The connections between plants and animals drive countless trophic interactions. These interactions fall into 4 main categories: mutualism, commensalism, antagonism, and competition. Most animals depend on plants, whether directly, through shelter and food, or indirectly as predators upon herbivores and other animals lower in the trophic system. Furthermore, the majority of carbon and solar energy is fixed by plants in both terrestrial and aquatic systems, making it accessible as an energy source for other species.
It is for these reasons that the study of animal-plant interactions is so biologically significant, not only to aide our understanding of ecology, to provide the most effective conservation methods and allocation of funds, aiming to preserve its delicate and intricate equilibriums; but also because understanding of these trophic relationships has the potential to benefit human development.
Human societies require a constant and reliable food supply and are always searching of ways to improve the success rates of agriculture. Along with weather conditions, natural disasters, disease, and soil degradation, crops often fail or perform badly due to pest populations growing or the invasion of invasive species.
Our understanding of biological interactions is allowing scientists to develop methods of manipulating species relationships, to modify the behaviour of crop pests and their natural enemies (predators, parasites, parasitoids), with the aim of protecting human food supply, in the most ‘natural’ and targeted way available, reducing the need for chemical pesticides. In other words, to protect plants from herbivores, methods are being developed to conserve, encourage, and augment the natural enemies of several agricultural pests.
This essay will explain the methods being used at the moment, and examine case studies of natural enemy manipulation, by first evaluating projects to manipulate pest predators, then moving onto cases using parasites/parasitoids.
What are Semiochemicals, and how are they used?
Animals and plants cannot utilise spoken language, but they have other means of communicating to each other, both to individuals of the same species, but also between species.
These include methods such as visual displays and body language, vocal signals, and olfactory markers. An additional process is the use of chemical cues, which convey information to either conspecifics or members of other species (Reddy, 2004).
A semiochemical can be defined as a compound, or mixture of compounds, that conveys information or signals from one organism to another, with the aim of modifying the behaviour of the recipient individual (Norin, 2007). There are two types of semiochemical: when a chemical aims to mediate interactions between individuals of the same species, this is called a Pheromone, and those which convey information to organisms of different species are known as Allelochemicals (Rodriguez-Saona, 2012). Additionally, Allelochemicals can be further classified into signals which benefit both the emitter and the receiver of the signal (Synomones – mutualism), compounds which benefit only the emitter (Allomones – antagonism), and those which benefit the receiver (Kairomones – commensalism), showing the huge variety of uses that these signals provide (Rodriguez-Saona, 2012) (Nordlund, 1981). Semiochemicals determine many insect life history events (Norin, 2007), such as mating and egg laying cycles, courtship, and guidance to feeding/foraging sites.
An important category of semiochemicals are called Herbivore Induced Plant Volatiles (HIPV’s), which are context-dependent induced defences. These compounds enable signals in tri-trophic interactions: plant, herbivore, and their natural enemies. These chemicals are released by plants in response to damage by herbivores, such as leaf or root eating, and can be used as a sign to alert natural enemies to the presence of prey/hosts, to aide them in locating their prey organism (Rodriguez-Saona, 2012). It is unclear what the evolutionary explanation of HIPV production is, with some claiming that co-evolution with predators and parasites has led to this interaction, which appears beneficial to both parties. But it has also been suggested that HIPV’s may aide healing of plant flesh, and are simply exploited by natural enemies, to hijack the information of prey location (Rodriguez-Saona, 2012). Either way, the utilisation of semiochemicals increases plant fitness and survival, due to the reduction in abundance of pests.
There is even evidence of further complexity, after studies suggested that certain plant species emit different compounds, depending on which organism is damaging them (Karban, 1989). For instance, some plants can identify which species of aphid are attacking, and release specific compounds, or respond in other specific ways, which can then be exploited by natural enemies, identifying the single prey species that they specialise in feeding on or parasitizing. This enables predators and parasites to target communities with precision and raise their foraging success rate.
The first developments in the field of semiochemicals were essentially ‘bait and kill’ pest control measures (Kennedy, 1981) as a form of ‘integrated pest management’ (IPM), which relies on combining multiple strategies, such as biological and chemical, to maintain low pest populations (Rodriguez-Saona, 2012).
Compounds which mimicked insect pheromones such as the scent of a fertile female, or plant allelomones aiming to draw in pollinators, were strategically used to entice the pests which would respond to these chemical signals. The most common semiochemicals used in these methods are aggregation pheromones (Kelly, 2013), which are compounds emitted by males, to attract both sexes and all life stages, into pheromone-traps containing insecticide chemicals (Lanier, 1990).
There are indicators that using natural lures to bait problematic pest species into traps is an effective, and a less environmentally disruptive method of population control, versus blanket use of pesticides and other synthetic methods (Kennedy, 1981).
However, the step forward from here, with the aim of an even more natural approach (Agelopoulos, 1999), was to remove the need for human capture and kill as the last step. In place of this, we encourage the presence of ‘natural enemies’ of the pest species, such as specialised predators and parasites, by using chemical lures to the site of pest infestation (Rodriguez-Saona, 2012). Thus, augmenting existing tri-trophic interactions, by manipulating the behaviour and location of crop pest natural enemies.
It is such investigations that the remainder of this essay will explore, to evaluate whether the use of semiochemicals to manipulate predator behaviour can be a successful pest control method in agroecology.
Predator Case Studies:
Currently, the most successful studies on arthropod-produced semiochemicals to reduce pests have been using Lepidopteran sex pheromones, or aggregation pheromones of Coleoptera (Agelopoulos, 1999).
The experiments by Jessica Kelly in 2014 aimed to control populations of the Tobacco Hornworm Moth, which is responsible for destruction and defoliation of many economically valuable plants from the solanaceous family, namely tomatoes, peppers, and tobacco (Kelly, 2013). The caterpillar of this moth is specialised for herbivory on these crops, but luckily has many natural enemies (Rabb, 1971) which can be utilised to reduce the economic loss of crop damage. In this case, Kelly aimed to manipulate the behaviour of a stink bug species called P. maculiventris, which is a generalist predator of lepidopterans. The aggregation pheromone of the stink bug was formulated in a laboratory, and then diffused in plots of tomato plants, and being compared to control areas with the same conditions. The results of the results showed an increase in the number of predatory P. maculiventris in the semiochemical treated areas but were inconclusive on whether there was a higher predation rate.
In a second case, the control of Bark Beetles in North America has been a priority of researchers in recent years, as the effects from their interactions with disease rates, climate change, and fires has led to the destruction of millions of acres of woodland since 2007 (Bentz, 2010). A primary predator of the pine engraver bark beetle (Ips pini) is the family of predaceous Cleridae called checkered beetles (Herms, 1991). Experiments in Wisconsin and Michigan (areas both heavily affected by bark beetles) showed a significant increase in bark beetles caught in traps when they were pheromone baited, but also highly significant differences in the numbers of Cleridae (predatory beetles) when pheromone lures were used; the total number of Cleridae captured rose by +97% (Herms, 1991).
Predatory Heteropterans have been investigated again, with the aim of suppressing the infestation of Colorado Potato Beetles after it was confirmed as the most destructive pest of potato in eastern North America (Aldrich, 2001). The two-spotted stink bug, Perillus bioculatus, has been extensively researched as a means of biological control, due to it being virtually host specific on the potato beetle, along with the spined soldier bug, Podisus maculiventris, which has similar levels of predation on the bug. In 2001, Aldrich investigated the effects of semiochemical release on predator and pest numbers, with results showing that augmentation of these two carnivorous insects significantly suppresses Colorado Potato Beetle populations (Aldrich, 2001). The method of this experiment involved the positioning of pheromone dispensers as chemical signals, and served as an attractant for these key biocontrol agents.
In 2012, Rodriguez-Saona identified two studies which tested the effects of HIPV semiochemicals in the field; implementation of these methods in the field is often less successful, due to multiple variables and weak methodology (Kelly, 2013), therefore it is more common for greenhouse or ‘closed plots’ to be used. Both studies identified were successful in finding increased predation on target pests, namely Cabbage root fly and Soybean Aphids (Ferry, 2009 ) (Mallinger, 2011).
Parasite Case Studies:
Just as semiochemicals can be utilised to attract beneficial predators, the other main form of natural enemies to crop pests, parasites and parasitoids, can also be augmented using similar methods. A distinction can be made between these two as although both need a host organism for a portion in their life history, but parasitoids often kill the host in the process, where parasites just live on or inside the host, usually reducing the organisms fitness, but not ultimately causing mortality. The most common type of parasitoids is the Hymenoptera, mainly the wasp family, where females use an ovipositor to insert eggs into a host, as well as other reproductive mechanisms (Tumlinson, 1993). The following experiments investigated the effectiveness of semiochemical use to manipulate parasitoids behaviours.
Many parasitic insects use chemical cues to guide them to a host when foraging. In 1991, research showed that female wasps searching for a host for their eggs, use the sex pheromones of their host species as kairomones, essentially hijacking the host signals for their own benefit (Noldus, 1991). Specifically, the species Trichogramma has been shown to be attracted to the pheromones of the Corn Earworm, Large White butterfly, and the Cabbage Moth, all of which are pests that cause significant damage to their specialist plant (Noldus, 1991).
Bark beetles have also been a subject of interest in parasite studies, as well as predator investigations, due to their detrimental effect to ecosystems if left unchecked. The European Red-Bellied Clerid (Thanasimus formicarius) has been shown to recognise and aggregate towards the specific combination of compounds that Bark Beetles produce for reproduction, then parasitize the pest (Bakke, 1981).
In addition to interpreting other animal’s hormonal signals, parasites can also utilise the chemicals given off by plants to locate likely sites for hosts.
Corn and Sorghum are essential and economically valuable crops in Africa, but are heavily targeted by Lepidopteran pests, which cause between 20%-80% loss of crop yield yearly (Khan, 1997). Research has shown that in these cases, semiochemicals released during herbivore damage can stimulate parasitoid foraging; the Maize Stalk Boarer (Busseola fusca) and the Spotted Stalk Boarer (Chilo partellus) moths cause are attracted to aggregate in crop fields by the compounds they release, but so are the parasitic Braconid wasps (Khan, 1997). Researchers discovered a plant species (M. minutiflora) that passively produces the same compounds as damaged Maize, then used a method called ‘intercropping’, dispersing this plant throughout valuable crop fields, to augment the colonisation of the beneficial parasitic wasps, and control the populations of the moth caterpillars.
There are many cases in the literature that conclude semiochemicals can manipulate the behaviour of parasites/parasitoids, but less is available which aims to apply this knowledge, to subjects like pest control or conservation methods. However, in the Rodriguez-Saona overview of semiochemical uses, 3 key studies were identified which targeted parasites and their pest hosts; two found increases parasitism and reduced pest numbers when semiochemicals were strategically placed in fields of broccoli and cotton, while the third study on strawberries was inconclusive (Williams, 2008) (Yu, 2010) (Lee, 2010).
When looking at the current level of knowledge of semiochemicals and their applications for pest control, it is clear this area of research is promising. We have extensive evidence that both predator and parasite behaviour is affected by the chemical cues of other organisms, both animals and plants. In evaluating the present frontiers of this research, I have found that there are currently more field studies on predatory natural enemies than parasitic, perhaps because parasites and parasitoids are a less obvious route for pest control (Tumlinson, 1988). I believe that the manipulation of natural enemy behaviour using semiochemicals, with the goal of decreasing insect crop pest populations, has a lot of potential as a more natural and hands-off method, which avoids the issue of indiscriminate killing of invertebrates and micro-organisms, as many conventional pesticides do.
But, we need to continue research in field studies, in order to identify the most efficient compounds for each case, and from this develop a commercialised form, which currently does not exist at all, compared to the hundreds of forms of pesticides available on the wholesale market for agricultural purposes, which are markedly more damaging to ecosystems. I believe that it makes more ecological and economic sense to utilise the tools that nature has given us to control pest populations, rather than poisonous chemical additives, which cause long-term damage to ecosystems; the combination of natural semiochemicals and the augmentation of crop pest enemies is a hopeful new mechanism to protect both human resources, and biological stability.
Word Count: 2200.
Agelopoulos, N., 1999. Exploiting semiochemicals in insect control. Pesticide Science, 55(3), pp. 225-235.
Aldrich, J., 2001. Suppression of Colorado potato beetle infestation by pheromone‐mediated augmentation of the predatory spined soldier bug, Podisus maculiventris (Say) (Heteroptera: Pentatomidae). Agricultural and Forest Entomology , 1(3), pp. 209-217.
Bakke, A., 1981. Kairomone response in Thanasimus predators to pheromone components ofIps typographus. Journal of Chemical Ecology, 7(2), pp. 305-312.
Bentz, B., 2010. Climate Change and Bark Beetles of the Western United States and Canada: Direct and Indirect Effects. BioScience, 60(8), pp. 602-613.
Ferry, A., 2009 . Field evaluation of the combined deterrent and attractive effects of dimethyl disulfide on Delia radicum and its natural enemies. Biological Control , 49(3), pp. 219-226.
Herms, D., 1991. VARIATION IN SEMIOCHEMICAL-MEDIATED PREY-PREDATOR INTERACTION: Ips pini (Scolytidae) AND Thanasimus dubius (Cleridae). Journal of Chemical Ecology , 17(8), pp. 1705-1714.
Karban, R., 1989. Induced Plant Responsed to Herbivory. Annual review of Ecology and Systematics, 20(1), pp. 331-348.
Kelly, J., 2013. Semiochemical lures reduce emigration and enhance pest control services in open-field predator augmentation. Biological Control, 71(1), pp. 70-77.
Kennedy, J., 1981. Practical Application of Pheromones in Regulatory Pest Management Programs. In: M. Everett, ed. Management of Insect Pests with Semiochemicals: Concepts and Practice. New York : Plenum, pp. 1-13.
Khan, Z., 1997. Intercropping increases parasitism of pests. Nature, 388(1), pp. 631-632.
Lanier, G., 1990. Principles of attraction–annihilation: mass trapping and other means. In: R. S. M. I. R.L. Ridgway, ed. Behavior modifying chemicals for insect pest management: applications of pheromones and other attractants. New York: Marcel Dekker Inc., pp. 25-45.
Lee, J., 2010. Effect of methyl salicylate-based lures on beneficial and pest arthropods in strawberry. Environmental Entomology , 39(1), pp. 635-660.
Mallinger, R., 2011. Methyl Salicylate Attracts Natural Enemies and Reduces Populations of Soybean Aphids (Hemiptera: Aphididae) in Soybean Agroecosystems. Journal of Economic Entomology, 104(1), pp. 115-124.
Noldus, L., 1991. How Trichogramma parasitoids use moth sex pheromones as kairomones: orientation behaviour in a wind tunne. Physiolgical Entomology , 16(3), pp. 313-327.
Nordlund, D., 1981. Elucidation and Employment of Semiochemicals in the Manipulation of Entomophagous Insects. In: E. Mitchell, ed. Management of Insect Pests with Semiochemicals. Boston: Springer, pp. 463-475.
Norin, T., 2007. Semiochemicals for insect pest management. Pure Applied Chemistry, 79(12), pp. 2129-2136.
Rabb, R., 1971. Naturally-Occurring Biological Control in the Eastern United States, With Particular Reference to Tobacco Insects. In: C. Huffaker, ed. Biological Control . Boston: Springer, pp. 294-311.
Reddy, G., 2004. Interactions of insect pheromones and plant semiochemicals. Trends in Plant Science, 9(5), pp. 253-261.
Rodriguez-Saona, C., 2012. Manipulation of Natural Enemies in Agroecosystems: Habitat and Semiochemicals for Sustainable Insect Pest Control. In: S. Soloneski, ed. Integrated Pest Management and Pest Control: Current and Future Tactics. Rijeka, Croatia: InTech, pp. 89-127.
Tumlinson, J., 1988. CONTEMPORARY FRONTIERS IN INSECT SEMIOCHEMICAL RESEARCH. Journal of Chemical Ecology , 14(11), pp. 2109-2130.
Tumlinson, J., 1993. Semiochemically mediated foraging behavior in beneficial parasitic insects. Archives of Insect Biochemistry and Physiology , 22(4).
Williams, L., 2008. EAG-active herbivore-induced plant volatiles modify behavioural responses and host attack by an egg parasitoid. Journal of Chemical Ecology , 34(1), pp. 1190-1201.
Yu, H., 2010. Electrophysiological and Behavioral Responses of Microplitis mediator (Hymenoptera: Braconidae) to Caterpillar-Induced Volatiles From Cotton. Environmental Entomology , 39(2), pp. 600-609.