Inhibitors of Growth Development and Reproduction

That many plant extracts suppress the growth of insects in a laboratory setting is little more than an explanation and confirmation of one of the most obvious "non-events" in biology - the observation that insects do not defoliate terrestrial plants on a widespread scale, except in highly disturbed and anthropogenic ecosystems, e.g., crop monocultures. This non-event is attributed to plant secondary chemistry evolved to deter or otherwise thwart herbivores, of which insects are the largest class. This is also the common explanation for the fact that most plants are unsuitable as hosts for most herbivorous insects -host-plant specialists are more common taxonomically speaking than generalists.

According to one authority, demonstrating that plant secondary compounds are toxic, repellent or growth-inhibiting to herbivores has become a minor industry supporting professional ecologists. One could easily extrapolate that comment to include natural product chemists, in part because demonstrations of bioactivity better justify their search for novel molecules, and in part because insects are convenient (and arguably economically significant) organisms upon which laboratory bioassays can be conducted. And among bioassays with insects, those that purport to demonstrate inhibition of insect growth are the easiest - simply add a plant extract to the insect's normal diet (artificial or otherwise) and compare growth to controls maintained on untreated diet -although the interpretation of results is not as simple. Why? Because a reduction in insect growth can be a consequence of behaviour (feeding deterrence or anorexia), of physiological malaise (sublethal poisoning or impaired nutrient utilization), or a combination of the two. So while it is relatively easy to find plant extracts or allelochemicals that interfere with insect growth in the laboratory, what proportion of these actually show bioactivity at a level that suggests potential uses in crop protection?

We have screened numerous plant extracts over the past 30 years in search of new botanical insecticides; in our experience, the proportion of extracts that are potent inhibitors of larval growth (based on noctuid caterpillars feeding on artificial media to which plant extracts are added) is quite small. Our standard screening concentration has been 1000 ppm (0.01%) fresh weight, and we consider extracts that reduce larval growth by 90% or more to be relatively

Figure 7.3 Structures of the natural insect growth regulators juvabione and precocene II.

potent.20 Using these criteria, we found that only four of 50 extracts of Aglaia species from Southeast Asia were potent growth inhibitors,21 only one of eight extracts of Annona squamosa from Indonesia were potent,22 and only two of eight extracts of Trichilia species from Costa Rica were potent.23 Among 18 wood extracts from tropical timber species in Indonesia and Malaysia, only one was potent.24 It should also be noted that the observed bioactivity can in some cases be attributable to a single chemical or closely-related suite of chemical substances (e.g. azadirachtin in neem seed extracts),25,26 but in other cases may be a consequence of several chemicals acting in concert (e.g. rosemary, Litsea essential oils).27,28

Genuine inhibitors of insect development and/or reproduction are probably as rare as those plant substances that are acute toxins. The best known examples are those plant natural products that interfere with the endocrine control of development. These include the juvenile hormone (JH) mimicking substance juvabione from Balsam fir (see Figure 7.3), the anti-JH substance precocene II from the bedding plant Ageratum houstonianum (see Figure 7.3), and the aforementioned azadirachtin from neem (Azadirachta indica) that blocks molting and reproduction by preventing the synthesis of prothoracico-tropic hormone that in turn stimulates synthesis and release of ecdysteroids (= moulting hormone). Many studies purport to show developmental aberrations in pupal or adult holometabolous insects (especially moths) after feeding as larvae on diets containing specific plant extracts. However dietary imbalances (especially limitation of dietary fatty acids) can have similar effects, so the "developmental" effect on the insect could be very indirect.

7.2.3 Inhibitors of Feeding and Oviposition

It is safe to say that more than a thousand natural products isolated from plants have been demonstrated to deter feeding by one or more insects based on laboratory bioassays. Countless crude plant extracts have similarly been shown to deter plant feeding. The subject of plant-based insect antifeedants has been reviewed by several authors. Indeed, the frequency with which plant extracts or substances thereof have been shown to deter insect feeding suggests that this may be the most common mechanism through which terrestrial plants avoid depredation by herbivorous insects in natural ecosystems. In spite of the diversity of chemicals and plant sources with feeding deterrent bioactivity, and the general enthusiasm amongst the scientific community for their potential use as nontoxic crop protectants, hardly any such products have seen commercial-scale use.29

Interest in insect feeding deterrents and their use in crop protection was in large part stimulated by the discovery of azadirachtin, the active constituent of neem seed extracts. First isolated in the late 1960s, azadirachtin remains the most potent antifeedant for the desert locust (Schistocerca gregaria) discovered to date.16 The profound activity of this compound in the locust and other specific pests, combined with the systemic action of this compound in some plants augured well for its use as a nontoxic crop protectant. Unfortunately, subsequent studies demonstrated wide interspecific variation in the antifeedant action; for example, the migratory grasshopper (Melanoplus sanguinipes) of North America can eat azadirachtin-treated foliage with impunity.30 Furthermore, insects initially strongly deterred by azadirachtin are capable of rapidly habituating to this compound,31 and the systemic action may be limited to certain crop plants.32

In fact, the efficacy of azadirachtin as a crop protectant based on its anti-feedant action has yet to be rigorously and unambiguously demonstrated under field conditions, even though many pest management practitioners assume this to be the primary mechanism of action. In our opinion, it is the physiological actions of azadirachtin on the insect endocrine system that more likely account for the efficacy of commercial neem products currently used in North America, Western Europe and elsewhere.17 Several other plant extracts and isolated compounds have potent antifeedant action against certain pest species,29 but none of these have seen commercial use.

A number of plant substances that deter insect feeding additionally deter oviposition by adult insects33 and this mechanism could also potentially be exploited for crop protection. However, development of products based on oviposition deterrence is in its infancy and demonstration of this action at the field scale is needed.

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