Another factor is the right timing of the release. It seems so evident that there must be eggs for egg parasitoids, but their density is not regular. Flight activity of adults describes curves, with peaks every 4 to 5 weeks according to temperatures, when captured in traps (speaking about open field crop tomato for industry) and so do eggs present in the field. H. armigera females can put 500 eggs per night, distributed one by one on the crop, (we had about 44.000 plants per hectare, with about 120 leaves per plant during the season, to produce 40 fruits per plant). Eggs were deposited on the upper outer third. In southern Portugal, we had 3 generations of H. armigera (and several Plusiinae species) on the crop, and the overwintering 4th.

Strand & Vinson 1984 determined by lab experiments that Trichogramma can only parasitize a host egg during the first 56 hours after oviposition. Later, the ovipositor would not enter any more into the embryo in development.

On the other hand, Trichogramma is only working in day light (Hassan) which means that the nights help the embryos to develop (if temperature is high enough), and the age "window" is closing for efficient parasitization. Egg parasitoids don't need to keep in the field (they have wings), if there are fresh eggs of other lepidopteran (or Neuropteran) around. Trichogramma has a life cycle (here) of about 14 days, H. armigera of about 5 weeks, at the same temperatures. H. armigera adult longevity in the field might last for 4 weeks, with an overall oviposition up to 2500 eggs per female, during this period... but if there are web spiders, or bats and owls, when armigera starts to fly at dawn, they might not see the next day. All these factors determine the efficiency of releases. The better we know the "receiver system" (field ecology), as I called it in my PhD Thesis, the better the donor system will work. If you are interested in more details, just ask.

At first place one must consider climate variables (precipitation and temperature). If these factors are limiting the ontogenetic development and/or daily activity of agents, then it does not make sense to think on other factors. Probably climate is one and most important in these respect. If one aims to establish biocontrol agents for a long time, than number of other potential bio-abiotic factors could be considered depending on the species.

One biological important factor is "intraguild-predation" where a large body of literature exists. In short more general predators such as lacewing larvae or ladybugs can also prey on other predators, parasitoids or parasitised pests and also disturb/deter them.

The most important abiotic factors are surely temperature and humidity, as most insects have an optimal range in which they "work" best (being active, have lower mortality, highest performance etc) whereas too low or too high values can lead too reduced performance (e.g. inactivity), higher mortality or dispersal to more suitable localities.

Field margin structures are quite important for beneficial predators and also the surroundings (e.g. high-yield crops, fallow etc.):

Tscharntke, Teja; Randl, Tatjana A.; Bianchi, J. J. A. (2005): The landscape context of trophic interactions: insect spillover across the crop-noncrop interface. In: Annales Zoologici Fennici 4.

http://www.sekj.org/PDF/anz42-free/anz42-421.pdf?origin=publication_detail

Another factor is the right timing of the release. It seems so evident that there must be eggs for egg parasitoids, but their density is not regular. Flight activity of adults describes curves, with peaks every 4 to 5 weeks according to temperatures, when captured in traps (speaking about open field crop tomato for industry) and so do eggs present in the field. H. armigera females can put 500 eggs per night, distributed one by one on the crop, (we had about 44.000 plants per hectare, with about 120 leaves per plant during the season, to produce 40 fruits per plant). Eggs were deposited on the upper outer third. In southern Portugal, we had 3 generations of H. armigera (and several Plusiinae species) on the crop, and the overwintering 4th.

Strand & Vinson 1984 determined by lab experiments that Trichogramma can only parasitize a host egg during the first 56 hours after oviposition. Later, the ovipositor would not enter any more into the embryo in development.

On the other hand, Trichogramma is only working in day light (Hassan) which means that the nights help the embryos to develop (if temperature is high enough), and the age "window" is closing for efficient parasitization. Egg parasitoids don't need to keep in the field (they have wings), if there are fresh eggs of other lepidopteran (or Neuropteran) around. Trichogramma has a life cycle (here) of about 14 days, H. armigera of about 5 weeks, at the same temperatures. H. armigera adult longevity in the field might last for 4 weeks, with an overall oviposition up to 2500 eggs per female, during this period... but if there are web spiders, or bats and owls, when armigera starts to fly at dawn, they might not see the next day. All these factors determine the efficiency of releases. The better we know the "receiver system" (field ecology), as I called it in my PhD Thesis, the better the donor system will work. If you are interested in more details, just ask.

In greeenhouse intensive horticulture, the crop is of the utmost importance to any pest control strategy, the phytosanitary state of which is dependant on the cultural practices it is subjected to (irrigation, fertilisation, pruning, etc.). These will consequently have a decisive effect on the management of the beneficial fauna used in the greenhouse. It is therefore necessary, to synchronise cultural tasks (pruning) with the release of beneficial insects to avoid any interference with the establishment of these natural enemies. Pruning, if possible, should always be carried out prior to releases, and refrained from during the two following weeks.

Biological pest control efficiency is tightly interrelated with greenhouse characteristics

and equipment, their handling and also crop and beneficial biological agent management. The greater the knowledge of these interrelations, the higher the effectiveness and efficiency of integrated pest and disease management practices in greenhouse horticultural crops.

From our experience in semi-closed (strawberries) and open air crops (tomato) meteorological conditions and release dates would be very important factors to consider because it may much limit biocontrol agent establishment. Chemicals drifts from neighbouring plots and timing of some agricultural practices may also interfere the performance of some species. Hope this helps. Cheers.

Dear all,

Many thanks for your contributions, great!!

Well, in addition to all of the limiting factors you cited above, I can add the two following biotic factors known to hamper the action of natural enemies when attacking their host insect pests:

1/ The presence of tending ants: the case of mutualistic interactions of these ants with honeydew-excreting hemipterans such as scale insects (especially mealybugs), aphids and psyllids.

Indeed, in this case, tending ants are capable of disrupting or killing parasitoids and/or predators to protect these hemipteran insects in an attempt to having easier access to the sugary-rich honeydew (primary food resource for ants) secreted by these latter insect pests. To avoid such a problem when using natural enemies, those tending ants should be effectively and sustainably controlled prior to using either predators or parasitoids in biological control programs. Effective control of these ants can be achieved using direct insecticidal sprays and/or using liquid baits.

2/ The occurrence of encapsulation process.

Encapsulation is a host immune defense mechanism used by an insect (hemocytes and other cells of the host insect organism) in response to an attack/invasion by an endoparasitoid or another foreign organism): as consequence, the parasitoid will be killed inside the body of its host insect pest.

To avoid this problem, it is highly recommanded to use species-specific (specialist) parasitoids instead of using generalist parasitoids when implementing biological pest control programs.

Further contributions are appreciated!!

Cheers

Another limiting factor is the use of insecticides. Parasitoids are very susceptible to insecticides.

Prof. Phillip Nkunika, University of Zambia.

Hi Ramzi,

I will just add a short comment concerning host resistance to parasitoids by showing this paper by Oliver et al 2005, showing that resistance is linked to the presence of bacterial symbionts:

http://www.pnas.org/content/102/36/12795.long

All the best,

Yann

Hi Yann-David,

Thank you so much for your answer and for providing the link to this publication.

Yes, absolutely, this is another possible biotic factor limiting the action of a parasitoid on its host insect pest. So, according to the article that can be found through the link you’ve provided, bacterial symbiont-mediated resistance to parasitism is a phenomenon that can hamper parasitization of pea aphid Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) by the parasitoid wasp Aphidius ervi Haliday (Hymenoptera, Braconidae); for this case the occurrence of this type (and the level) of resistance to the parasitoid wasp is strictly dependent on the (heritable) bacterial symbiont isolate (in this case, aphid genotype do not determine host aphid resistance to parasitoid).

Best regards,

Ramzi

Dear colleagues,

Thanks for all these interesting practical information. Surely, that does help for taking into consideration factors that hamper the establishment of a good integrated pest management in crops. There are two aspects that has not been discussed yet above, which are the shelters providing a sustainable protective habitat & the population dynamic of the natural enemies, parasitoids and predators respectively.

In the oil palm plantations, they are using beneficial plants around blocks sheltering various parasitoids and providing them with a long term habitat, giving parasitoids a sustainable presence that could become preventive against potential pest defoliatiors outbreaks (i.e bagworms, Metisa plana and Pteroma pendula).

The effectiveness of a biological control agent is also based on the stability of its population dynamic for a long term operational control in field plantations against pests. If the population is unstable cause of a weak threshold dynamic, the pests would still overpower and outnumber the available control agent. My work in oil palm plantations in Malaysia and Indonesia permitted me to observe this with Oecophylla smaragdina, the Asian weaver ants. There is till further work to be done on dynamic population in long term study like 10 years period.

The ability of natural enemies in effective regulation of pest dynamic population below economic threshold has been amply proven (Zhang and Swinton, 2006), with some recommendations on dependence reduction of pesticides towards achieving harmless application in order to avoid injury level to natural enemies, thus sustaining their safety with the dual direct interest and benefit of preservation for the stability of the oil palm agro ecosystem (Wood, 1968; Wood, 1973; Wood, 2002).

Related to Zhang & Swinton, i propose the following:

http://www.ucl.ac.uk/bioecon/8th_2006/Zhang_Swinton.pdf

http://www.aec.msu.edu/theses/fulltext/zhang_phd.pdf

Another paper specific to oil palm pest with parasitoids and predators documented as follows:

http://palmoilis.mpob.gov.my/publications/joprv8dec1996-dhileepan.pdf

Beside those factors, as mentioned above the time of release is paramount but related to the life cycle of target taxa insect pests. You need to know the weakest time to attack those pests = right time of release, usually during eggs release and larval stage of development. But within the same large monoculture, there are discontinuity of pest occupation in various blocks, eggs hatching process occurs variably.

From my field survey experiences on certain predators, noticed one like Sycanus sp are scarce compare to the high number of individual defoliators pests. Without rearing for a mass release, in that case the predator is inefficient.

http://hbs.bishopmuseum.org/pi/pdf/14%281%29-57.pdf

Eminent scientists (ecologist, entomologist and environmentalist) around the world agreed on the deleterious effects of broad spectrum long range contact (bslrc) pesticides against natural enemies and the natural fauna alike. Literature is wide on this topic. Those of the range of pyrethroids and the like aromatics.

http://edis.ifas.ufl.edu/pi091

Finally, heavy rain can help opportunistically to reduce pest during eggs deposition and early larval stage instar, by wash-off direct effect causing high mortality: this is good, not hampering...

Pierre (French Island of Martinique near Miami Florida USA)

It all depends of your system, but one other things that come to my mind in addition to the answers you already gathered is "endosymbionts". If you introduce insect in the field, check if the naturally occurring population is infected with the same symbionts, over wise incompatibility may arise and the next year your parasitoid/predator population may crush to lower level than it already is.

Dear Exélis and Anne,

Thank you so much for your contributions!!

Further to all answers above, I can add that: non-attractive host plant volatiles (odours) also could negatively impact (hamper) parasitoid’s action toward its host insect pest (these volatiles mask the attractive effect of the host-induced (E)-β-caryophyllene to an egg parasitoid). You can find out further details about this issue in this newly published article entitled “Smelling the tree and the forest: elm background odours affect egg parasitoid orientation to herbivore induced terpenoids” by Büchel et al. (2014) through this link:

http://link.springer.com/article/10.1007/s10526-013-9544-9#page-1

Cheers

Dear Ramzi,

Specific host-parasitoid interactions are the results of co-evolutive processes. When a parasitoid is searching for its host, many chemical filters (for example) of compatibility have to be passed at both long and short ranges (it is the same within the host with immune system). Thus for example, if one parasitoid coming from Asia is introduced to South America, this one could be not able to detect or recognize the target host even if the host is cosmopolitan. Indeed, in the introduction area, the host could feed on different plants emitting different volatile compounds. The host itself could have different cuticular compounds. Both could compromise the host detection and recognition. This is the results of the geographic mosaic of coevolution. Cf. papers of Thompson.

The presence of a better host than the targeted one is also possible. But in that case, the introduced population of parasitoids should be able to survive.

Bests regard

Dear Dr. Olivier,

Thank you so much for your well- written, clearly explained contribution. I totally agree with you; indeed co-evolution has a noteworthy impact on such plant-insect interactions that may be either beneficial (in other cases) or not (the case we are discussing here) to insect parasitoids (although the survival of the parasitoid may not be affected). Due to the importance of chemical ecology of plant-insect interactions, I asked last week in ReseachGate a question in this context (how to manipulate insect behavior through adequate exploitation of plant volatiles), I invite you to see the full discussion via this link : https://www.researchgate.net/post/How_could_host_and_non-host_plant_volatiles_be_adequately_exploited_to_manipulate_insect_behavior_for_enhancing_integrated_pest_management_programs

As you stated above, this is true especially for new invasive insects invading new areas (new ecosystems including new host plants). The overall success of these invasive insects (either parasitoids or pests) would depend on their positive adaptation with the new invaded ecosystem.

Best regards

I just saw this paper, maybe you should have a look:

Goldson et al "If and when successful classical biological control fails". Biological Control. (in press)

Best regards

Dear Dr. Olivier Roux,

Thank you so much for your precious response, great!! Yes this publication truly matches our discussion. I’ve just seen the Abstract and it seems to be very interesting article, I’ll try to get its full text later once published. Indeed, successful establishment of an invasive insect in newly invaded areas would not be so easy to occur, involving failure of the classical biological control program implemented.

Best regards

one of the most important aspect of the efficacy of the parasitoide to be effective on noctuid lepidopteran pest is a natural biorhythm It is generally seen that the max egg laying of noctuid leps is around New moon day if the noctuid parasite is released on these days it will be highly effective to parasitize the freshly laid eggs

Species resistant due to a history of indiscriminate use of the pesticide is also a limiting factor..secondly the mutation of species and emergence of sub species is also a limiting factor.

Number of good thoughts and published articles already mentioned here, that's nice. Generally, abiotic factors hamper when natural enemies introduce from far away, in that case locally available enemies should be given preferences. Many causes are included in biotic factors, of those, intra- and inter-specific competition including multiparasitism, superparasitism etc. are important. In this case, host density should be in mind and food availability of adult natural enemies should be considered during release of natural enemies. Otherwise the populations of natural enemies will be breakdown soon afterward.

With best,

Dear M. Mostafizur,

Thank you very much for your precious contribution!!. Yes, I totally agree with you; indeed the factors you mentioned should also be highly considered when implementing biological pest control programs.

Best regards

Dear Ramzi Mansour,

Thanks a lot for mentioning me. One thing I forgot to raise here that is host feeding. Though we know that host feeding is also a way to control target pest populations but it, indeed, hamper on the offspring production of natural enemies. So, if there prevail food crisis for adult wasps, they will feed host. Flower honey is the main food of adult wasps. That's why, if there is no or little flower in the target field/ greenhouse, we may spray there artificial honeydew to avoid host feeding.

Thanks once again.

With the best..

Maybe some information on Trichogramma brassicae (and T. ostriniae) used in our experiments on biological control of Ostrinia nubilalis (European corn borer - ECB) would interest you.

As mentioned above by Carola Meierrose, the correct timing of release of Trichogramma brassicae is crucial for a successful biological control strategy. Ideally, the timing of egg parasitoid release should anticipate peak ECB oviposition . Asynchrony between parasitoid release and ECB oviposition activity can drastically reduce parasitation efficiency. We carefully timed our releases so that they coincided well with the beginning of more damaging second generation ECB flight. We, besides monitoring the ECB aduls using light traps, carefully observed the development of first ECB generation. When pupation of the first generation reached 30% we planned the release one week later. This insured a significantly higher parasitation rate in release plots.

Another important thing, as you already mentioned, are adverse environmental conditions. Several papers report that drought and heat may prevent or obscure significant differences of crop yields between T. ostriniae release plots and control plots. Moreover, high temperatures can reduce Trichogramma spp. efficacy. Thermal shock has been shown to negatively affect T. brassicae and T. ostriniae. Papers report that high temperatures (35 or 44°C) reduces emergence, longevity, and fecundity of T. brassicae.

Other experimental confounding factors include parasitoid emigration, quality of Trichogramma spp., surface density of parasitoid release, ECB population density, and presence of indigenous Trichogramma spp... Hope any of this helps!

Interesting, Jaka Razinger, that you mention high temperatures (35-44ºC) what reminds me of some testing we did. Onillon (France, Versailles) had tested our Trichogramma cordubensis strains at those high temperatures in the lab and concluded they couldn't do their job under these conditions.

But ours had been collected from parasitized host eggs, out of nature, with those conditions. So, we used a "Squirrel" measurement instrument locating a series of sondes into the crop and registering the effective temperatures, a day with very high temperatures, and another with moderate ones. (speaking of furrel irrigated field tomato in the Mora region of Southern Portugal): we placed different sondes on top of the leaf surface, under the surface, both located either in direct sun or in the shade of upper leaves, on top of green or red tomato fruits, inside those fruits, and found out that the evapo-transpiration of the leaves could buffer up to 16ºC between the temperature above the crop canopy and the shady part (where the mobile insect stages stay when the air temperature can, for some hours, reach 53ºC. We measured on dry soil, where the tomato plants grow, 56ºC (with diverse thermometers offered from the Physics department of U Evora, under the control of a Physics professor). So, when the "outside the crop" day temperature was 48ºC, under the crop canopy we found temperatures about 32ºC. And 32ºC were viable for the Trichogramma species we found in the fields, mass reared and released again. (My PhD Thesis, 1991). Try it out in other crops, it is interesting!

Parasitoids are host specific..one practical challenge we had with Encarsia formosa in Kenya was mixed population of both Greenhouse Whitefly (Trialeurodes vaporariorum)and Bemisia tabaci in the fields..given that Encarsia prefers T. vaporariorum..it had very little success in kenya.

Secondly the temperatures were high..especially for farmers who attempted to use it outside while our exports to Europe under greenhouses and in controlled tempratures were doing an excellent job..

Bioticontrol agents are susceptible to biotic and abiotic factors. Biotic factors like status of insect (host) larvae regarding resistance or tolerence , collection site and host plant , stage etc. Abiotic factors like humidity and temp. are responsible for the effectiveness of parasitoides as they are very host specific and Sensitive .

Speaking about larval parasitoids, there has in time been mentioned the fact that some Noctuids like H. armigera are feeding on plants with high contents of secondary plant alcaloids (tomatine, maisine, nicotine) which function with many insects as food deterrents, or kill them (you'll never find ants on tomato plants). The question was that the insects preserve in their hemolymph enough toxin to kill developing parasitoids but are not killed themselves. I think to remember that H. armigera was equipped with an enzyme system detoxicating these plant substances and thus certain pesticides too. I think these data were developed in France /French (Avignon INRA) and the main key word was tomatine. These substances / facts would reduce the self propagation of released natural enemies (Cotesia kazac) in the field, and their effect, we are counting upon with Trichogramma.

The principal factor: correct taxonomic determination of natural enemies!!!!

You must be careful with exotic biocontrol agents, first you need to find local fauna with the potential to control your pest.

Then there are many factors, biotic, abiotic, even social and economical, who can limit your biocontrol success!!!!

In Mexico, many farmers think that parasitoids can be a potential pest for their crops, so, the educational farmer level can be a limiting factor.

Added to the above interesting feedback, the host plant would be an important factor in carnivores performance. It is widely known that carnivores make use of the herbivore induced volatiles (HIVs) from infested plant hosts. These HIVs are completely variable based on various factors as host plants, varieties and inbreed lines of the same plant, environmental factors (i.e.: photoperiods, temperature, drought, soil conditions, and nutrition). Thus, all aforementioned conditions could subsequently affect the released HIVs which eventually perceived by the natural enemies and thence impact their foraging in locating their hosts or victims. Interestingly, the higher trophic level (secondary parasitoids) is also affected by the same factors (for more details, please check the attached paper).

Dear Islam,

Thank you very much for your very interesting answer and for the key scientific article you have provided. Yes, I totally agree with you, all points you mentioned above should also be highly considered for ensuring a successful action of pest's natural enemies (especially parasitoids).

Best regards,

Ramzi

It is a preliminary observation (not yet proved and a detailed work is in the way):

that in the surroundings of a target crop, presence of an unrelated crop (the plants where neither the host nor the parasite is found) could cause effects on the parasite populations specially in the green house environment.

...

Dear Dr. Ramzi,

Greetings! This discussion you have initiated four years ago is indeed very helpful for us, aspiring researchers in this field. For me, it is very relevant since I am working on my master thesis regarding this topic (biological control). I am particularly interested about your comment about the ants tending to honeydew-excreting hemipterans. Although it is pretty obvious (since they attack non-myrmecophilous species), I am concerned on the proper citations of this claim. I would really appreciate your recommendations regarding articles or links that would indicate that it is one of the limiting factors in the use of biological control agents. Thank you very much for your guidance!

Sincerely yours

Hi Terence,

Thanks for your comment. OK, you are very welcome !! To do so, I need receive your email address to send you several scientific articles explaining how biological control (using predators and/or parasitoids) can be hampered by tending ants. The action of the latter constitute indeed a major limiting factor in achieving successful biological control.

Best,

Ramzi