Strategies for Successful Parasitism

Abstract

Female parasitoids use a variety of information to detect and evaluate suitable hosts.  This decision is 
integral to their overall fitness, so a vast amount of energy is devoted to making the correct choice.  There 
are a series of differing strategies and cues that parasitoids respond to during host selection and host 
evaluation, including actual handling and parasitism.  While some of these behaviors are highly specific, 
there is a range of flexibility wherein the host and parasitoid can adapt to changes in  their particular 
environment.  To locate their hosts, parasitoids rely primarily on olfactory cues from the plant-herbivore 
complex, usually in the form of volatile compounds released by the host or the  damaged plant. Visual 
cues play a part in the recognition of the host by evaluating such phenotypic characteristics as color, shape 
and movement. The degree of discrimination of a parasitoid for its host can vary widely.  Many species of 
parasitoids are generalists; however, the more interesting host evaluation behaviors are associated with the 
specialists.  The degree of specialization also varies widely, from preying on a single species to 
exclusively parasitizing a single instar.  A potential host must conform to the parasitoid's profile if a 
response is to be elicited.  Overall, parasitoids are faithful to these cues, and only deviate from them when 
they encounter adverse conditions. Analysis of time spent foraging reveals how parasitoids make "second 
choices" or how long they search before changing microhabitats. If there is an environmental change in 
temperature, density of prey, or quality of prey, the parasitoids react differently.  The interrelationship of 
host and parasitoid can be characterized by specific behaviors and strategies regardless of the species.  
Olfactory cues in location, visual feature extraction in host recognition and gustatory or chemosensory 
cues in handling lead a parasite to choosing a suitable host.  Comparisons between parasitoid strategies are 
presented.  

Introduction

The group of behaviors that comprise host foraging and parasitism can be evaluated similarly regardless of 
the species involved.  The parasitoids have a series of strategies which, when confronted with the proper 
cues, allow them to make a positive choice that will maximize their fitness return (Mackauer et al, 1996).  
Volatile compounds and airborne cues emanating from the host and the host plant aid the parasitoid in 
locating a general vicinity in which to search (Roland et al, 1995; Monge &Cortesero, 1996). Acoustic 
cues sometimes orient the parastoids toward their prey. (Cade et al, 1996) Visual cues, including shape, 
color and movement, can also be evaluated from a distance.  Gustatory or contact chemical cues, are 
assessed through the use of the antennae and the ovipositor. (Mackhauer et al, 1996) 

Parasitoids can be generalists or specialists.  The overall fitness of a generalist can be improved by greater 
array of choices than those of a specialist.  Many parasitoids exhibit a marked preference for a specific sex 
or instar larvae (McGregor, 1996; Mattiacci &Dicke, 1995).  This can be due to an increased survival of 
their offspring or a difference in the ease of parasitism. Most parasitoids avoid competitive superparasitism 
or multiparasitism using interspecific host discrimination to ensure being the primary parasitoid (Pijls et al, 
1995).  Parasitoids often encounter sub-optimal conditions and are forced to change their criteria.  Host 
plant quality, host density or sex ratio (Fox et al, 1996; Stadler & Mackhauer, 1996) can contribute to the 
changing conditions under which parasitoids make less than ideal choices.

Host Location and Recognition

Olfactory

Olfactory cues are the primary signals for host location used by parasitoids.   While olfactory cues are 
important to host searching and location, other cues are used to trigger oviposition  (Roland et al, 1995; 
Conti et al, 1996).  Volatile chemicals from the damaged host plant, frass and the host itself serve as a 
trigger to the parasitoid (Monge & Coretsero, 1996), allowing it to increase the efficiency of its search 
efforts (Roland et al, 1995).  General chemical cues may also include substances that are produced by the 
host, such as sex hormones, kairomones and host products  (Mackhauer et al, 1996).  Herbivory- related 
volatiles facilitate location of the host microhabitat. (Geervliet et al, 1996) Plant cues are the most reliable 
over distance.  Parasitoids are more attracted to herbivore-damaged plants than undamaged plants, though 
the species of the herbivore may not be of importance at that point.  In many cases, it is the species of plant 
being damaged that is of interest.  If the damaged plant odor is from a host plant, that cue alone may be 
profitable in guiding the parasitoid to a location which could potentially house host species (Roland et al, 
1995).  However, in some parasitoids there was a marked preference between damaged plants, both of 
which housed hosts.  This may indicate that there is a difference in suitability or quality of hosts that feed 
on this plant, or an evolutionarily recent migration of the host species to a new plant.   The signals emitted 
by the damaged plant may not provide the parasitoid with the identity of the herbivore.   If the parasitoid is 
a generalist, these cues need only be broad or non-specific.  When compared to plants damaged by host 
and non-host species, the stimulus from  mechanically damaged plants results in a similar response by 
foragers. (Geervliet et al, 1996) Parasitoids face a reliability-detection problem.   Parasitoids should be 
able to distinguish between differing plant-host complexes.  Stimuli that originate from the host are the 
most reliable cues for indicating host presence and suitability, however they are difficult to detect at any 
distance (Mattiacci & Dicke, 1995).  Once the proper microhabitat has been located the probability of 
encountering a host increases, and the use of host distinguishing olfactory cues becomes possible and 
advantageous. Some method of long range host location must exist if the parasitoid is to ever encounter 
hosts, but a more sensitive indicator is necessary to minimize search and handling time while still 
narrowing the potential choices.  Specialists can distinguish very sensitive chemical cues, specific not only 
to species but also to developmental host stages within a species  (Mattiacci & Dicke, 1995). 

Visual

Parasitoids are mainly diurnal and can distinguish colors.  Because visual cues can be evaluated at a 
distance, resulting information is important to habitat and host plant location.  Color preferences play a role 
in plant recognition  (Mackhauer et al, 1996). Characteristic visual appearances of hosts and host plants are 
targets for this foraging strategy.  Such cues can differentiate host sites at the level of plant structure 
(Wackers & Lewis, 1994).   Size, shape and color are the main visual attributes of a potential host.  These 
cues can be assessed at a distance and can be utilized in a number of decisions (Mackhauer et al, 1996).  
Visual cues can be used as a first screen to distinguish between hosts and non-hosts.  Differing types of 
potential hosts are compared in this way.  Polymorphisms in color often may indicate differences in other 
attributes of the potential host.  Color forms that do not conform to the search profile of a parasitoid are 
eliminated. This may be a mechanism for the maintenance of color polymorphisms in prey species 
(McGregor, 1996)  Species that do not use visual cues may make choices that are less than optimal by 
choosing inferior hosts.  Size and shape are evaluated at close range after host recognition.  One or more 
of these cues are enough to induce acceptance of the host in some species.  Movement is also assessed 
visually.  Parasitoids most often are attracted to moving hosts, rather than non-moving or anaesthetized 
host choices. (Mackhauer et al, 1996)

Auditory

Utilization of acoustic cues in host location is more rare relative than the use of other cues, but in a 
parasitoid fly, phonotaxis is the method of choice.  The parasitoid discerns patterns of cricket song at a 
specific time of day and locates the host based on its orientation to the sound.  Both the host and the 
parastioid become acoustically active at sunset.  These temporal patterns of cricket song are very specific.  
The auditory cues must occur in the proper season and at the correct time of day for the appropriate 
response to be elicited.  When the correct cue was played during the day, there was no response by the 
parasitoid. Variations in parasitoid attraction were directly correlated with the changes in the cricket song 
that occurred with temperature fluctuations (Cade et al, 1996).

Gustatory

Gustatory or contact cues register the presence of chemicals on the host.  Unlike the olfactory chemicals, 
which are mainly used for host location, these cues indicate the host suitability for oviposition.  Often 
these cues are actually oviposition triggers (Roland et al, 1995).  Tactile chemical cues are registered in one 
of two ways.  The antennal sensoria perceive contact chemicals present on the cuticle of the host during 
antennation.  Numerous chemosensilla on the ovipositor serve the same purpose during ovipositor 
probing.  These specific contact cues allow the parasitoid to use infochemicals in distinguishing between 
host and non-host species, circumventing chemical camouflages and assessing the quality of the host.  
This strategy is effective for host identification in species that do not utilize visual cues.  (Mackhauer et al, 
1996) Tactile cues can be very sensitive indicators for discerning specific instars within a host species by 
assessing the chemicals present during handling of host, silk and frass (Mattiacci & Dicke, 1995).     

Host Selection  and Acceptance 

Learning

There are many cues present in parasitoid host recognition and selection.  The efficiency with which these 
cues are processed is integral to the overall fitness of the parasitoid.  Opportunity costs for inefficiency are 
high and can endanger the life of the parasitoid as well as the potential for propagating the next generation. 
Many responses by the parasitoid to visual or olfactory cues are innate.  This is demonstrated by a marked 
recognition and unchanging preference for specific cues.  However, in some cases the parasitoid acquires 
the recognition of the appropriate cues by learning (Takasu & Lewis, 1996).   In learning profitable cues, a 
parasitoid can adapt to spatial and temporal variations in its environment (Monge & Cortesero, 1996).  
There are different types of learning; pre- and post-emergence.  Pre-emergent behaviors are the early 
learning that takes place before the parasitoid is fully developed.  Before the young adult emerges, it is 
subjected to host and host plant odors.  These are the volatile cues that are most integral to the location of 
the host when it emerges as an adult (Monge & Cortesero, 1996).  Post-emergent learning is portrayed by 
the absence of host preferences by naive female parasitoids.  These females have no difficulty in locating a 
host microhabitat, but show equal interest in both host and non-host species.  Their handling time is 
greater than experienced females, but after only a few trials they grow more competent (Greervliet et al, 
1996).   Learning can play a valuable role in scent discrimination.  By learning the odors that are 
associated with their particular host, parasitoids are able to distinguish subtle differences between 
advantageous cues and non-profitable cues (Geervliet et al, 1996; Wackers & Lewis, 1994). Since plant 
structures and hosts can be assessed in many ways, it is important to distinguish the method of choice in 
each instance and what strategy is being used. (Wackers and Lewis, 1994)  Combinations of cues may be 
more reliable and sometimes constitute automatic acceptance or rejection.  

Host Age

Parasitoid preference for specific instar or larval stages can occur for a variety of reasons.  There are 
differences in host quality with increasing age , pertaining to the developmental possibilities for the new 
larval parasitoid. The developing hosts grow in size and increase their array of  defense mechanisms, 
making the encounters more dangerous for the parasitoid (Mattiacci and Dicke, 1995).  The different host 
instars may consume different portions of the plant, thereby being easily distinguishable from other age 
categories.  The olfactory and gustatory cues may change with age and development of the host 
(McGregor, 1996).  The trade-offs associated with the various host ages  may explain how the parasitoid 
preference evolved and how the changes in the host life history came about..  (Mattiacci and Dicke, 1995)  
Parasitoids, through their mechanism of selection, can influence the timing of life history events( 
McGregor, 1996) . Parasitoids which are specific foragers optimally must gain a greater reward for the 
increased opportunity costs.  It is more difficult and time- consuming to prey only on a fraction of hosts 
species.  However, some parasitoids partially overcome this disadvantage by correlating their preference 
with seasonal availability (McGregor, 1996)

Previous Parasitism: Competition

It is in every parasitoid's best interest to be the first and the only user of a particular host.  Competition 
varies with host density. Interspecific host discrimination is the ability of females to distinguish between 
unparasitized hosts and hosts that have been parasitized by another species of parasitoid.  When a 
parasitoid oviposits in a hosts already parasitized by a conspecific, it is termed superparasitism.  When the 
same occurs by another species, the term is multi-parasitism (Pijls et al, 1995).   The fewer the number of 
potential hosts, the greater the amount of superparasitism and  multiparasitism.  Discrimination of 
previously parasitized hosts becomes a valuable tool when hosts are scarce.  The ease and facility with 
which the parasitoid can accomplish this increases their overall fitness.  The sooner an undesirable host 
can be identified, the sooner the parasitoid can begin a new search.  External cues would be most 
favorable, while internal cues would be less so because they require actual inspection to determine the state 
of the host.  

In observing the amount of time spent foraging in a particular patch, an efficient forager was one that 
stayed in a given patch until the capture rate fell below average.  If other suitable hosts are nearby, then the 
forager parasitoid would seek them out, and if none were available, the parasitoid would accept one of 
lesser quality (Steenis et al, 1996).  There are different types of cues that can trigger acceptance or rejection 
of hosts during various stages of searching.  The earlier it occurs, the more beneficial.  Parasitized male 
crickets have a reduced ability to sing a few days before death, altering their temporal patterns and the 
parasitoids' response to them. (Cade et al, 1996) This may indirectly aid other parasitoids by allowing 
them to avoid the expenditure of energy and resources required to search out and handle this previously 
parasitized and now unsatisfactory host.   Some species of parasitoids mark previously parasitized hosts 
with a contact pheromone.  This is easily discernible by other parasitoids utilizing gustatory strategies.  
(Mackhauer et al, 1996).  The rejection of these hosts was strongest during shorter time intervals of 
parasitism and may be due to the response to an external cue or some internal stimulus signaling a change 
in host quality.  This is a cue occurring in handling and it requires a greater input of initial energy to 
determine the status of the host.

Host Plant Quality

Parasitoids and their hosts occur in patchy environments, with resources varying seasonally in quality and 
availability ( Stadler & Mackhauer, 1996).  Parasitoid behavior may be directly influenced by the plants on 
which their hosts feed.  Plant quality controls host body size and population density, influencing parasitoid 
sex ratio, fecundity and survival (Fox et al, 1996; Stadler & Mackhauer, 1996).  The species of parasitoid 
that provision their eggs poorly, relying on host nutrient stores, can be severely affected by changes in the 
host plant quality (Stadler &Mackhauer, 1996). The usual influences of sex ratio variation are host quality, 
mate competition and environmental conditions. The role of the plant is indirect, influencing qualities of 
the host; size, growth or survival.  The parasitoids are responding to those cues in the herbivore.  When 
tested, parasitoids prefered hosts raised on high quality plants  (Fox et al, 1996).  Selection of hosts can 
take the form of generalist or specialist.  In the case of a host plant generalist, the parasitoid may accept 
hosts from many host plants.  A specialist may choose only a single host-plant interaction to exploit.  
There are different opportunity costs associate with each strategy.  

Second Choices: A Study in Opportunity Costs

While optimal hosts are ideal, they are rare.  A "second choice" means a host which under perfect 
conditions would be rejected.  When conditions change, the parasitoid has options. Its primary urge is to 
satisfy its preferences, but it can prioritize its cues.    If the parasitoid is a generalist, it may simply opt to 
search for another species of host.   A parasitoid specialist may face a more dire situation.  Within its 
chosen host species, it will accept hosts of lesser quality.  Many sets of environmental conditions may 
trigger a secondary response.  The first choice the parasitoid is faced with in the absence of quality hosts is 
how long to keep searching.  There is a biological constraint, within which a female must oviposit.  Here 
the shift between ideal and suboptimal hosts is factor of time. While most parasitoids prefer to rear their 
young in hosts that have not been previously parasitized, they do not completely avoid superparasitism or 
multiparasitism.  Parasitoids need to learn what is available to them in order to make a choice.  In some 
situations, the parasitoids eventually accept hosts that were initially rejected (Pijls et al, 1995). This 
indicates a unfufilled preference which resulted in a less that perfect choice.  When parasitoids must 
choose to oviposit in a previously parasitized host, they spend additional effort to locate a minimally 
damaged host.   

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