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SUCCESSFUL ESTABLISHMENT OF WOLBACHIA IN AEDES POPULATIONS TO SUPPRESS DENGUE TRANSMISSION

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Now Hear This: Changing the Message About Non-Native Species – Paul Roman

“The pathway of degradation differs from that of recovery.” – Suding and Hobbs, 2009.

Restoration ecologists have long worked to restore native habitats to their “natural state” by eradicating non-native species.  Such conservation efforts need the community’s support to succeed.  To obtain this support, a clear message was crafted: non-native species (including invasives) are harmful and must be eradicated.  But this assertion is no longer entirely true.  We now know that some non-natives are actually beneficial and should be preserved…or even introduced.  Most habitats are now “novel” and will never again be “natural.”  To ensure the community’s continued support for ongoing and future restoration efforts, the message must be changed.  Realistic goals and practices must be conveyed convincingly to the public.  Economic and cultural values should also be considered.  Scientific credibility and community support are at stake.

Changing the Perspective

Global human movement of species has resulted in a breakdown of biogeographic barriers.  Combined with climate change, the consequence has been novel ecosystems and species combinations (Hobbs 2006 & Meyerson 2007).  Conservationists have declared war on these non-natives.  The battle cry has remained unchanged: native habitats should be restored to their natural state by eradicating non-native species.  This message has been forcefully and repeatedly conveyed to the public.  And to some extent the message-bearers have a point.  Some non-native species have had devastating effects: causing extinctions of native species, altering and destroying native habitat, and threatening animal and human health by spreading disease.  Non-native species are recognised as a great threat to biodiversity.  They also threaten our global environmental and economic welfare.  The estimated economic impact of non-natives, including control costs, is $1.4 trillion annually, which is almost 5 percent of the global GDP (Pimentel 2001).

But it is equally clear that some non-native species are beneficial, both directly and indirectly, to native species and ecosystems.  Conciliation biology, a subgroup of invasion biology, recognises just this. It promotes the concept that short- and long-term conservation management should include these interactions (Caroll 2011).

Restoration ecologists already know this, and more adaptive management plans now call for the preservation and/or introduction of non-natives.  Yet, the conservation community continues to deliver a contrary message to public.  Let’s take a look at some essential restoration practices that are currently in use.

Take for Example…

Taxon substitutes

Taxon substitutes are non-natives that support restoration efforts by filling ecological niches left by extinct or fragmented populations.  One example is the non-native Aldabra giant tortoise (Aldabrachelys gigantea) which was introduced to the surrounding islands of Mauritius.  These animals were intended to replace extinct native large-bodied vertebrates that served as generalists and seed dispersers.  The tortoises’ introduction has succeeded in maintaining ecosystem heterogeneity and native biodiversity.  As a result, the giant tortoise is being considered for other similarly degraded insular ecosystems around the world (Griffiths & Harris 2010, Hansen 2010).

Figure 2: Dinizia excelsa (canopy tree) http://www.jstor.org/stable/3067823

Ecosystem services

The introduced African honeybee (Apis mellifera scutellata) had an unexpected positive effect on Dinizia excelsa (canopy tree) in Amazonian pastures (Figure 2).  Due to human-induced habitat loss and fragmentation, D. excelsa was expected to experience a decline in population resulting from the disruption in mutualism by native pollinators.  Instead, the honeybee replaced the native pollinators, enabling the D. excelsa to not only thrive in fragmented areas but to have a higher vigour and genetic diversity than the same trees in a contiguous forest (Dick 2001).  Once considered a pest, this non-native has become an invaluable part of the management strategy, ensuring the preservation of this native habitat and species.

And lest we forget about biocontrol…

Biocontrol is another restoration practice which introduces non-native species to control other non-natives.  A prime example of biocontrol is the introduction of the non-native Tanzania Eurytoma erythrinae to control a non-native gall wasp (Quadrastichus erythrinae).  The wasp was introduced to Hawaii and soon attacked a native Erythrina species, leading to massive population declines (Rayna 2013).  The biocontrol successfully suppressed some of the wasp infestation, allowing the Erythrina population to partially recover.  This non-native biocontrol agent should be preserved.  It has become part of its adopted environment and will protect the native Erythrina from extinction.

Changing the Message  

Introducing and/or preserving non-natives are essential to restoring and protecting native habitats.  But how can conservationists reconcile these practices with the repeated message that all non-natives should be eradicated?  They can’t.  And worse, they will likely have trouble promoting these new practices to a public made sceptical by the conflicting messages.  The public may even lose confidence in the scientific community, seeing the changing message as an admission of faulty science.  (“Hey Alexander, did you hear that the world really isn’t flat after all?!”)  And if they were wrong before, perhaps they are wrong now.  The public may oppose these new practices or simply throw their hands up in resignation, not knowing what to believe.

Yes, the message must change, but it must be done in a thoughtful way, considering ongoing and future management practices including non-natives.  In other words, we have to learn from our mistakes.

In the excitement of a dawning movement and the rush to convince the public, scientists sometimes put little thought into crafting the message.  For example, environmentalists used to warn against “global warming”.  Scientists subsequently changed the message to the broader term, “climate change” after determining that other environmental changes posed more significant impacts on humans than increasing surface temperatures.  The changing message fuelled scepticism about the legitimacy of the underlying science, eroding public support.

In the conservation context, non-native species were once referred to as “alien” species.  That term, which conjured up visions of space invaders, was subsequently discouraged.  Similarly, “invasive” species suggests an unwelcome visitor.  “Non-native” connotes a species that doesn’t belong.  These terms implicitly suggest that the subject species is harmful and intrusive.  The negative connotation of these terms supports the message that non-native (alien, invasive, etc.) species should be eradicated.  Predictably, this will make it even harder to garner public support when the message is changed to call for the preservation and/or introduction of “non-native” or “invasive” species.

Perhaps then it is time to retire the terms, “native” and “non-native.”  In “Who’s Invading What,” the author suggests that the non-native/native dichotomy may eventually give way to “dominant”/“non-dominant” species.  The spread of a dominant species may promote a decline in species diversity (Larson 2007).  Whether the dominant species is “native” or “non-native” would seem to be of little importance (Houlahan and Findlay 2004; White 2006; Meiners 2007).  More important is the reduction in ecological functioning and the diminished landscape diversity.

The New Message

So, the message should change.  But what should it become?  Perhaps something like this: Although there are legitimate reasons to eradicate some non-natives, restoring a native habitat to its natural state should not top the list.  Restoring a habitat to its natural state is a largely unattainable goal – a financial “luxury” affordable by only a handful of communities.  For the rest, restoration efforts should be designed to restore merely some of the habitat’s original functional attributes.  This could be watershed preservation, providing habitat for natives, and economic recovery or return (Ewel and Putz 2004).  The use of non-natives can play an integral part in these efforts.  But even partial restoration efforts are not inexpensive (Mitsch and Gosselink 2000).  Non-natives are often the most cost-effective option (D’Antonio and Meyerson 2002).  Reducing the restoration price tag may engender social acceptance.

The new message should inform the public about the unavoidable development of “novel” ecosystems which are normal responses to environmental changes and disturbances.  Alterations in climate change and land use affect species distributions and the environment.  These alterations modify the composition and/or function of ecosystems.  If you think about it, all ecosystems were novel at some point in time (Root 2006 and Harris 2006).

The new message should also consider the cultural uses and socio-economic value of non-native species.  Restoration ecologists should be mindful of the cultural and political sensitivities of local communities.  The success or failure of any particular restoration project can easily turn on social acceptance or rejection.  The public’s support may be a prerequisite to obtaining the funds, labor, and regulatory approval necessary to complete the project.  Resources should be carefully allocated to conservation efforts that yield more desirable results.

The new message should be broad enough to encompass ongoing as well as future practices.  New research, co-evolutionary responses, and environmental resilience should be considered.

Now is the Time

It is time to modify efforts to restore native habitats to their “natural” state.  Long-term adaptive management plans must include appropriate non-natives to promote the efficient use of resources. Most habitats are now novel and dependent on non-native species.  There will continue to be a subgroup of non-native species that cause environmental, economic, and social damage.  However, other non-natives will adapt and contribute to evolving ecosystems (Schlaepfer 2011).  Messaging is key to obtaining critical public support.  Evolving science and conservation practices may require future changes to the messaging.  Today’s message must be flexible enough to accommodate these future changes.  Scientific credibility and community support depend on a coherent message.  We must always look forward while working to preserve the past.

 

References

Carroll, S. P., J. E. Loye, H. Dingle, M. Mathieson, T. R. Famula, and M. Zalucki. 2005. And the beak shall inherit—Evolution in response to invasion. Ecology Letters 8:944–951.

Carroll, Scott. 2011. Conciliation biology: the eco-evolutionary management of permanently invaded biotic systems. Evolutionary Applications pg. 186-199.

D’Antonio, C.M. and Meyerson, L.A. 2002. Exotic plant species as problems and solutions in ecological restoration: a synthesis. Restoration Ecology 10: 703–13.

Dick, Christopher W. 2001. Genetic rescue of remnant tropical trees by an alien pollinator.  The Royal Society. Pg. 2391-2396.

Ewel, J.J., Putz Francis, E. 2004. A place for alien species in ecosystem restoration. Front Ecol Environ 2(7): 354-360.

Griffiths, C. J., and S. Harris. 2010. Prevention of secondary extinctions through taxon substitution. Conservation Biology 24:645–646.

Hansen, D., 2010 On the use of taxon substitutes in rewilding projects on Islands.  Island and Evolution. Perex-Mellando, V and Ramon, C (eds) Institut Menorquid’Estudis.  Recerca 19: 111-146.

Hobbs, R.J. et al. (2006) Novel ecosystems: Theoretical and management aspects of the new ecological world order. Global Ecol. Biogeog. 15, 1–7

Houlahan, J. E. and Findlay, C. S. 2004. Effect of invasive plant species on temperate wetland plant diversity. Conserv. Biol. 18:1132–1138.

Larson, B. Dec. 2007, Who’s invading what?  Systems thinking about invasive species. Canadian Journal of Plant Science. Pg. 993-999.

Maguire, L. A. 2004. What can decision analysis do for invasive species management? Risk Anal. 24: pg. 859–868.

Meiners, S. J. 2007. Native and exotic plant species exhibit similar population dynamics during succession. Ecology 88: 1098–1104.

Meyerson, L.A. and Mooney, H.A. (2007) Invasive alien species in an era of globalization. Front. Ecol. Environ. 5, 199–208.

Mitsch, W.J. and Gosselink, J.G. 2000. Wetlands, 3rd Ed. NY: John Wiley & Sons.

Olden, J. D., N. LeRoy Poff, M. R. Douglas, M. E. Douglas, and K. D. Fausch. 2004. Ecological and evolutionary consequences of biotic homogenisation. Trends in Ecology & Evolution 19:18–24.

Pimentel, D., S. McNair, J. Janecka, J. Wightman, C. Simmonds, C. O’Connell, E. Wong, L. Russel, J. Zern, T. Aquino, and T. Tsomondo. 2001. “Economic and Environmental Threats of Alien Plant, Animal, and Microbe Invasions.” Agriculture, Ecosystems and Environment 84: 1–20.

Rayna, C. Bell, Amos Belmaker, Courtney S. Couch, Katherine M. Marchetto, Joseph L. Simonis, R. Quinn Thomas, and Jed P. Sparks. April 2013.  Effectiveness of Erythrina gall wasp biocontrol and implications for the recovery of threatened Wiliwili trees (Fabaceae: Erythrina sandwicensis) The Journal of the Torrey Botanical Society pg. 215-224.

Root, T. L. and Schneider, S. H. 2006.  Conservation and climate change: the challenges ahead. Conserv. Biol. 20, 706–708.

Schlaepfer, M. A., P. W. Sherman, B. Blossey, and M. C. Runge. 2005. Introduced species as evolutionary traps. Ecology Letters 8:241–246.

Southwick, E. E., and L. Southwick. 1992. Estimating the economic value of honey bees as agricultural pollinators in the United States. Economic Entomology 85:621–633.

Suding, K. N., and R. J. Hobbs. 2009. Threshold models in restoration and conservation: a developing framework. Trends in Ecology and Evolution 24:271–279.

Tate, J. A., Z. Ni, A.-C. Scheen, J. Koh, C. A. Gilbert, D. Lefkowitz, Z. J. Chen, P. S. Soltis, and D. E. Soltis. 2006. Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics 173:1599–1611.

Walker, B. and Salt, D. 2006. Resilience thinking: Sustaining ecosystems and people in a changing world. Island Press, Washington, DC. 192 pp.

Weber, J. R. and Word, C. S. 2001. The communication process as evaluative context: What do nonscientists hear when scientists speak? BioScience 51: 487–495.

White, P. S. 2006. Disturbance, the flux of nature, and environmental ethics at the multipatch scale. Pages 176–198 in D. M. Lodge and C .Hamlin, eds. Religion and the new ecology: Environmental responsibility in a world in flux. University of Notre Dame Press, Notre Dame, IN.

 

 

10313386_10154153204430492_108213344555422454_nPaul G. Roman is currently enroled in the Masters of Conservation Biology programme.  This unique programme is offered jointly by Victoria University of Wellington, located in New Zealand’s capital city, and The University of New South Wales in Sydney, Australia.  Mr. Roman graduated with a Bachelor of Science in Biology from the University of Hawaii in 2010.  After graduation, he worked in conservation in Hawaii for 3 years as a field technician for both the Ko’olau Mountains Watershed Partnership and the Wai’anae Mountains Watershed Partnership.

 


Augmentative Biocontrol: Is it the perfect solution for pest control? –Julia Murphy

Biological invasions are happening everywhere. As a main part of global environmental change, they have become a leading cause of the worldwide decline in biodiversity (Mack et al 2000). With such far-reaching ecological effects a lot of effort has been put into finding efficient ways to manage these species. Obviously, the best way to deal with invasive species is to prevent them from invading in the first place (Mack et al 2000). This is, however, not always possible. After establishment, most methods of control are expensive, labor intensive and can have unintended costs. Additionally, for marine environments, where invasions can be much more complex, most of the common methods of prevention and control are not feasible (Atalah et al. 2013a).

As an alternative to the labor-intensive and terrestrial-centric methods, biocontrol has become a popular option. The release of a biological agent, which could be anything from a pathogen to a plant, can be an easier alternative to methods like manual removals or continuous trappings. Howeverthere are many downsides to biocontrol and non-target effects are often associated with these introductions (Thomas & Willis 1998). There is always a danger when introducing a species that they will in turn become a pestand doubly so if it is an exotic species, as is often the case in classic biocontrol (Louda et al. 2003; King & Moody 1982). Avoiding these non-target effects has therefore become a focus for biocontrol efforts. A leading option for this is augmentative biocontrol. Itconsists of bolstering a population that already exists so it can naturally fight off the invaders (Van Lenteren 2012). This would mean significantly decreasing the risk of non-target effects while getting the same amount of control as classical biocontrol.

Sounds perfect, right? Like the panacea for the negative sides of biocontrol?

…Well that’s not quite the case.

A large-scale literature review done by Collier & Van Steenwyk (2004) showed that almost half the time augmentative biocontrol was studied it failed to meet the desired outcome. These failures were based on a multitude of variables including predation, badly chosen environments, and cannibalism within the released species. Additionally, there were times that native populations will almost always be outcompeted just due to ecological circumstances.

Of course this is not to say that augmentative biocontrol is never effective. There are cases where this process can be ecologically and economically the right choice (Atalah & Forrest 2013; van Lenteren 2000; van Lenteren 2012). It has been pointed out that the Collier & Van Steenwyk (2004) review was heavily based on examples in the USA, rather than giving a full view of augmentation applications (van Lenteren 2006).   This means that the 50% failure rate is skewed towards a country where augmentative biocontrol is seldom the right choice.  In other parts of the world the success rate may be much higher.

Additionally the Collier & van Steenwyk (2004) study is in some part based on poorly selected applications.  Usage of augmentative biocontrol on pests which aren’t appropriate for this type of control would skew the results as well.  If the review was based on only properly selected applications the success or failure rates may have been extremely different.  Below are two such situations where the application of augmentative biocontrol has been demonstrated to have the capacity to control pest species while decreasing non-target effects.

Case 1: Agricultural Pests

Biocontrol has been used heavily for agricultural pests due to its reputation as a safer alternative to chemical herbicides and pesticides (van Lenteren et al. 2003). With agricultural profits being based on the health of the crop species, it seems obvious that non-target effects could have large costs associated with them. Therefore it is necessary to find a way to control pest species without endangering the crop and the insect species needed for successful harvests.

Augmentative biocontrol has been applied to both insect and plant pest species in the agricultural world. Squirting cucumber, a common agricultural plant pest in the Mediterranean Basin, was the focus of one of these studies. The insect Aspongopus viduatus F. was used in an inundative release to define its ability to control the pests. The tests were successful in showing that squirting cucumber was the preferred host of these insects and would therefore be very unlikely to affect similar species used as crops. The prospects for mass rearing and further releases are therefore very good and will be used on a larger scale (Ben-Yakir et al 1996).

FIg 1: Lepidopteran pest on North American crop species. (Cordero et al. 2006)

FIg 1: Lepidopteran pest on North American crop species. (Cordero et al. 2006)

In North and South America, and several parts of Asia, Trichogramma spp, are currently being used successfully as control for Lepidopteran pest species, which damage everything from cereal crops to forests (Van Lenteren & Bueno 2003). These parasitic insects work as control by infecting the eggs of the Lepidopteran species through an inundative releases (Smith 1996). In Latin America specifically, this type of augmentative control is used widely as a cost effective control method used to avoid pesticides (Van Lenteren & Bueno 2003).

 

Case 2: Marine Invasions

Augmentative biocontrol has not been heavily researched in marine environments but it shows a great deal of promise.  Invasive seaweeds, kelps and algae have invaded coastal regions around the world and consistently efficient methods of eradication and control have not been found (Anderson 2007).  One of the main worldwide invaders is the Asian kelp Undaria pinnatifida.  It has been found out of its native range in North and South America, Europe, Australia, and New Zealand (Atalah et al. 2013a; Casas et al. 2008; Thornber et al. 2004).  Control of this species is a large concern and the focus of worldwide research.  In one of those studies, augmentative biocontrol has been used in conjunction with other methods as a control of Undaria in New Zealand.  A large group of sea urchins, Evechinus chloroticus, were transplanted into Breaksea Sound, Fiordland on the South Island.  These sea urchins have been found to successfully control Undaria with little to no non-target effects (Atalah et al. 2013a).

Fig 2: Translocation of sea urchins to control Undaria in the Breaksea Sound, Fjordland, New Zealand (Biswell 2014)

Fig 2: Translocation of sea urchins to control Undaria in the Breaksea Sound, Fiordland, New Zealand (Biswell 2014)

Similar types of augmentative biocontrol have also been applied to biofouling of marine structures.  Biofouling communities, often found in ports and similarly developed areas, can be composed of many translocated exotic species brought by marine vessels.  In these cases natural grazer populations can often not be sustained due to other environmental factors. Due to this fact, augmentative biocontrol has been focused on competitors to exotic pest species (Atalah et al. 2013b).   Again New Zealand is leading the way for research into the areas.  On the South Island of New Zealand, the population of the sea anemone Anthothoe albocincta was increased through translocations in the Marlborough Sounds.  The presence of these sea anemones was found to decrease the amount of problematic pest fouling species (Atalah et al. 2013b).  It seems likely that similar augmentative methods, with only a small bit of alteration, could be applied to other marine pests.

Fig 3: Asian green mussel (left) and Biofouling of marine structures in a port in Australia (right) (Polgaze 2009; Gazinski 2009)

Fig 3: Asian green mussel (left) and biofouling of a marine structure in a port in Australia (right) (Polgaze 2009; Gazinski 2009)

 

So where does augmentative biocontrol stand now?

Even with its limitations, augmentative biocontrol has been successful in the cases discussed above.  Additionally it shows promise in other ecosystems like the Australian arid zone where dingoes are being studied as a possible form of feral cat control (Fleming et al. 2012).  The methods are, however, applied in a frustratingly small percentage of the world (van Lenteren 2012).  This could be due a variety of reasons including a lack of research and perhaps just the fact that many managers are unaware of the idea itself.  Or maybe the name “augmentative biocontrol” itself just scared people off the idea. It sounds so overly complicated without really giving you an idea of what it is. Something simpler like augbio or even just augmentation could change things.

As for the limitations found through past research, they are ones that can, in many cases, be controlled for with careful research and site selection. Just like any other form of pest control, You have to identify what species are the best candidates to be controlled. You have to pay careful attention to whether what you’re doing is actually the right thing for what you are trying to control.

Though the uses of augmentative biocontrol are not all encompassing, there is no reason wider applications should not be conducted.  There are specific instances where augmentative biocontrol can be extremely effective and these instances are found on a global scale. Success could be seen anywhere that native populations could control an invader at higher numbers or in marine environments where most other control methods for invasive species are not possible.  With proper research and well-designed releases augmentative biocontrol could decrease non-target effects of invasive species management worldwide.  The success or failure of augmentative biocontrol is entirely up to those people implementing it.

 

 

References

Atalah J, Bennett H, Hopkins G A &. Forrest B M. (2013) Evaluation of the sea anemone Anthothoe albocincta as an augmentative biocontrol agent for biofouling on artificial structures. Biofouling: The Journal of Bioadhesion and Biofilm Research, 29:5, 559-571, DOI: 10.1080/08927014.2013.789503

Atalah J, Hopkins GA, Forrest BM (2013) Augmentative Biocontrol in Natural Marine Habitats: Persistence, Spread and Non-Target Effects of the Sea Urchin Evechinus chloroticus. PLoS ONE. 8(11): e80365. doi:10.1371/journal.pone.0080365

Ben-Yakir D, Gal D. Chen M,  & Rose D. (1996). Potential of Aspongopus viduatus F. (Heteroptera: Pentatomidae) as a Biocontrol Agent for Squirting Cucumber, Ecballium elaterium (L.) A. Rich. (Cucurbitaceae). Biological Control. 7, 48–52

Biswell, S. (2014). Fighting the Sea Invaders. Retrieved from <http://www.stuff.co.nz/nelson-mail/features/primary-focus/9654073/Fighting-the-sea-invaders>

Casas GN, Piriz ML, & Parodi EL (2008) Population features of the invasive kelp Undaria pinnatifida (Phaeophyceae:Laminariales) in Nuevo Gulf (Patagonia, Argentina). J Mar Biol Assoc UK. 88(1):21–28.

Collier, T., & Van Steenwyk, R. (2004). A critical evaluation of augmentative biological control. Biological Control31(2), 245-256.

Cordero, R. J., Kuhar, T. P., Speese, J., III, Youngman, R. R., Lewis, E. E., Bloomquist, J. R., Kok, L. T., and Bratsch, A. D. (2006). Field efficacy of insecticides for control of Lepidopteran pests on collards in Virginia. Online. Plant Health Progress doi:10.1094/PHP-2006-0105-01-RS.<http://www.plantmanagementnetwork.org/pub/php/research/2006/collard/>

Elliott N, Kieckhefer R and Kauffman W (1996) Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia 105, 537–544

Fleming, P. J., Allen, B. L., & Ballard, G. A. (2012). Seven considerations about dingoes as biodiversity engineers: the socioecological niches of dogs in Australia. Australian Mammalogy34(1), 119-131.

Gazinski, C. (2009). National Biofouling Management Guidance for the Petroleum Production and Exploration Industry.  Commonwealth of Australia. Retrieved from
< http://www.drillingcontractor.org/biofouling-is-tip-of-green-iceberg-1995>

King, C. M., & Moody, J. E. (1982). The biology of the stoat (Mustela erminea) in the National Parks of New Zealand I. General introduction. New Zealand journal of zoology9(1), 49-55.

Mack, R. N., Simberloff, D., Mark Lonsdale, W., Evans, H., Clout, M., & Bazzaz, F. A. (2000). Biotic invasions: causes, epidemiology, global consequences, and control. Ecological applications10(3), 689-710.

Nicot, P. C. (Ed.). (2011). Classical and augmentative biological control against diseases and pests: critical status analysis and review of factors influencing their success. IOBC/WPRS.

Phillips, B. L., Brown, G. P., & Shine, R. (2003). Assessing the potential impact of cane toads on Australian snakes. Conservation Biology17(6), 1738-1747.

Polglaze, J. (2009) National Biofouling Management Guidance for the Petroleum Production and Exploration Industry.  Commonwealth of Australia. Retrieved from
< http://www.drillingcontractor.org/biofouling-is-tip-of-green-iceberg-1995>

Thomas, M. B., & Willis, A. J. (1998). Biocontrol—risky but necessary?.Trends in ecology & evolution13(8), 325-329.

Van Lenteren, J.C. (2000). Measures of success in biological control of arthropods by augmentation of natural enemies. In: G. Gurr and S. Wratten (eds), Measures of Success in Biological Control. Kluwer Academic Publishers, Dordrecht. pp. 77–103.

Van Lenteren, J.C. (2006). How not to evaluate augmentative biological control. Biological Control 39. 115–118

Van Lenteren, J. C. (2012). The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl,57(1), 1-20.

Van Lenteren, J. C., & Bueno, V. H. (2003). Augmentative biological control of arthropods in Latin America. BioControl48(2), 123-139.