Intraguild Predation: Disruption of Biological Control?
Determining which enemies can be used together will result in greater success when using biological controls.
Biological control is a pest management strategy that involves the use of natural enemies such as parasitoids, predators or pathogens to control pest populations, including insects and mites. It is important to understand that biological control is a regulatory process. Natural enemies will not eradicate an arthropod pest population; the success of natural enemies is based on maintaining arthropod pest numbers at levels low enough to minimize plant damage.
There have been many trade journal articles written on how to succeed using biological control in greenhouse production systems; however, very few, if any, articles actually address the interactions that can occur when releasing more than one biological control agent. First of all, there are two types of natural enemies: specialists and generalists. Specialists attack and feed on one or at most only a few arthropod hosts or prey. Generalist natural enemies tend to feed on several different species. Generalists may also feed and reproduce on alternative food sources including pollen. However, an inadvertent effect of having generalist predators in a biological control program is that they may attack other natural enemies that share the same pest hosts. This is oftentimes referred to as intraguild predation.
How Intraguild Predation Works
Intraguild predation is defined as a natural enemy feeding on another natural enemy when both natural enemies share another resource as food (usually plant-feeding prey or host species). As such, the interaction may involve either predation (or parasitism) and competition. Therefore, intraguild predation, or IGP, can decrease or eliminate resource competition, which may directly enhance individual fitness as a result of eliminating a competitor for similar resources. For example, parasitoids may eliminate other parasitoids that are developing within a shared host.
As mentioned above, many predators are generalists, which means they consume or feed on a wide range of different host types, and this can increase the probability of IGP. For example, generalist parasitoids or predators may feed not only on herbivore (pest) prey, but also on parasitized hosts or other predators. Whether or not IGP has a negative impact on biological control depends on how much of it occurs, whether the intraguild predator prefers pests to other natural enemies, and how important the predator or parasitoid that is fed upon by IG predators is for biological control.
There are numerous examples of IGP associated with natural enemies used in greenhouse production systems. For example, Neoseiulus californicus, a predatory mite, may feed on Phytoseiulus persimilis, another predatory mite, in the absence of prey, whereas P. persimilis does not feed on N. californicus; however, IGP may be neglible when prey are present because N. californicus prefers to feed on the twospotted spider mite (Tetranychus urticae) rather than P. persimilis. Adults of Orius majusculus have been shown to feed on whitefly (Bemisia tabaci) nymphs parasitized by the whitefly parasitoid, Encarsia formosa, although pupae were preyed upon less than the nymphs. It has been suggested that parasitized whiteflies tend to swell and become opaque, which makes the parasitized whitefly nymphs more noticeable to the searching predators. Therefore, it appears that IGP interactions between O. majusculus and E. formosa disrupt biological control of B. tabaci. Furthermore, it has been demonstrated that IGP occurs when the predatory beetle, Delphastus catalinae is used in conjunction with parasitoids. Some additional examples include reports of Amblyseius barkeri feeding on P. persimilis, Iphiseius degenerans eating Aphidoletes aphidomyza, and A. swirskii consuming A. aphidomyza.
Types of Intraguild Predation
Intraguild predation may be unidirectional or bidirectional. Unidirectional IGP occurs when one of the interacting natural enemies is considered the intraguild predator and the other natural enemy is the intraguild prey, or one predator always feeds on another. For example, O. laevigatus has been shown to feed on both N. cucumeris and I. degenerans, but neither of the predatory mites feeds on O. laevigatus. There are two types of unidirectional IGP associated with predators and parasitoids: 1) predators may prey directly on parasitoids by feeding on the immature stages developing on the outside of the host or on parasitoid adults; and 2) predators may feed on parasitized hosts, which results in consuming both the actual host and immature parasitoid located inside the host.
Bidirectional or mutual IGP is when predators are capable of feeding on each other. For example, IGP is a common occurrence when the predatory mites, N. cucumeris and A. swirskii both occupy or share similar regions in the crop-plant canopy. This type of IGP is of interest to biological control practioners because use of both predators should be avoided if IGP reduces the level of pest control due to mutual elimination of predators compared to releasing only one predator, even if each predator contributes to pest suppression.
Life stage may influence the intensity of IGP because individuals tend to be more susceptible when small and/or in life stages such as eggs, young and/or pupae. For example, green lacewing larvae may consume the larvae of the ladybird beetle, Hippodamia convergens and immatures of the parasitoid, Aphidius smithi. Natural enemies may also be more susceptible to predation at certain life stages such as eggs, young larvae/nymphs and pupae. In addition, IGP may be more prevalent during or after molting. In fact, periods of molting and pupating dramatically increases susceptibility to IGP. Also, sessile or non-mobile life stages including eggs and pupae are highly susceptible to IGP although it has been suggested that hosts containing parasitized pupae are less vulnerable to predation. The feeding on smaller or susceptible life stages is commonly associated with IGP. In fact, larvae of some parasitoids will kill younger larvae within the same host. Therefore, relative body size, life stage, and even specialization are important factors that influence the frequency and direction of IGP.
What Influences IGP?
Plant characteristics and encounter rate may also impact the intensity of IGP. Intraguild predation may be indirectly influenced by plant characteristics including trichomes (leaf hairs) and waxes on plant surfaces, which can also negatively impact the encounter rate.
The presence of refugia or locations on plants where natural enemies can hide may decrease predation on susceptible life stages. Plants may provide hiding places for certain natural enemies (as interguild prey) thus reducing the potential encounter rate. Furthermore, prey may develop behaviors that allow them to escape or avoid areas with other species. The intensity of IGP may be higher in certain cropping systems, not only because of the encounter rate of the natural enemies, but also because different cropping systems have different natural enemies. Encounter rates may increase when natural enemies exploit a common resource. For example, aphids distribute themselves in groups and on new terminal growth, which increases the potential for IGP as many natural enemies such as ladybird beetles, syrphid flies and green lacewings may simultaneously exploit aphid colonies, which may increase the occurrence of IGP.
Ladybird beetles may also consume developing parasitoids and fungal pathogens infecting parasitized aphids. Intraguild predation may involve predators consuming hosts harboring developing parasitoid larvae although they may not be able to distinguish between unparasitized and parasitized hosts. Furthermore, IGP may occur indirectly based on formulation of the natural enemies. For example, N. cucumeris, applied in “breeder piles,” may not be “compatible” with the rove beetle, Dalotia (formally Atheta) coriaria because rove beetle adults and larvae feed on the predatory mites in the “breeder piles.”
Impact on Biological Control
It has been suggested that IGP may negatively impact or disrupt biological control and could be a factor in determining the abundance and distribution of biological control agents. However, there is still debate on whether IGP between natural enemies results in a positive or negative effect, or no effect, which may be associated with the types of natural enemies involved. This is especially the case where there are high levels of mortality for one or both natural enemies whereas the total mortality on the target arthropod pest population is minimal. Intraguild predation may disrupt biological control if two natural enemies compete for a single shared host; however, if multiple hosts are available then this may decrease the intensity of IGP.
In addition, IGP among predators may be intense, resulting in high mortality between the interacting predators with minimal mortality imposed upon the shared host. Therefore, IGP may relieve arthropod pest populations from regulation by natural enemies although the presence of multiple host species may reduce the potential for IGP because ample food sources are available. Intraguild predation may result in lower mortality of insect and/or mite pests, which may allow them to increase in numbers. This suggests that the use of multiple natural enemies may decrease the effectiveness of biological control programs resulting in an increase in prey abundance associated with IGP.
Although the concept of IGP is primarily focused on predator-predator or predator-parasitoid interactions, there are instances in which IGP can occur in association with pathogen-natural enemy interactions. There are a number of ways, for instance, by which pathogens, primarily fungi, may directly and indirectly impact natural enemies including 1) infecting and killing or reducing the fitness and thus overall effectiveness of natural enemies; 2) reducing the population of hosts to the point such that either parasitoids or predators cannot find sufficient numbers to breed, feed upon or sustain populations; and 3) infecting both the host and natural enemy, or reducing the nutritional value of hosts so that they are no longer a viable food source resulting in starvation of natural enemies. For example, Beauveria bassiana and Metarhizium anisopliae are broad-spectrum or generalist fungi that may infect a wide-range of insects including natural enemies.
In summary, IGP is the interaction between natural enemies that utilize similar resources or share the same food source, which may impact the success of biological control programs although this is not always the case. There are a number of factors that determine the extent of IGP including whether the natural enemy is a specialist or generalist, encounter rate, size of the natural enemies involved, and the presence of plant refugia. Therefore, in order to succeed with biological control it is important to avoid using too many natural enemies or at least determine those that can be used together without resulting in IGP.