Searching Behavior in Parasitoids and Predators
Allen Bradbury
Abstract
Bell (1990) defined searching behavior as "an active movement by which insects
seek resources." In complex environments, how do parasitoids and predators seek
essential resources such as food, mates, oviposition sites, nesting sites, and
refuges? ( In this review, the topic is confined to prey and host searching
behaviors.) Insects are constrained in their searching by the spatial and temporal
distribution of resources. An insects searching behavior is defined by at least
three factors including: (i) its biological characteristics and abilities,
including sensory modalities and method of locomotion; (ii) the external
environment, both abiotic and biotic factors; and (iii) internal factors such as
deprivation. Once an insect begins searching for prey/host, its behavior may change
as it narrows the search. For example, larvae of aphidophagous coccinellids begin
with extensive searches, characterized by long linear paths and a fast speed. Once
prey is located and consumed, larvae exhibit intensive searches, which involve an
increase in angular speed and the number of stops and a lowering of linear speed.
Parasitoid wasps utilize semiochemicals, visual cues, and associative learning to
choose the most likely areas to find hosts. Female wasps learn to associate both
volatile and nonvolatile compounds with the presence of a host. Searching behavior
is not only an interesting scientific exploration but also a useful pest management
tool. Tritrophic interactions between plants, herbivores, and predators/parasitoids
suggests unique strategies to exploit the learning abilities of beneficial
insects.Introduction
Searching behavior is an important activity in the life of parasitoid and
predatory insects. Bell (1990) defined searching behavior as "an active movement by
which insects seek resources." Insects must acquire food, mates, oviposition sites,
nesting sites, and refugia sites for growth, development, and maintenance. Although
searching behavior is relevant to many aspects of an insect's life this discussion
will concern itself with prey searching in predators and host searching in
parasitoids.
The study of searching behavior generally falls into one of two categories, the
classical approach or the dynamic approach (Michaud and Mackauer 1994). Vinson
(1984) uses the classical or mechanistic approach in describing the factors
important in successful parasitoidism. He divides these factors into (a) host
habitat location, (b) host location, (c) host acceptance, (d) host suitability, and
(e) host regulation. Similarly, the components of the predation cycle include (a)
search for and locate prey (b) pursue and attack, and (c) handle and ingest (O'Brien
et al 1990). In essence, the classical approach simply answers the question how
animals forage. The dynamic approach is the same as optimality models. These types
of models "try to predict the particular combination of costs and benefits that will
ultimately maximize the individuals inclusive fitness" (Drickamer and Vessey 1992).
Optimality models assume that a foraging insect would try to maximize it's rate of
energy intake by making decisions about prey to consume or feeding in one particular
area versus moving to a new area. Each decision incurs either a benefit in terms of
energy gained, versus a cost such as time taken away from mating, defending
territory, or protecting nests. A criticism leveled at optimality models is the
failure to distinguish between predators and parasitoids and the differing
constraints to which they are subject (Carter and Dixon 1982).
Environmental Structure
Predators and parasitoids face a common dilemma in navigating through a complex
environment. Resources are distributed throughout the environment both temporally
and spatially. Even if an insect succeeds in searching at the right time, it must
find the necessary resources within a given volume of space. Researchers assume
that insects perceive their environment as a hierarchical system (Bell 1990). Three
general categories are the resource item, the patch, and the habit. A resource item
includes prey, hosts, mates, food, or shelter. A patch is an aggregation of
resource items. More specifically, a patch can be defined by the particular forager
as "an area containing a stimulus or stimuli that at the proper intensity elicit a
characteristic foraging activity in a responsive forager" (Hassell and Southwood
1978). The final level is a habitat, which is a collection of patches (Hassell and
Southwood 1978). By no means do these terms eliminate all confusion. For example,
consider the predator, Orius insidiosus, foraging on corn plants. A foraging O.
insidiosus will search corn silks first for corn earworm eggs then search leaves for
European corn borer eggs, but it never searches the tassel (Reid 1991). The field
is the habitat, but there are at least two levels of patchiness, first the corn
plant and second the corn leaves and silks where the two different egg types are
found.
Search Information
To negotiate the complex environmental structure, the process of natural
selection has endowed insects with unique biological characteristics and abilities.
Both predators and parasitoids use information obtained from the external
environment as well as internal cues. Diurnal carabid beetles use visual cues to
orient to the movement of prey (Bauer 1985). Other insects which utilize visual
information include Aphidius spp. wasps which distinguish between aphids on the
basis of color, movement, and species ( Michaud and Mackauer). Similarly,
Coccinella semptempunctata exhibits a strong response to yellow while Chrysoperla
carnea has a preference for yellow, green, and red (Maredia et al 1992). Parasitic
wasps use olfactory cues from both volatile and nonvolitile chemical sources to find
hosts (Tumlinson 1993). Euphasiopteryx ochracea, a tachinid, uses auditory cues to
find its host, the male cricket, Gryllus integer (Cade 1975). Another external cue
which influences search behavior is temperature. Different Carabid beetles
increased consumption rate of prey items at temperatures above 20øC (Wallin 1991).
Internal factors also play a role in insect search behavior. Information can
be derived from the proprioceptors located in or near the locomotory organs (Bell
1985). Genetically stored information characterizes both the individual and the
species. Searching behavior is probably controlled by a combination of factors
mediated from both the internal and external environment (Bell 1990).
Search Strategies
Smith (1974) defines a search strategy as "a set of basic rules of scanning and
locomotion which results in the effective encountering of a specific distribution of
food." There are three basic types of search strategies employed by predators.
First, cruise (O'Brien 1990), ranging (Jander, 1975) or extrinsic search (Bond
1980), this phase of searching is characterized by relatively straight locomotion
throughout the environment without information about potential resources (Bell
1985). In this case, the searching takes place while the insect is moving. This
type of strategy is associated with certain prey characteristics, large prey size,
relative to predator, and prey with a defense strategy of speed or hiding (O'Brien
1990). Adult tiger beetles, Cicindela spp., are an example of an insect using the
cruise strategy. Second, ambush or sit and wait predators remain stationary for
long periods of time waiting for prey to wander into their strike space, which is
the extreme opposite of cruise searching. In this case, searching takes place while
the predator is pausing for long periods of time. This type of behavior is
characteristic of predators which hunt relatively large prey which moves often, and
its major defense is its size (O'Brien 1990). Examples of ambush predators include
ant lions, which lie in wait at the bottom of their excavation pit, and praying
mantids, which remain motionless on branches waiting for prey. Either predator may
move its ambush site after a certain period without success. The third and most
common search strategy is the saltatory search. Predators which employ this
strategy alternate between periods of stationary scanning of the environment with
repositioning movements through the environment (O'Brien 1990). Two species of
Carabid beetles, Bembidion lampros and Pterostichus cupreus, exhibit this type of
strategy when hunting the cereal aphid, Rhopalosiphum padi. Both beetles exhibit a
pattern of running or walking and stopping to search for aphids (Chiverton 1988).
This strategy is a characteristic search strategy when the prey is small relative to
the predator, moves very little, and its major defense strategy is hiding (O'Brien
1990).
For parasitoids, the task of finding a habitat which contains patches with
suitable host for oviposition involves a more directed search. Certainly, the
specialized lifestyles of insect parasitoids creates a great deal of variation
within the group. Parasitoids may use olfactory, visual, and host vibrational-
stimuli as cues to narrow the search for hosts (Vet et al 1991; Vinson 1984). One
or more modalities can be useful depending upon the characteristics of the host's
ecology. A useful concept is the tritrophic system, which relates three levels of
energy movement throughout the system of plants, phytophagous insects, and their
natural enemies (Vet and Groenewold 1990). Important information is available for
the parasitoid from both the first and second trophic levels. By eavesdropping on
the chemical communication of plants and phytophagous insects, parasitoids can
detect the presence of potential hosts. However, a major constraint is low-
detectability of host-derived information at long distances (Vet et al 1991).
Therefore, parasitoids must use less reliable sources of information such as the
semiochemicals produced by the plant or from the feeding activity upon the plant,
visual cues such as shape or color, or vibrational cues (Vet 1991; Vinson 1984). (It
should be noted that predators deal with these constraints in similar ways during
searching.)
Parasitoids have evolved at least three strategies to exploit the tritrophic
system. The first strategy is called the infochemical detour. This involves using
information from a more detectable stage in the host insect's lifecycle. For
instance, Opius lectus an egg and larval parasitoid of Rhagoletis pomonella
exploits the oviposition-deterring pheromone of the adult R. pomonella (Prokopy and
Webster 1978). The second strategy is called herbivore-induced synomones, which
refers to the ability of parasitoids to respond to the emission of plant volatiles
from insect herbivore damaged plants. For example, corn plants damaged by
Spodoptera caterpillars release volatile attractants for the parasitoid Cotesia
marginiventris (Turlings et al 1990; Vet et al 1991;Tumlinson 1993). The third
strategy is called associative learning. Parasitoids are very good at learning to
associate different cues. The benefit of learning is that they can associate easily
detectable cues, such as plant volatiles, to more reliable but harder to detect
stimuli, such as host specific odors (Vet 1991). Further studies have indicated
that female parasitoids can learn to respond to a novel odor (Vet and Groenewold
1990). One implication of associative learning, is that insectary raised
parasitoids may be trained in the laboratory to improve initial foraging success
(Tumlinson 1993).
Search Tactic
A search tactic is "an adaptive change in scanning or locomotion occurring once
a predator has arrived in a specific area where prey are available" (Smith 1974).
Insects often employ a local search (Jander 1975), intrinsic search (Bond 1980), or
area- restricted search (Curio 1976). This tactic "involves an increase in turning
rate (klinotaxis), an increase in scanning movements, and a reduction in searching
speed (orthokinesis) around the feeding point" (Carter and Dixon 1982). Lady
beetles such as Hippodamia convergens larvae (Hunter 1978), Coccinella
septempunctata adults (Nakamuta 1985), and Semiadalia undecimpunctata larvae (Ferren
et al 1994) exhibit an area-restricted search within the immediate vicinity of the
prey capture site. Using video-computer tracking, Ferren et al (1994) studied
switching from extensive to intensive (area-restricted) searching in Semiadalia
undecimpunctata larvae. Significant differences were found between individuals in
the number of stops, distance traveled, linear speed, and angular speed. The
average duration of intensive search was approximately six minutes before extensive
search resumed. Generally, the larvae adopted an intensive search pattern after
feeding, however, some (16%) adopted an intensive search pattern only later (>180
seconds), while others (11.3%) never adopted an intensive search. These
observations suggest that these predators are able to adapt to short-term changes in
the environment, such as prey distribution (Ferran et al 1994). Nakamuta (1985)
examined the cues which elicit switchover from extensive to area-concentrated search
in Coccinella septempunctata. Giving-up time or the elapsed time from end of
feeding to beginning of extrinsic search were measured for each insect. Adult lady
beetles were either fed a large prey first and a small prey second or vice versa.
Results revealed a significant difference between giving-up times which indicates
that adult lady beetles have a shorter intensive searching period if they consume a
large prey item first and a small prey item second. Further, it was found that
switchover from intensive search to extensive search was due to prey contact rather
than prey consumption.
Adult female green lacewings, Chrysoperla carnea, alter their searching
behavior after contact with honeydew of the black scale Saissetia oleae. There is a
characteristic reduction in mean walking speed, an increase in turning speed, and
an increase in turning angle. Adult C. carnea are non-predatory but utilize
honeydew as a major food source and often oviposit near black scale colonies(McEwen
et al 1993).
Carabid beetles, Calosoma affine, respond to differing prey densities, of
alfalfa caterpillar and armyworms, by altering their movement pattern and foraging
speeds. Diode tagged beetles were tracked with a portable radar system in low prey
density settings and high prey density settings. Turning angles and move lengths
were recorded for hungry and satiated beetles. Results indicated that hungry
beetles in low prey densities displayed directed movements (extensive searching),
characterized by high speed, little turning, and covered long distances. With
increased prey density hungry beetles changed movement patterns to a correlated
random walk (area-restricted search) with low speed, frequent turning, and short net
displacement. Conversely, satiated beetles displayed a correlated random walk in
both low and high prey density situations (Wallin 1991). This demonstrates the
importance of internal factors (e.g. hunger) on the decision to switch from
extensive to intensive searching.
Search Mechanisms
Both predators and parasitoids are faced with the decision to either leave a
patch or continue searching a patch. Bell (1990) lists four decision rules that may
be used by an insect to remain within a patch. The first, as previously shown, is
the decision to restrict searching to the current patch after resource utilization
(e.g. feeding). The insect adopts a turning bias, turning sharply either left or
right, but over time, if resources are not encountered the search path becomes
straighter. The second decision rule is to decrease movelength or move only short
distances before stopping to scan. If resources are not encountered the movelength
gradually increases. The third decision rule directs the insect to leave the
resource patch in a direction that differs from the arrival direction. The fourth
decision rule is to turn back when the edge of the patch is detected (Bell 1990).
For example, when the parasitic wasp Nemeritis canescens is placed on a glass plate
bearing a patch of a chemical produced by its host, Plodia interpunctella, it turns
sharply upon reaching the edge of the secretion. This turning decision functions to
bring the wasp back into the patch (Waage 1978).
How long should a forager search within a patch? Four different mechanisms are
proposed for the decision to leave a patch. First, a forager may leave after a
fixed number of food items have been captured. Second, a forager may leave after a
fixed amount of time has passed. Third, a forager may leave after a fixed searching
time, in other words, spend only a constant amount of time per patch. Fourth, a
forager may leave when the capture of food items falls below a fixed rate (Hassel
and Southwood 1978 after Waage PhD Thesis). Current literature lacks information
verifying these mechanisms.
Conclusion
One of life's major dilemmas is finding the resources needed for survival.
Insects in particular have a daunting task. Resources exist in a complex world
composed of predators, intraspecific and interspecific competitors. Resources are
removed in both time and space. To solve the problem of resource location insects
utilize both internal and external cues to negotiate the structure of the
environment. Various search strategies are used to move between habitats and
patches and search tactics enable the individual insect to locate resources.
It is necessary to understand the searching behaviors of predators and
parasitoids at two different standpoints. Scientifically, the tritrophic component
of plant, herbivore (prey or host), predator or parasitoid is a system which offers
many opportunities in the study of behavior. Both field studies and laboratory
studies can isolate this system and explore its many relationships. From a
practical perspective search behavior is very important to the success of biological
control programs. Understanding the various constraints placed on predators or
parasitoids can help avoid problems which limit their effectiveness. Further
understanding of the search efficacy between species of predators or parasitoids
could help entomologists effectively match natural enemies to particular
agricultural systems.
References
Bauer, T. 1985. Different adaptation to visual hunting in three ground beetle
species of the same genus. -J. Insect Physiol. 31: 593-601.
Bell, W. J. 1985. Sources of information controlling motor patterns in arthropod
local search orientation. -J. Insect Physiol. 31: 837-847.
Bell, W. J. 1990. Searching behavior patterns in insects. -Ann. Rev. Entomol. 35:
447-467.
Bond, A. B. 1980. Optimal foraging in a uniform habitat: the search mechanism of
the green lacewing. -Anim. Behav. 28: 10-19.
Cade, W. 1975. Acoustically orientating parasitoids: fly phonotaxis to cricket song.
-Science. 190: 1312-1313.
Carter, M. C. and Dixon, A. F. G. 1982. Habitat quality and the foraging behaviour
of Coccinellid larvae. -J. Anim. Ecol. 51: 865-878.
Chiverton, P. A. 1988. Searching behaviour and cereal aphid consumption by Bembidion
lampros and Pterostichus cupreus, in relation to temperature and prey density.
-Entomol. exp. appl. 47:173-182.
Curio, E. 1976. The Ethology of Predation. Berlin: Springer-Verlag.
Drickamer, L. C. and Vessey, S. H. 1992. Animal Behavior: Mechanisms, Ecology, and
Evolution. Wm. C. Brown Publ., Dubuque, IA.
Ferren, A., Ettifouri, M., Clement, P., Bell, W. J. 1994. Sources of variability in
the transition from extensive to intensive search in Coccinellid predators
(Homoptera: Coccinellidae). -J. Ins. Behav. 7: 633-647.
Hassell, M. P. and Southwood, T. R. E. 1978. Foraging strategies of insects. -Ann.
Rev. Ecol. Syst. 9: 75-98.
Hunter Jr., K. W. 1978. Searching behavior of Hippodamia convergens larvae
(Coccinellidae: Coleoptera). -Psyche. 85:249-253.
Jander, R. J. 1975. Ecological aspects of spatial orientation. -Ann. Rev. System.
Ecol. 6: 171-188.
Maredia, K. M., Gage, S. H., Landis, D. A., and Wirth, T. M. 1992. Visual responses
of Coccinella septempunctata (L.), Hippodamia parenthesis (Say), (Coleoptera:
Coccinellidae), and Chrysoperla carnea (Stephens), (Neuroptera: Chrysopidae) to
colors. -Biological Control. 2: 253-256.
McEwen, P. K., Clow, S., Jervis, M. A., and Kidd, N. A. C. 1993. Alteration in
searching behaviour of adult female green lacewings Chrysoperla carnea (Neuroptera:
Chrysopidae) following contact with honeydew of the black scale Saissetia oleae
(Homoptera: Coccidae) and solutions containing acid hydrolysed l-tryptophan.
-Entomophaga. 38: 347-353.
Michaud, J. P. and Mackauer, M. 1994. The use of visual cues in host evaluation by
aphidiid wasps: Comparison between three Aphidius parasitoids of the pea aphid.
-Entomol. exp. appl. 70: 273-283.
Nakamuta, K. 1985. Mechanism of the switchover from extensive to area-concentrated
search behaviour of the ladybird beetle Coccinella septempunctata Bruckii. -J.
Insect Physiol. 31: 849-856.
O'Brien, W. J., Browman, H. I., and Evans, B. I.1990. Search strategies of foraging
animals. -Am. Sci. 78:152-160.
Prokopy, R. J. and Webster, R. P. 1978. Oviposition-deterring pheromone of
Rhagoletis pomonella: a kairomone for its parasitoid Opius lectus. -J. Chem. Ecol.
4:481-494.
Reid, C. D. 1991. Ability of Orius insidiosus (Hemiptera: Anthocoridae) to search
for, find, and attack European corn borer and corn earworm eggs on corn. -J. Econ.
Entomol. 84: 83-86.
Smith, J. N. M. 1974. The food searching behaviour of two European thrushes. II:
The adaptiveness of the search patterns. -Behaviour. 49: 1- 61.
Tumlinson, J. H., Lewis, W. J., and Vet, L. E. M. 1993. How parasitic wasps find
their hosts. -Sci. Amer. :100-106.
Turlings, T. C. J., Tumlinson, J. H., and Lewis, W. J. 1990. Exploitation of
herbivore-induced plant odors by host-seeking parasitic wasps. -Science. 250: 1251-
1253.
Vet, L. E. M. and Groenwold, A. W. 1990. Semiochemicals and learning in parasitoids.
-J. Chem. Ecol. 16: 3119-3135.
Vet, L. E. M., Wackers, F. L., and Dicke, M. 1991. How to hunt for hiding hosts: the
reliability- detectability problem in foraging parasitoids. 41: 202-213.
Vinson, S. B. 1984. How parasitoids locate their hosts: A case of insect espionage.
-In: Lewis, T. (ed.), Insect Communication. Academic, New York, pp. 325-348.
Waage, J. K. 1978. Arrestment responses of the parasitoid, Nemeritis canescens, to a
contact chemical produced by its host, Plodia interpunctella. -Physiol. Entomol. 3:
135-146.
Wallin, H. 1991. Movement patterns and foraging tactics of a caterpillar hunter
inhabiting alfalfa fields. -Func. Ecol. 5: 740-749.