Prey or host searching behavior that leads to a sigmoid functional response in invertebrate predators and parasitoids

Invertebrate predators and parasitoids have long been characterized as having a hyperbolic (Type 2) functional response. Modifications were made to Holling's sand paper disc experiment which consisted of limiting the initial period of search during which a host must be contacted. Failure to contact a host during this initial period causes the predator to emigrate from the search area. The modification generated a sigmoid (Type 3) functional response. This response resulted from the low probability of encountering a host during the initial period of search at low host densities in the time allotted. A limited period of search has been found in several insect parasitoids. Such a strategy would minimize the time (energy) spent per offspring produced by minimizing the time invested in searching microhabitats in which hosts are scarce or absent.     

Functional response and searching efficiency inPseudogonatopus flavifemur Esaki and Hash. (Hymenoptera: Dryinidae), a parasite of rice planthoppers

The functional response of Pseudogonatopus flavifemur E & H (Hym., Dryinidae) was investigated by offering hosts (brown planthopper) at densities ranging from 8 to 160 per cage. The response curve was found to be sigmoid, i. e.Holling 's (1959) Type III curve. In experiments involving 310 hosts per cage distributed unevenly in 5 densities (10, 20, 40, 80 and 160 per hill), and a different female parasite density each time (viz. 1, 2, 4, 8 or 16 per cage), the behavioral response was described well by the “random predator equation” ofRoyama (1971) andRoger (1972), which is a convex exponential curve. The area of discovery (a) decreased with an increase in female parasite density (P), and the relationship was described by the equation: log a=−1.0099−0.3638 log P. There was an apparent increase in handling time per host as the number of female parasites increased. Superparasitism, a rare phenomenon under natural conditions, was often observed in the laboratory. The potential of P. flavifemur as a biocontrol agent of the brown planthopper is discussed.     

Role of a parasitoid with a low fecundity,Praestochrysis shanghaiensis (Hymenoptera: Chrysididae), in the population dynamics of its host

1. Analysis of life tables of the oriental moth, Monema flavescens, obtained for 8 generations over 4 years, disclosed that the cocoon parasitoid, Praestochrysis shanghaiensis, acted as a density-disruptive factor.
2. The density of the host cocoon remained stable (max./min.=3.2), whereas that of the host adult varied (max./min.=14.3) although both showed similar fluctation patterns.
3. Stability of the host population was associated with the density-dependence in the ratio of first generation cocoons to overwintered generation moths, which was the key factor for the rate of change throughout the year. Chrysidid parasitism among the first generation cocoons ranged from 37.7 to 70.1%, and that among the second generation cocoons from 16.7 to 63.2%, each showing an inverse density-dependence and acting as the main determinant (key-factor) of the between-year variation in the density of the adult moths.
4. The density-dependence of the rate of change from overwintered generation adults to first generation cocoons was so strong that the parasitism on the second generation hosts had not effect on the cocoon density of the first generation. On the other hand, the density-dependence of the rate of change from first generation adults to second generation cocoons was weak, and the parasitism on the first generation hosts became the key factor for the between-year variation of the second generation cocoons.
5. It is suggested that the stability of the parasitoid-host system will be disrupted without three parasitism-restricting factors: asynchrony in the parasitoid attack on the second generation hosts, high mortality among parasitoid larvae of the second generation, and the high proportion of those first generation parasitoids that enter diapause. These factors are considered to be effective only in cooler parts of the distribution of the parasitoid.

     

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.     

Ambient temperature affects mechanosensory host location in a parasitic wasp

Certain parasitic wasps (Ichneumonidae, Pimplinae) use self-produced vibrations transmitted on plant substrate to locate their immobile concealed hosts (i.e. lepidopteran pupae). This mechanosensory mechanism, called the vibrational sounding, depends both on physical cues of the environment and physical activity of the parasitoid and is postulated to depend on ambient temperature. We analysed the influences of temperature on vibrational sounding by choice experiments using plant-stem models with hidden host mimics in the temperate species Pimpla turionellae. The results show a significant effect of temperature on host-location activity and on the success of this process. Outside an optimum range, the performance of the wasps decreased both at low and high temperatures. Below 10°C and beyond 24°C, the wasps displayed (1) substantial reduction in responsiveness, i.e. proportion of females showing ovipositor insertions, (2) reduction of quantitative activity with ovipositor insertions in the individuals, and (3) reduced precision of mechanosensory host location. Nevertheless, female wasps were able to locate their host over a surprisingly broad range of ambient temperatures which indicates that the wasps are able to compensate for temperature effects on vibrational sounding.     

Host-attacking behavior of a eulophid parasite,Kratochviliana sp., to the leaf mining host,Phytomyza ranunculi (Diptera: Agromyzidae) during its stay on the leaf

The present paper studies how the female parasite of Kratochviliana sp. visits and attacks its host larvae of Ranunculus leaf mining fly, P. ranunculi at a single leaf visit. The parasite visited its hosts at random on the leaf. The frequency of host visits was independent of the host density and the proportion of hosts survived from the parasite attack, in a leaf and its distribution was expressed as a single straight line. It almost always attacked living hosts at the first host visit after isolated from them for one day but with the rate of about 0.5 at the subsequent visits. In consequence, the relationships of the number of host attacks and killed hosts to the host density drew satulated curves in each. A model of host attack by this parasite at its single leaf visit was formulated by modifyingBakker et al.'s model (1972) basing upon these observations and the attack avoidance by the parasite to already attacked hosts previously reported.     

Functional response,numerical response,and stability in arthropod predator-prey ecosystems involving age structure

Summary A general model of arthropod predator-prey systems incorporating age structure in the predator is employed to study the role of functional and numerical responses on stability and the paradox of enrichment. The destabilizing effect of age structure leads to both qualitatively and quantitatively new results for an environment which has an infinite prey carrying capacity, including a lower bound to prey density for a stable equilibrium, a feature not present in models without age structure. When applied to an environment with finite prey carrying capacity, the effect of age structure is to reinforce the arguments implicit to the paradox of enrichment originally developed for traditional models lacking age structure.     

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.     

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.     

Searching preference of the parasitoid,Anisopteromalus calandrae (Howard) for different stages of the host,Callosobruchus maculatus (F.) in the laboratory

The functional response parameters of the parasitoid, Anisopteromalus calandrae (Howard ) to the third instar, the fourth instar and the pupae of Callosobruchus maculatus (F.) were estimated from the Random Parasitoid Equation. By modifying this equation for a two host situation and using the parameters estimated above, a no switch model could be obtained. This model was then used to test for switching. In the preference experiments where two stages of the host were presented to the female parasitoid, a definite preference for the fourth instar followed by the pupa and the third instar, respectively was shown. There was, however, no evidence of switching. There was also no evidence that the data fitted the no switch models which suggests that when the parasitoid is searching in an environment with two or more hosts, its searching behaviour is more complex.     

The effect of prey size and prey density on the functional response,survival, growth and development of a predatory pentatomid bug,Podisus maculiventris say

Two experiments on the nymphal predation of Podisus maculiventris were conducted using Spodoptera litura larvae as prey. First experiment: The predator nymphs divided into three groups were reared individually from second instar to adult in a small vessel. Each nymph in the groups 1, 2 and 3 was allowed to attack the serially growing larvae (these were supplied at the rate of one per day) from 3-, 5- and 7-day old after hatching, respectively. The first prey used for the group 1 was so small that it was not only insufficient to satiate the predator but also was difficult to be searched out. But these disadvantages were soon recuperated due to the rapid growth of the prey and all nymphs could survive to adults. The survival rate of third and fourth instar nymphs in the group 3 was severely affected by vigorous counterattack of older prey larvae. Second experiment: The predator nymphs were individually reared either in a small vessel or in a large one at various rates of food supply (the prey larvae of 7-day old were used). The functional response curves obtained for each instar of the predator took a saturation type within a certain range of the prey density. The saturation level specific to each instar was generally higher for the predator reared in the large vessel than in the small one. The functional response of fourth and fifth instar nymphs was accelerated at a high prey density, viz. 16 larvae per vessel. Even at the low rate of food supply, viz. one larva per day per predator, the predator nymphs could survive to adults, but the size of resultant adults were abnormally small.     

Effect of wasp size, physiological state, and prior host experience on host-searching behavior in a parasitoid wasp (Hymenoptera: Ichneumonidae)

Host-searching behavior in insects generally varies among individuals. A number of physiological and environmental factors can be involved in such individual variation. Here, a series of behavioral observations were made to highlight the importance of physiological state (i.e., number of mature eggs a female carries, amount of nutrient reserves, etc.) and learning state (i.e., prior host experience) on host-approaching behavior of parasitoids. Itoplectis naranyae (Hymenoptera: Ichneumonidae), a solitary endoparasitoid wasp attacking lepidopteran pupae and prepupae, was used as a test insect. The results show that female wasps with experience ovipositing on hosts 2 days before the test found hosts more quickly than did naïve wasps. Prior experience of host odor itself did not affect host-finding behavior, however. A single oviposition was enough for wasps to shorten time to find a host; additional experience had no significant effect on the efficiency of searching. The number of mature eggs a female carried had no effect on the time required to find a host regardless of prior host experience. The size of wasps, instead, was a significant factor when wasps had no prior host experience, and larger wasps found hosts more rapidly than did smaller wasps. Searching activity was not affected by how many hosts a female wasp had fed on before testing.     

Demographic dynamics of Platygaster demades in response to host density

Platygaster demades Walker (Hymenoptera: Platygastridae) is the only hymenopteran parasitoid of apple leaf-curling midge, Dasineura mali Kieffer (Diptera: Cecidomyiidae), in New Zealand. Prior to the present study the mechanisms behind the parasitoid–host density interactions were poorly understood. In this study we carried out both laboratory and field experiments to determine the response of P. demades to D. mali density. In the laboratory, when only a single parasitoid was allowed to forage D. mali eggs of a given density, P. demades displayed a Type II functional response leading to an inverse density-dependent parasitism. However, P. demades showed a Type III functional response in the field where females were able to freely search and disperse between apple shoots infested with D. mali eggs of different densities. As a result, the Type III response reflects a more realistic nature of P. demades in response to D. mali density. Our results also indicate that the numeric response and mutual interference in P. demades significantly contributed to the stability of the parasitoid–host system. The density-dependent parasitism in a host range of 50–300 D. mali eggs per apple shoot suggests that P. demades is highly efficient in controlling D. mali populations of the first, third and fourth generations and when necessary, argumentation measures may be taken before the onset of the second generation.     

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.     

Life table studies on the paddy field population of the green rice leafhopper,Nephotettix cincticeps Uhler (Hemiptera: Cicadellidae), with special reference to the mechanism of population regulation

The population growth of the green rice leafhopper, Nephotettix cincticeps, in the paddy field was analyzed based on the life table data accumulated for six years. The paddy field population, which stems from the invading adults of the first generation (G-I), repeats two complete generations, and the hatchlings of the fourth generation (G-IV) enter diapause and overwinter as the fourth instar nymphs in fallow paddy fields. It was clarified that the density dependent reduction in the mean longevity and oviposition rate of adult females in G-II and III played a primary role in stabilizing the annual population densities. The annual average of the mean longevity of G-II females (3.9 days) was much shorter than that of G-III ones (7.7 days) and thus the density dependent reduction in the mean longevity induced a more prompt regulatory effect on the oviposition of G-II females compared with G-III ones. As the result, two equilibrium densities of eggs were obtained, e.g., ca 100 and 700 eggs per hill in G-III and IV, respectively. Density dependent decrease in the proportion of mature females in the adult population was especially conspicuous in G-II, and this was closely associated with the density dependent reduction in the mean longevity and fecundity. Thus, the density dependent dispersal (emigration) of the adult females by flight in G-II and III was the most convincing factor in the process of population regulation. The density dependent dispersal of the adult females is effective in avoiding the deleterious effects of nymphal crowding in a breeding habitat unit (a paddy field), and may result in a more even distribution of the population over a continuous habitat units in a locality than otherwise.     

Models of the spatial pattern of egg population of Ranunculus leaf mining fly,Phytomyza ranunculi (Diptera: Agromyzidae), in host leaves

This paper considers two kinds of model of the spatial pattern of egg distribution of the Ranunculus leaf mining fly, Phytomyza ranunculiSchrank , as a step to determining the effect of the distribution upon the parasitism of this species by the eulophid parasite, Kratochviliana sp.. Each model incorporates submodels in several important stages of both the processes of visiting and subsequent oviposition by the fly. Model 2 is more general than model 1, because the former also includes the effect of oviposition restraint. Both models fitted well the egg distribution on fresh plants and on exploited plants. The fitting similarity on exploited plants is due to the fact that there were not so many heavily exploited leaves which lead to oviposition restraint, owing to the low density of mature larvae contained in the leaves. These models will be applicable to the distribution of larvae as well as eggs, because most larvae remain in the leaf where they occurred as eggs, until emerging just before pupation. This paper also discusses by use of these models the fact that this fly tends to effectively avoid excessive oviposition in leaves by laying fewer eggs per visit and visiting leaves more sparsely and also by refraining from further oviposition on leaves exploited heavily by mature larvae.     

Ecological studies on the population of isaza,Chaenogobius Isaza Tanaka,in Lake Biwa,with special reference to the effects of population density upon its growth

1. In order to get the knowledge on the age composition of “isaza” population in Lake Biwa and the effect of population density on growth, monthly distribution of mean body length and mean body weight has been analyzed on the basis of monthly haul by “isazabiki” trawl during 1949 to 1953 and also 1960 to 1965.
2. There is no apparent sex difference in the growth in the first and second years of life.
3. “Isaza” population is composed of two age groups, age 0 and 1 groups (1+fish), the latter occupying by far the greater part in commercial catch.
4. During the growth season fishes of both ages feed mainly on zooplankton, though in winter frequently take chironomid larvae, gammaridae and others in volume.
5. The growth season falls in the period from April to October in both age groups.
6. A considerable yearly variation occurring in growth is in close connection with the fluctuation of population density of all ages.
7. The influence affected by the density of age 1 group is larger than that by age 0 group.

     

Population regulation of a mosquitoArmigeres theobaldi with description of the animal fauna in zingiberaceous inflorescences

1. Inflorescences of some Curcuma and Zingiber (Zingiberaceae) in tropical Asia provide an unique aquatic habitat being discrete, small, and made of numerous smaller compartments (the bracts).
2. The aquatic community in inflorescences of Curcuma in northern Thailand was composed of immature Diptera, of which the biting midge Dasyhelea and the mosquito Armigeres theobaldi were the commonest. No important competitors, predators or pathogenic parasites for the mosquito were confirmed.
3. Inter-inflorescence distribution of the mosquito was contagious. Within each inflorescence, the fourth-instar larvae or pupae usually occupied bracts singly.
4. The k-value analysis detected density-dependent mortality due to contest competition in the mosquito larvae.
5. Variations in the larval and pupal mosquito size were density-independent and remarkably small as compared with size variations known for other mosquitoes.
6. These population attributes (large density-dependent mortality with density-independent, minimally variable individual size) appear unique among mosquitoes, arising from conspecific killing, efficient foraging (inter-bract movement by crawl and single occupation of bracts), and availability of host plant tissues as supplementary food.
7. A simple population model suggested that a small proportion of adult females lay eggs.