (Geococcys californianus). While energy-based concepts will remain useful in the study of hummingbird feeding behaviour, the lack of predation on these birds should not be equated with an insensitivity to the risk of predation. This realization may lead to further insights into hummingbird-plant interactions, and hummingbird biology in general.     

Polymorphism, distribution, and segregation of AFLP markers in a doubled haploid rice population

We exploited the newly developed amplified fragment length polymorphism (AFLP) technique to study the polymorphism, distribution and inheritance of AFLP markers with a doubled haploid rice population derived from ‘IR64’/‘Azucena’. Using only 20 pairs of primer combinations, we detected 945 AFLP bands of which 208 were polymorphic. All 208 AFLP markers were mapped and distributed over all 12 chromosomes. When these were compared with RFLP markers already mapped in the population, we found the AFLP markers to be highly polymorphic in rice and to follow Mendelian segregation. As linkage map of rice can be generated rapidly with AFLP markers they will be very useful for marker-assisted backcrossing. Received: 11 April 1996 / Accepted: 14 June 1996     

Competition between Bufo larvae in a eutrophic pond

Competition between larvae of two anuran species (Bufo bufo and B. calamita) was investigated under field conditions likely to disfavour cell-mediated interference mechanisms. The experiment used triplicated cage treatments in an unshaded farm pond, a poor habitat for the unicellular pathogen Anurofeca richardsi implicated in interference competition between these anurans in sand dune ponds. The farm pond experienced lower maximum temperatures than a nearby dune pond but sustained larger numbers of eukaryotic algae and therefore had higher primary productivity. Survival and growth of B. calamita larvae were inversely related to density in all treatments but interspecific effects were much more severe than intraspecific ones. There was no evidence of A. richardsi in any treatment and competition between the Bufo larvae was therefore intense in the absence of Anurofeca-mediated interference effects. Anuran larvae reduced the standing crop and altered the community composition of algae in the treatment cages but larval growth rates were not simply related to food availability. Algal cell numbers in larval guts, a measure of food acquisition, were however inversely related to tadpole density in both species. Feeding niche overlap was high but decreased as larval density increased. Resource competition was implicated as the most probable major mechanism. Received: 1 September 1999 / Accepted: 20 January 2000     

Efficacy of the parasitoid,Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae) against Myzus persicae (Sulzer) (Hemiptera: Aphididae) infesting rapeseed-mustard

Efficacy of Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae) was determined by studying its biological and behavioural attributes on the aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Total developmental duration of the parasitoid was longer in younger instars compared to that in older instars of aphid. Host age negatively affected the oviposition period and fecundity of the ovipositing parasitoid. Survival of the immatures was higher in older than the younger instars of the aphid. Sex ratio for the parasitoid was female-biased. Longevity of female parasitoid was higher while parasitizing aphid nymphs of younger age groups (1–2 days old) compared to that of older age groups (4–5 days old). Parasitoid showed a higher preference towards second instar of M. persicae both in choice and no-choice tests. Results on mutual interference revealed that per capita searching efficiency decreased from 0.91 to 0.07 as parasitoid densities increased from 1 to 8. Logistic regression exhibited a type II functional response for D. rapae. The estimated values of search-efficiency (a) and handling time (T_h) were 0.038 h⁻¹ and 1.59 h, respectively. The maximum parasitization rate was 15.08. This investigation suggests that D. rapae could be an effective candidate for augmentative biological control of M. persicae which infests several plant species of economic importance.     

The importance of scale of patchiness for selectivity in grazing herbivores

The notion that spatial scale is an important determinant of foraging selectivity and habitat utilization has only recently been recognized. We predicted and tested the effects of scale of patchiness on movements and selectivity of a large grazer in a controlled field experiment. We created random mosaics of short/high-quality and tall/low-quality grass patches in equal proportion at grid sizes of 2×2 m and 5×5 m. Subsequently, we monitored the foraging behaviour of four steers in 16 20×40 m plots over 30-min periods. As predicted on the basis of nutrient intake maximization, the animals selected the short patches, both by walking in a non-random manner and by additional selectivity for feeding stations. The tortuosity of foraging paths was similar at both scales of patchiness but selectivity was more pronounced in large patches than in small ones. In contrast, the number of bites per feeding station was not affected by patch size, suggesting that selection between and within feeding stations are essentially different processes. Mean residence time at individual feeding stations could not be successfully predicted on the basis of the marginal-value theorem: the animals stayed longer than expected, especially in the less profitable patch type. The distribution of the number of bites per feeding station suggests a constant probability to stay to feed or to move on to the next feeding station. This implies that the animals do not treat larger patches as discrete feeding stations but rather as a continuous resource. Our results have important implications for the application of optimal foraging theory in patchy environments. We conclude that selectivity in grazers is facilitated by large-scale heterogeneity, particularly by enhancing discrimination between feeding stations and larger selection units. Received: 1 March 1999 / Accepted: 14 July 1999     

Flow cytometric analysis of the chromosomes and stability of a wheat cell-culture line

A rapidly growing, long-term suspension culture derived from Triticum aestivum L. (wheat) was synchronized using hydroxyurea and colchicine, and a chromosome suspension with chromosomes was made. After staining with the DNA-specific fluorochromes Hoechst 33258 and Chromomycin univariate and bivariate flow-cytometry histograms showed 15 clearly resolved peaks corresponding to individual chromosome types or groups of chromosomes with similar DNA contents. The flow karyotype was closely similar to a histogram of DNA content measurements of Feulgen-stained chromosomes made by microdensitometry. We were able to show the stability of the flow karyotype of the cell line over a year, while a parallel subculture had a slightly different, stable, karyotype following different growth conditions. The data indicate that flow cytometric analysis of plant karyotypes enables accurate, statistically precise chromosome classification and karyotyping of cereals. There was little overlap between individual flow-histogram peaks, so the method is useful for flow sorting and the construction of chromosome specific-recombinant DNA libraries. Using bivariate analysis, the AT:GC ratio of all the chromosomes was remarkably similar, in striking contrast to mammalian flow karyotypes. We speculate about a fundamental difference in organization and homogenization of DNA sequences between chromosomes within mammalian and plant genomes. Received: 24 April 1996 / Accepted: 24 May 1996     

Intraguild predation on the parasitoid Aphidius ervi by the generalist predator Harmonia axyridis: the threat and its avoidance

Interactions between natural enemies can be crucial for determining their overall control of pest species, yet the mechanisms that govern such interactions are often poorly understood. The risk of negative effects such as intraguild predation and the possibility of mitigating such risks are important components for ultimately determining the compatibility of biological control agents. We performed a group of experiments to determine whether the coccinellid Harmonia axyridis Pallas (Coleoptera: Coccinellidae) poses an intraguild threat to the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae) and to see whether A. ervi is able to avoid predation by responding to the chemical tracks deposited by H. axyridis. We show that although H. axyridis does not readily consume A. ervi mummies, it preferentially consumes parasitized aphids over unparasitized aphids. We also show that A. ervi can defend against this threat by avoiding oviposition in the presence of H. axyridis chemical tracks. Aphidius ervi parasitized far fewer pea aphids Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) on plants [Vicia faba L. (Fabaceae)] with H. axyridis chemical tracks in a no‐choice environment at a single‐plant scale. Similarly, when parasitoids could move freely between plants with and without tracks, A. ervi parasitism was higher on plants without tracks. Behavioral observations of A. ervi foraging suggested that this might be because of reduced A. ervi attack rates and patch residence times in the presence of H. axyridis tracks. Despite a risk of intraguild predation by H. axyridis, our study suggests that A. ervi may be able to mitigate this risk by altering its behavior in response to chemical cues.     

Children's competition in a natural setting: evidence for the ideal free distribution

Little is known of the foraging abilities of children in modern cultures, especially when children forage in groups. Here we present a test of optimal foraging theory in groups of street children working for money. The children we observed were selling bottles of water to drivers distributed in two lanes at a crossroad of Istanbul, Turkey. As predicted by the ideal free distribution (a model of optimal group foraging), the ratio of children working in the two lanes was sensitive to the ratio of cars (and therefore the ratio of potential buyers) present in each lane. Deviations from the ideal free model arose largely from numerical restrictions on the set of possible ratios compatible with a small group size. When these constraints were taken into account, optimal behavior emerged as a robust aspect of the children's group distribution. Our results extend to human children aspects of group foraging that were previously tested in human adults or other animal species.     

Patch choice from a distance and use of habitat information during foraging by the parasitoid Ibalia leucospoides

1. In environments in which resources are distributed heterogeneously, patch choice and the length of time spent on a patch by foragers are subject to strong selective pressures. This is particularly true for parasitoids because their host foraging success translates directly into individual fitness. 2. The aim of this study was to test whether: (i) females of the parasitoid Ibalia leucospoides (Hymenoptera: Ibaliidae) can discriminate among patches according to host numbers; (ii) the surrounding context affects the initial choice of patch, as well as time spent on patch; and (iii) the perceived quality of a given patch is affected by the quality of the surrounding patches. 3. Each female was randomly exposed to one of three different three‐patch environments which differed in host number per patch, mean environment host number and host distribution among patches. For each treatment level, the first patch chosen and the time allocated to each patch visited by the female were recorded. 4. Females of I. leucospoides were able to discriminate different levels of host numbers among patches from a distance. The patch bearing the highest number of hosts was, predominantly, the first choice. Patch host number in association with mean habitat profitability influenced the length of time spent on the first patch visited. By contrast, variance in habitat profitability did not influence time allocation decisions. Contrary to the study prediction, there were no significant habitat‐dependent time allocation differences among patches holding the same number of hosts. 5. The results indicate that, for I. leucospoides, patch exploitation decisions are partially influenced by information obtained from the habitat as a whole, a behaviour that may prove to indicate adaptive ability in highly patchy environments, as well as suggesting the presence of good cognitive abilities in this parasitoid species.     

The role of vision and color in the close proximity foraging behavior of four coccinellid species

The role of vision and color in close-proximity foraging behavior was investigated for four species of lady beetles: Coccinella septempunctata, Hippodamia convergens, Harmonia axyridis, and Coleomegilla maculata. The effect of light level and color cues on consumption rates varied among the four predator species. The consumption rates of these predators on the pea aphid Acyrthosiphon pisum (Harris) was measured under light and dark conditions. C. septempunctata,H. convergens, and Ha. axyridis consumed significantly more aphids in the light than in the dark, while the consumption rate of Col. maculata was not affected by light level. Foraging ability was also measured on red and green color morphs of the pea aphid on red, green, and white backgrounds. C. septempunctata consumed significantly more of the aphid morph that contrasted with the background color, and showed no difference between morphs on the white background. H. axyridis consumed significantly more red morph aphids regardless of background. The remaining two species showed no difference in consumption rates on the two color morphs. The variation in the use of visual cues demonstrates how different species of predators can exhibit different foraging behaviors when searching for the same prey. Received: 4 August 1997 / Accepted: 3 February 1998     

Community structure and stability analysis for intraguild interactions among host, parasitoid, and predator

Intraguild predation (IGP) occurs when one species preys on a competitor species that shares a common resource. Modifying a prey–predator model with prey infection, we propose a model of IG interactions among host, parasitoid, and predator, in which the predator eats parasitized and unparasitized hosts, and the adult parasitoid density is explicitly expressed. Parameter dependences of community structure, including stability of the system, were analytically obtained. Depending on interaction strength (parasitization and predation on unparasitized and parasitized hosts), the model provides six types of community structure: (1) only the host exists, (2) the host and predator coexist stably, (3) the host and parasitoid coexist stably, (4) the host–parasitoid population dynamics are unstable, (5) the three species coexist stably, and (6) the population dynamics of the three species are unstable. In contrast to a traditional prey–predator model with prey infection, which predicts that population dynamics are always locally stable, our model predicts that they are unstable when the parasitization rate is high.     

Food uptake and fine structure of Cryothecomonas longipes sp. nov., a marine nanoflagellate incertae sedis feeding phagotrophically on large diatoms

Cryothecomonas longipes Schnepf and Kühn sp. nov. is a colourless biflagellate organism, 9–14 μm long and 7–9 μm wide when not filled with food vacuoles. It was detected in the North Sea, feeding with pseudopodia on diatoms. It penetrates the host shell, while the main body of the flagellate remains outside the frustule. Cells are covered with a multilayered theca. The pseudopodium protrudes through a preformed slit in the theca. Each flagellum also emerges through a pit in which the theca forms a funnel of complex structure that girdles each flagellum. The anterior flagellum is 9–15 μm long and oriented forward; the ventral flagellum, posteriorly directed, is 20–24 μm long and bears fine hairs. The flagellar roots consist of microtubules that emerge at satellites around the basal bodies and run along the flagellar pits. In addition, the ventral flagellum is accompanied by a band of six microtubules. It is proximally attached to a small fibrillar band, which interconnects the basal bodies. Cryothecomonas longipes has two or three types of extrusomes which pierce the theca when discharged. Their mode of discharge is discussed. Microbody-like vesicles containing small tubules are closely associated with older digestion vacuoles. Cryothecomonas longipes is compared with other species of the genus and a diagnosis is given. Received: 4 March 1999 / Received in revised form: 28 July 1999 / Accepted: 30 August 1999     

Abundance of Aphis gossypii (Homoptera; Aphididae) and its main predators in organic and conventional cotton fields in north‐west China

Understanding how natural assemblages of predators are affected by organic agriculture, and whether these changes can contribute to biological control, is important for the design of Integrated Pest Management (IPM) strategies and sustainable agriculture. The effect of organic management practices on the abundance of the cotton aphid Aphis gossypii and its major predators was evaluated in northwestern China during the cotton‐growing seasons of 2004–2006. The predators of A. gossypii in cotton fields included Coccinellidae (ladybirds), Chrysopidae (lacewings), spiders (Linyphiidae and Thomisidae) and Syrphidae (hoverflies). Higher peak densities and longer persistence of predators in organic fields were found, and the average annual densities of all predators except Chrysopidae adults were higher, on average by 200%, in organic fields than in conventional fields in all 3 years. The abundance of larvae of Coccinellidae, Chrysopidae and Syrphidae was higher in organically managed crops indicating that these predators bred more successfully in organic fields. Although there was a significant difference between A. gossypii abundance in organic and conventional fields each year, taken over the three‐year period as a whole there was no significant difference. This suggests predation by natural enemies in organic fields can achieve the same efficacy in aphid control as pesticides used in conventional fields over the long term, but that predation does not prevent outbreaks of A. gossypii in some years.