Naturally Occurring Chemicals and Environmental Cues and Current Application
Shawn S. Gartside
EN 570-Spring 2000
Abstract
There is a war going on in the biotic environment around us. The constant fight for survival between plants and herbivores have produced many highly specialized defense and attack strategies. This review will describe in some detail some of these interactions the have led to the chemical and biological warfare between plants and their enemies.
There are many types of defenses that plants can express. Herbivory induced chemical defense is very common throughout the plant community. These inducible defenses can take many forms that target a variety of both enemies and allied. Plant toxins are often produced in response to herbivory that can either kill the intruders outright or reduce their capacity for normal functioning or reproduction. Induced plant defenses can also call on reinforcements from beneficial parasitoids that can greatly reduce herbivory from their foes.
Direct chemical defenses are also effective in plant-insect interactions. These also come in the form of toxins but these chemicals don't have to be induced. They provide an umbrella of protection against many generalist and specialist insect species. A delicate balance of these two defenses is considered with respect to the multitude of environmental cues and pressures.
Herbivorous insects however are not without their own weapons. Various strategies and new behavioral techniques are constantly being developed and used to counter the effects of plant defense and predation to increase their success. One such technique is the adaptation of insects to harmful plant chemicals is very effective as this allows for herbivores to become specialists who can then exploit a no longer toxic plant. Herbivorous insects have even developed ways of adapting by sequestering the plants chemical defense and using it for themselves against predatory insects.
Another main theme in the general scheme of insect fitness is the chemical and visual cues in the environment that trigger successful oviposition by female insects. They have complex methods of sensing and deciding whether possible oviposition sites meet the right requirements acceptable for laying her precious package of eggs.
Only by paying close attention to these intense plant-insect interactions can we attempt to benefit from these naturally occurring chemicals and behavioral cues. Parasitoid manipulation and knowledge of intricate allelopathic relationships can also offer valuable information that we can use in developing effective methods of natural biocontrol.
Introduction
Ecological responses to both direct and indirect defenses are vastly complex and understanding of them must be considered from a co evolutionary standpoint. Parasitoid manipulation by plants is a valuable weapon in the war against attacking herbivore specialists. A mutualistic relationship between plants and parasitoids that has co evolved include a complex web of plant-herbivore-predator interactions. As one member develops new methods for success, another will evolve adaptations that can exploit those defenses. These adaptations to defenses can be described as a continuous pattern of co-evolution1 of all members in an ecological microsystem.
Plant Defense Strategies
Direct and indirect defenses
One type of defense used by plants can be described as plastic-induced defenses. This occurs in nature when a single genotype, when exposed to recognizable environmental cues, can produce several phenotypes that increase overall plant fitness in those environments. These cues, when properly identified, can elicit the expression of the best possible phenotypic variation to succeed in harsh or high-risk predatory conditions2. However there is a cost for the expression of such an induced defense to some plants as seen in the lack of male reproductive character in wild radish plants. Due to the genetic change in phenotype, the plant will increase in fitness but has sacrificed expression of the genes necessary for normal reproductive function3.
Plants have also developed induced defenses from herbivorous insects at a more complex tritrophic level as evident in the induced systemic plant response by the oviposition of egg laying insects. It is suggested that chemicals released in the oviposition process that come in contact with the damaged leaves of elm trees, produce unique volatiles. These volatiles are attractant to egg-parasitoids resulting in greater predation and decreased herbivory from hatched larvae4. It is evident that plants and insects have developed in the presence of the complex adaptations of other species and show variation in their responses that are dependant on their environment and the co-evolution with its members.
Evidence of these intimate relationships is expressed in recent literature. Research has revealed one way that Nicotiana attanuata has adapted to cope with different environmental cues. Nicotine is used by N. attanuata as a direct defense against generalist herbivores, but the larvae of one ant species, Manduca sexta, have adapted to the toxin and are even able to sequester it and use it as its own defense against their nicotine sensitive predators. N. attanuata has retaliated in an amazing way. As and adapted response, the plant has developed a way to recognize the oral secretions of feeding larvae of M. sexta when coupled with its own Jasmonic acid produced for wound healing. The combination of chemicals triggers an increase in the levels of ethylene volatiles that are released. The flood of ethylene acts as an inhibitory factor in the plants own nicotine response, thereby reducing nicotine concentrations in leaves and also the feeding M. sexta larvae. The lower levels of nicotine in larvae, maintains the effectiveness of beneficial predation, which increases the plants defense against the adapted herbivoir5. This ethylene-mediated switch is a specific response that serves as a mechanism for converting from a direct chemical defense to an indirect defense strictly dependent on specific environmental pressures.
Another alternative to induced chemical defenses that plants express is a change in individual morphology. One example of this occurs with Mediterranean plants that evolved under high pressure from ungulate browsing mammals. Plants under intense pressure from ungulate browsers can effectively escape by changing their morphology. Producing smaller leaves and dense shoots proves to be an effective means to reduce foraging efficiency, thereby decreasing the rate of future damage6.
Insect predators can also adapt to toxins much in the same way as herbivorous insects. One such example is the resistance that two spot ladybird larvae Adalia bipunctata have for high levels of the toxin GNA (galanthus nivalis agglutinin) or snowdrop lectin. Artificial diets of GNA laden aphids resulted in no acute affects to growth or development, however approximately 40% more aphids were eaten to maintain normal growth as nutritional value of GNA reared aphids was reduced. This illustrates how a plants chemical defense can be used as both a direct against aphids and an indirect defense utilizing a specialist predator7.
Research suggests that plants can sometimes choose whether to expend energy developing direct chemical defenses against herbivorous insects, or rely on a more energy efficient indirect strategy for protection. Two species of willow, Salix phylicifolia and Salix myrsinifolia, have developed different ways of dealing with the same problem of defoliation by foraging insects. S. phylicifolia has a chemically weak defense against herbivorous insects. They count on insectivorous birds to recognized high populations of insects by assessing foliage damage while flying overhead. Concentrated feeding by birds then reduces the threat of defoliation. The same birds will pass over S. myrsinifolia as they protect against attack by intense chemical defenses aimed at reducing insect herbivory directly8. Both tactics work effectively and the choice for either direct or indirect defenses, seem to be environmentally driven.
Insect Strategies
Insect diet
It's a two way street when it comes to inducible defenses. Insects have also developed induced defense in response to plant toxins. Detoxification as a direct defense by generalist insects is a means for dealing with a wide variety of toxic chemicals from a diversified diet. However, detoxification can also be an induced response for insects in some situations. Desert locusts, Schistocera gregaria, show limited adaptation when they ingest high levels of glucosinolates present in their diet of Schouwia purpurea. Glucosinolates induce the production of myrosinase in the midgut that enhance detoxification and increase tolerance. This response by the desert locust enables them to survive on a highly toxic diet without effective growth or development. However, glucosinolate induced defenses are relatively short term and long-term exposure can negatively affect insect fitness. This short-term tolerance would help S. gregaria endure times of nutritional scarcity9.
It was previously thought that the prey species consumed by most generalist predators contained relatively equivalent nutritional value10. However it has recently been shown, at least for the wolf spider Schizocosa stridulans, that the quality of food is also a concern for some predacious generalists. Varieties of prey may have differences in their constituents including energy content, nutrients, and toxins. These factors must be weighed when determining the overall nutritional value available to even the most opportunistic predatory insects such as spiders. Species-specific behavioral characteristics and nutritional also needs be taken into account when determining the food value of prey by some opportunistic spiders11. The requirement for a mixed species diet would seem to be beneficial, especially when essential prey becomes scarce.
A mixed diet has also been described to be beneficial to predatory insects and their ability to produce eggs. Many insects show decreased egg production when prey that only offers energy and nutrients for maintenance of adults is available, considered alternative prey. Essential prey, in contrast, is necessary for the reproductive efforts and egg production in predatory insects. It has been recently illustrated that a mixed diet of both essential and alternative prey enhances the ability of generalist predators to produce a greater number of eggs beyond a diet consisting of strictly essential pey12. Therefore a mixed diet would prove to be beneficial especially when a limited amount of essentials are available. This feeding technique can increase the range of functioning species as well increase survival in times of resource scarcity. Although egg production is low when feeding on a diet of alternative prey, it is not in vain and serves a valuable purpose. Aphidophagous ladybirds for example may use these small numbers of eggs produced on alternative diets as a timing mechanism that can exploit the short-lived colonies of aphids13.
However, from a plant perspective at a multitrophic level, a mixed diet could prove to be detrimental to plants that show induced chemical responses to herbivorous insects. By increasing the toxic levels of its foliage, the toxin levels would also increase in the herbivores. This could effectively decrease their nutritional value for beneficial predatory insects. As plants inducible defenses are activated, generalist predators may search elsewhere for a more nutritional or less toxic diet. In this instance, the induced defense must be totally effective as they lose some protection at the higher trophic level. If an herbivorous insect adapts to tolerate higher levels of induced toxins, it would prove to be disastrous as herbivory would increase due increased insect resistance and decreased predation by generalist. The combination of increased herbivore tolerance and resulting decrease in nutritional value for predatory insects accounts for a total reduction in both direct and indirect defenses.
Insect oviposition strategies
The initiation of probing by parasitoids can be dependant on a threshold concentration of allelochemicals most likely mediated by antennal sensilla. In conjunction with this, ovipositior sesilla contribute to the overall time spent by females in a particular area. This multisensory activity helps to ensure that energy is spent wisely when searching for suitable oviposition sites14. Further research suggests a hierarchy of sensation is the case when considering oviposition. Host selection for insects when considering oviposition sites is very important to the female insect. Host selection by Melittobia digitata is a complex three-step process. The first and most vital step is shape recognition. Once an acceptable shape has been identified, the female will with both antennate and probe the prospective host to identify the presence of specific chemical cues and then probe the host with the ovipositor to determine nutritional suitability her larvae will need to survive. At this point, the decision for oviposition is made taking into account carefully these three factors. A single female may pass up many prospective hosts if requirements are not to her satisfaction. In this case the ovipositor itself acts the most vital sensor to inform the wasp of the suitability of the host for oviposition15.
Another variation in ovipostion location can also affect larval survival rates and performance in herbivorous insects. Yamaga and Ohgushi studied the effects of oviposition in a lady beetle Epilachna petulosa on two plant species: Cirsium kamtschaticum, a thistle, and Caulophyllum robustum or blue cohosh. They found an interesting pattern in larvae success between these two co-occurring plant species. This relationship was attributed to a variation of intraspecific competition on blue cohosh and increased predation from arthropods on thistle in subsequent years. The first year studied, oviposition on blue cohosh resulted in a large number of larvae. As the larvae grew and ate the leaves, increased defoliation led to intraspecific competition and fewer larvae reached the adult stage. This created an increased preference of E. petulosa to lay eggs on the more abundant thistle the following year. This oviposition site also had its downfalls. Lurking about the thistle are two species of arthropod predators. As the number of developing larvae increases, so does the rate of predation, hence an alternation of preference for oviposition by E. petulosa from year to year16. This example demonstrates that a preference for oviposition can be directed by both intraspecific competition for nutritional food material and also by interspecies predation pressures within the same small ecosystem.
Environmental temperature is also a factor used by female insects when considering oviposition rates and fecundity. Chilocorus nigritus showed a trend for increasing both oviposition and total eggs laid with increasing temperatures. A change in temperature stimulated the activity and there was no increase in constant elevated temperature within a range of 20O C to 30O C 17. This data suggests that a female insects can recognized changes in temperature and produce more eggs as the weather becomes more suitable. This reaction would benefit the insect as it would not waste valuable energy producing large amounts of eggs or searching for oviposition sites when the temperature is dropping below suitable levels for larvae fitness.
Focusing on biocontrol
The field of chemical ecology is on the cutting edge of science as economic applications are becoming more apparent. The study of natural defenses of plants is helping in pest management techniques in agricultural crops. Increased awareness of the benefits of allopathic interactions coupled with knowledge of natural biological controls against plant enemies have also been used to increase the plants indirect defenses18. These factors can greatly improve the future sustainability of pest management in an agricultural system.
A recently developed screening technique has been discovered that can effectively separate the effects of allelopathic chemicals from competition. The method is called equal-compartment-agar-method (ECAM). This screening technique was developed to determine allelopathic potential of wheat, Triticum aestivum, on the inhibition of rye grass, Lolium rigidum, root growth during sowing time. Activated charcoal is added to an agar medium and placed between the two species of plants. ECAM effectively alleviated the allelopathic inhibition of wheat to rye grass roots19. A wide range of applications can be considered with ECAM and should be explored with respect to the many other allelopathic events in a variety of economically interesting plant specie interactions.
The goal of agroforestry is to maintain sustainable land use by the incorporation of woody species with agriculturally important crops that can help to decrease soil erosion while providing unique allelopathic benefits to the system. Temporal sequences and tactical spatial arrangements with respect to allelopathic contributions must be carefully considered to encourage both the production of food and sustainability of the land as a resource20.
We must be extremely careful in assessing the effects of insecticides. Widespread effects occur not only on target pest species, but also on beneficial species. Mortality rates are the norm for measuring insecticide performance but more studies are showing that the intricate balance of beneficial parasitoids and host plant relationships are being negatively affected by sub lethal doses. It has been reported that the parasitoid Microplitis croceipes that are commonly introduced in cotton, Gossypium hirsutum, have decreased host foraging ability by female insects after insecticide application 21. This practice is considered counterproductive to the success of the desired biological control obtained from releasing M. croceipes into cotton fields.
By watching the natural relationships and interactions in the agricultural environment, scientists are able to isolate specific natural chemical signals that are observed to elicit a predictable response. One such observation is the parasitoid Aphelinus asychis that is used as a biocontrol agent of the aphid. It was found that when presented with a chemical mimicking a host-plant complex, malathion, the parasitoid response was highly attractive22. Application of malathion to plants can be used as an effective attractant to lure these beneficial parasitoids and increase the success of natural occurring biocontrol.
Another avenue of research that is currently being pursued involves the western corn rootworm. It has been discovered that the corn rootworm larvae are highly attractive to even lethal doses of carbon dioxide. Natural concentration gradients of CO2 produced by the roots of corn serve as the environmental cue that fragile root worms need to find their host. Research is now being done to develop compounds that can copy the signals given off by corn thereby by confusing the larvae and reducing eventual damage done due to feeding23. This method and other natural methods such as these would greatly reduce the risk that some pesticides pose to the environment and the future sustainability of the soil. Nature has developed an intricate system of communication and we're finding more about these interactions through research and careful observation. We need to focus on nature's own blueprints to produce more effective means of biocontrol that could someday put an end to the negative health and environmental issues that plague current pesticides today.
References