Progress on entomopathogenic nematology research: A bibliometric study of the last three decades: 1980–2010

Biological Control 66 (2013) 102–124

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Review

Progress on entomopathogenic nematology research: A bibliometric study of the last three decades: 1980–2010 Ernesto San-Blas Laboratorio de Protección Vegetal, Centro de Estudios Botánicos y Agroforestales, Instituto Venezolano de Investigaciones Científicas, Av.8 con Calle 79, Maracaibo C.P. 4001, Venezuela

h i g h l i g h t s

g r a p h i c a l a b s t r a c t

 Studies on EPN increased from 24

papers per year in the 1980s to 91 in the 2000s.  Biogeography studies have grown, revealing the presence of EPN in 36 countries.  Coauthorship networking has doubled from 9% in the 1980s to 20% in the 2000s.  In the 1980s, 72 journals published papers about EPN, and 210 did it in 2010.

a r t i c l e

i n f o

Article history: Received 15 February 2013 Accepted 21 April 2013 Available online 30 April 2013 Keywords: Steinernema Heterorhabditis Publication Scientiometrics Coauthorship networking Database

a b s t r a c t Entomopathogenic nematodes have achieved a place in biological control programmes because of their effectiveness, speed of action, innocuousness to non-insect targets and simplicity of mass production. However many challenges derived to the lack of knowledge in some critical steps from laboratories to their use in the fields, have to be resolved in order to improve their performance and to reduce the mass production costs. For those reasons, studies on entomopathogenic nematology have increased considerably in the last few decades. Also, there have been important changes in the ways that results are published; many of them relate to major transformations in scientific trends. Using bibliometric tools we characterize variations in number, types of journal, countries of origin, research topics and the number of participating countries, of 1923 papers (from 1980 to 2010) reported in several on-line editorial databases. Ó 2013 Elsevier Inc. All rights reserved.

1. Introduction Since the discovery of entomopathogenic nematodes (EPN) in 1923 by Steiner, there has been a tremendous amount of research on these organisms. This progression has been particularly evident since the 1980s, due to the potential in using EPN as biological control agents (Steiner, 1929), for which the axenic mass rearing technique developed by Glaser (1940) was central. Due to the economic, human health and environmental importance of substituting traditional chemical control methods by biological agents, EPN have gained recognition because of their effectiveness, time of response, innocuousness to mammals E-mail addresses: [email protected], [email protected] 1049-9644/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.biocontrol.2013.04.002

and their relative simplicity in mass production. Nevertheless, many aspects related with shelf life, long term persistence, and biological and ecological issues which can lead to improved integrated pest management programs are still to be solved and understood. For these reasons, many research groups around the globe have focused their efforts to comprehend the nature of these organisms, and have developed an enormous gamma of technological advances, from biological control and integrated control programs, to formulation and delivery systems in the field. Once molecular biology techniques were implemented, the number of described species of EPN grew from 13 (10 Steinernema and 3 Heterorhabditis) in the late 1980s (Kaya and Gaugler, 1993) to 63 Steinernema, 1 Neosteinernema and 12 Heterorhabditis by

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December 2012. Additionally, in a workshop in England (Hominick et al., 1997), procedures to standardize EPN taxonomy and species descriptions were established. Globalization has caused many countries (especially less developed) to start their own research on EPN. As a consequence, this process of integration has contributed to an improved understanding of the biogeography, diversity and biological control potential, particularly for the control of tropical pests (Kaya et al., 2006).

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2.2. Biological control Papers in this group were explicitly written from experimental results that had set parameters of controlling pests, including insects, ticks and plant parasitic nematodes. This area was divided into two subareas: (1) biological control experimentation in the laboratory, and (2) biological control experimentation in green houses or in the field. 2.3. Mixed technologies

2. Building the database A resulting database of 1923 published articles (from 1980 to 2010) was built using the following on-line editorial databases: Science Direct, Scopus, Springerlink, Ingenta, OVID, Wiley, Highwire, Jstore, Scielo, MetaPress, Cambridge journals and Oxford Journals’ and organized in a spreadsheet from Microsoft ExcelÒ software. Citations were checked for repetitions and deleted manually. Data were classified by the decade of publication, country of origin (according to the affiliation of the corresponding author), research topics and number of participating countries, and sorted according to several criteria as explained in the figures, to build new data subsets. In order to explore the research topics deeper, the collected data were reclassified as follows: 2.1. Behaviour This term was applied in a very broad sense and all publications referring to advances in the knowledge of the nature of EPN were congregated into this group. At the same time two sub-sets were created; (1) abiotic factors, which gathered all papers related with the response of nematodes to environmental factors such as temperature, pH, metal ions, soil texture, moisture, salinity, etc., and (2) biological and ecological factors which included all papers related with behaviour itself, biochemistry, sexual components, population dynamics, competition, etc.

Papers clustered in this group included those related with the use of EPN in the field, in combination with other elements in integrated management programs or delivery systems. This topic was separated into four groups: (1) chemical pesticides, including nematicides, insecticides, fungicides, etc., (2) other biological control agents such as entomopathogenic bacteria, fungi, viruses, parasitoids, vegetal extracts, etc., (3) irrigation and delivery systems, and 4) other additives which included fertilizers, UV protectants, surfactants, etc. 2.4. Mass production This group gathered all published papers related to any stage in mass production and included storage and transport. They were split into three groups: (1) culture media and parameters on mass production, (2) quality control and formulation, and (3) storage and transport of the formulated product. 2.5. Relationship with other organisms This theme clustered all papers devoted to the effect of different organisms, excluding other biological control agents, in the performance or behaviour of EPN. This area was also divided into (1) effect of EPN on nontarget organisms, (2) effect of bacteria (e.g. Pasteuria penetrans (Thorne) Sayre and Starr)) on EPN, (3) effect on the nematode complex (e.g. population dynamics of different nematode species when EPN were applied to the soil), (4) interac-

Fig. 1. Number of publications per year between 1980 and 2010. Data were grouped by decades and a variance analysis was performed using a generalized linear model approach (ANOVA) (P < 0.05); Different letters means significant differences by decades (means ± sd).

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Fig. 2. Global contribution per continent (and excl. USA) in published papers and the most representative countries per continent in the decade of the 1980s.

Fig. 3. Global contribution per continent (and excl. USA) in published papers and the most representative countries per continent in the decade of the 1990s.

tion with fungi (e.g. nematode trapping fungi), (5) on plants (e.g. effect of root exudates when the plant is under attack), and (6) effect of other organisms, such as predation of EPN by acari or collembolans, deterrent effect of infected cadavers on ants, etc. 2.6. Symbiotic interaction In this area only papers referring to both symbionts together (i.e. EPN and its bacteria) were considered, published works

studying aspects of the symbiotic bacteria alone were left out. All other research topics: biogeography, taxonomy, legal issues, and genetic techniques, were taken as such. Statitical analyses were performed using MinitabÒ software. Differences between the numbers of publications per decade were assessed through analysis of variance (Fig. 1). Figs. 2–4 and 6–12 were built merely by descriptive means. Correspondence analyses of journals versus research topics per decade (Fig. 13) were done. Two way contingence tables were built and the ‘‘response cells’’

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Fig. 4. Global contribution per continent (and excl. USA) in published papers and the most representative countries per continent in the decade of the 2000s.

Fig. 5. Global presence of entomopathogenic nematodes per decade.

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Fig. 6. International coauthorship networking in the decade of 1980s. (A) Percentage and number of published papers by single countries (SC) versus two or more countries (MultiC). (B) Percentage and number of papers published by two or more countries. (C) Percentage of participation per country in published papers when were written by two or more countries. (D) Countries with the most collaborative performance (represented by the number of partner countries).

Fig. 7. International coauthorship networking in the decade of 1980s. (A) Percentage and number of published papers by single countries (SC) versus two or more countries (MultiC). (B) Percentage and number of papers published by two or more countries. (C) Percentage of participation per country in published papers when were written by two or more countries. (D) Countries with the most collaborative performance (represented by the number of partner countries).

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Fig. 8. International coauthorship networking in the decade of 2000s. (A) Percentage and number of published papers by single countries (SC) versus two or more countries (MultiC). (B) Percentage and number of papers published by two or more countries. (C) Percentage of participation per country in published papers when were written by two or more countries. (D) Countries with the most collaborative performance (represented by the number of partner countries).

Fig. 9. Contribution of published papers (%) by field of knowledge in the 1980s. (A) Relative contribution per field of knowledge; RWO, relationship with other organisms (B) contribution of sub-areas inside fields of knowledge; behaviour: AF, effect of abiotic factors; BAE, biological and ecological factors. Biocontrol: Lab, laboratory experiments, GrFi, greenhouses and field experiments. Mass production: QF, quality control and formulation; ST, storage and transport; CMP, culture media and parameters on mass production. Mixed technologies: Pest, chemical pesticides; OBA, other biological control agents; IrrD, irrigation and delivery systems; FOA, fertilizers and other additives (adjuvants, protectants, vehicles, etc.). RWO (relationship with other organisms): NTO, non-target organisms; Nem, other nematodes; Bac, bacteria (no biocontrol agents); Fung, fungi (no biocontrol agents); Othe, other organisms.

were filled with the number of articles published in every research topic per journal. Data related to the 1980s, only considered journals with 5 or more publications for the analysis, and for the rest of the decades the data set was constructed using journals with 10 or more articles.

3. From a few lab collections to a global phenomenon Thirty years ago only a few research groups, mostly from developed countries, made efforts to understand EPN for biological control purposes. The vast majority of the world did very little EPN

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Fig. 10. Contribution of published papers (%) by field of knowledge in the 1990s. (A) Relative contribution per field of knowledge; RWO, relationship with other organisms (B) contribution of sub-areas inside fields of knowledge; Behaviour: AF, effect of abiotic factors, BAE, biological and ecological factors. Biocontrol: Lab, laboratory experiments; GrFi, greenhouses and field experiments. Mass production: QF, quality control and formulation; ST, storage and transport; CMP, culture media and parameters on mass production. Mixed technologies: Pest, chemical pesticides; OBA, other biological control agents; IrrD, irrigation and delivery systems; FOA, fertilizers and other additives (adjuvants, protectants, vehicles, etc.). RWO (Relationship with other organisms): NTO, non-target organisms; Nem, other nematodes; Bac, bacteria (no biocontrol agents); Fung, fungi (no biocontrol agents); Plant, plants; Othe, other organisms.

Fig. 11. Contribution of published papers (%) by field of knowledge in the 2000s. (A) Relative contribution per field of knowledge; RWO, relationship with other organisms (B) contribution of sub-areas inside fields of knowledge; Behaviour: AF, effect of abiotic factors; BAE, biological and ecological factors. Biocontrol: Lab, laboratory experiments; GrFi, greenhouses and field experiments. Mass production: QF, quality control and formulation; ST, storage and transport; CMP, culture media and parameters on mass production. Mixed technologies: Pest, chemical pesticides; OBA, other biological control agents; IrrD, irrigation and delivery systems; FOA, fertilizers and other additives (adjuvants, protectants, vehicles, etc.). RWO (relationship with other organisms): NTO, non-target organisms; Nem, other nematodes; Bac, bacteria (no biocontrol agents); Fung, fungi (no biocontrol agents); Othe, other organisms.

research, probably because of a lack of information, funding or both. Back in the 1980s, the negative consequences of agrochemicals were less rooted in the public opinion and the awareness of using biological control measurements or integrated pest management programmes was mainly as local initiatives. It was in the late 1980s and early 1990s when some countries formally started

legislation efforts and programmes to reduce the use of pesticides (European Commission, 1988; World Wide Fund for Nature, 1993; Gullino and Kuipjers, 1994). As a consequence of reports on the toxic effects of pesticides on human health, such as ‘‘Pesticides in the diets of infants and children’’ report (USA National Research Council, 1993), the Food Quality Protection Act was approved by

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Fig. 12. Total number of journals which published papers in entomopathogenic nematology and the relative participation of the 10 most important journals according with the number of papers published in (A) 1980s, (B) 1990s and (C) 2000s.

the US congress in 1996. Today, evidences point to a considerable interest in using and studying EPN; even countries with incipient activities on biocontrol strategies using these nematodes, no longer consider EPN as ‘‘lab curiosities’’, as Gaugler (2002) and Stock (2005) coined them. Research on EPN (measured by published papers) has grown significantly over the last 30 years (ANOVA F = 65.07, p < 0.0001, a = 0.05) with means of 24, 73 and 91 papers per year in the 1980s, 1990s and 2000s, respectively (Fig. 1). In the 1980s, work from 24 countries gave rise to 238 papers, published in 69 journals. Almost half the publications in that period (46.2%) came from USA (Fig. 2) and almost three quarters came from just five countries (USA, Australia, Canada, Czech Republic and UK). In the following decade, the number of published papers almost tripled (Fig. 3), to 732 articles published in 132 peer reviewed journals. In the 1990s, 39 countries participated in EPN research. USA again produced the vast majority (46%), however Europe increased its participation to 33% of the global total. The only drop-off occurred in Oceania where the number of published papers was basically the same as that in the 1980s. This situation represented a dramatic drop in relative participation from 11.3% to 3% by the 1990s, and to 1% by the 2000s, probably because some very prolific and pioneering EPN researchers, such as Robin Bedding, Ray

Akhurst and John Curran, are not involved in research activities any longer. The first 10 years of the new millennium witnessed a change in perspectives. Less developed and/or more middle income countries, e.g., Brazil, India, Egypt, Mexico, Israel and China, joined the club as big EPN knowledge poles and innovators. More than 1000 articles, originated in 50 countries, were published in 219 journals (Fig 4.). Europe published the majority of the papers between 2000 and 2010, with 39.2% but the USA still kept its position as the country with top production (35%). The participation of Asian, Latin American and African countries (around 25% of publications) demonstrated a surging of interest in studying these organisms and how promising EPN have now become to solving tropical and subtropical pest issues.

4. Are nematodes where nematologists are? Before 1980, just 7 EPN (6 Steinernema and 1 Heterorhabditis) had been recovered from Europe (Steiner, 1923; Filipjev, 1934; Bovien, 1937; Weiser, 1955; Artyukhovsky, 1967; Stanuszek, 1970; Poinar and Linhartdt, 1971; Mrácˇek, 1977), USA (Steiner, 1929; Glaser et al., 1940, 1941), Australia (Poinar, 1972) and New Zealand

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Fig. 13. Correspondence analysis of journals versus studied areas by decade.

(Wouts, 1979). However, due to the potential use of EPN as biological control agents, more laboratories across the world have engaged in research aimed to find their native isolates, with the result that many places in the planet have been sampled, even Antarctic soils (Griffin et al., 1990). Generally, those involved in EPN studies have focused their interest on all aspects related to the EPN, and at the beginning, it was usual to read articles on different topics, such as storage, mass production or phylogeny, written by the same authors. The same pattern can be seen in biogeographical articles, at the beginning, the vast majority came from countries where those research groups resided (5.6% in the 1980s (Fig. 5)). However nowadays, nematologists from the more developed countries have been involved in EPN biogeographical work in less developed countries. In the decade of 1980s papers published on EPN biogeography were limited to Australia and New Zealand through the work of Akhurst and Bedding (1986), Europe (UK, Northern Ireland) with Hominick and Briscoe (1990a,b), and Blackshaw (1988), China by Liu and Zhang (1982), Wang and Li (1987), Japan by Kushida et al. (1987), Mamiya (1988), and in the Americas, USA Akhurst and Brooks (1984), Brazil Pizano et al. (1985), Fowler (1988), Puerto Rico Roman and Beavers (1983) and Argentina Agüera de Ducet (1986).

Once the studies on EPN were popularized and more laboratories joined the research (especially across Europe), biogeography studies were more frequent and more organized sampling programmes and reports appeared. The mentioned studies revealed the presence of EPN species in 36 countries (19 European, 9 Asian, 7 the Americas continent and 1 African). In that period, some of the more established groups of nematologists, such as Homminick and Briscoe (UK), Kaya and Stock (USA), Griffin, Moore and Downes (Ireland), Reid (Scotland), and Moens (Belgium) were involved with surveys of different latitudes in their own countries. Despite the significant amount of biogeography knowledge gathered from 1980 to 2000, 60.5% of that information was collected between 2001 and 2010. On the other hand, many articles were restricted to more detailed sampling processes in previously searched countries, e.g., work by Mrácˇek et al. (2005) and Salame et al. (2010) in the Czech Republic and Israel, respectively; an important group of publications in new countries, especially from tropical areas, produced 18% of the total knowledge between 2000 and 2010. The participation of well-established research groups from developed countries, such as the Nguyen’s group at the University of Florida, USA, Stock’s at the University of Arizona, USA, Griffin’s at the University of Maynooth, Ireland and Moens’ at the University of Gent, Belgium, in projects which involved sampling in less

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developed countries has been pivotal for the progress of EPN studies in countries from Latin America, Africa and Asia. Currently, many countries in Latin America and Asia have been, or are in the process of being, sampled (Fig. 5). Many African countries however, remain neglected with respect to both EPN sampling and projects to incorporate EPN into biological control programmes. The increasing interest of tropical and subtropical countries in developing their own biocontrol solutions using EPN will surely produce new information on the biogeography of EPN and the discovery of new species and/or strains.

5. International coauthorship networks In the past, the sole authorship of scientific articles was the rule and groups of collaborators from different nationalities were scarce, however, nowadays it is increasingly frequent to find papers signed by scientists from two or more countries; working in coauthorship networks have become highly productive over the years. From the 1990s onwards, many authors indicated the potential of using coauthorship data to perform reliable statistics and modelling; this procedure was possible around 2000 due to the creation of online bibliometric databases (Newman, 2004). International coauthorship networks have increased in all science fields over the past 35 years (Glänzel and Schubert, 2004), and entomopathogenic nematology has not been an exception. Apart from the reasons behind the formation of such working groups (which are not discussed in this paper), international collaboration has enhanced the productivity of those consolidated authorities and laboratories. International coauthorship networks have also allowed lesser known specialists from underdeveloped countries, an opportunity to publish in high impact journals, and to increase visibility within the scientific community. The field of EPN has followed the same pattern of the global coauthorship networking and doubled its relative numbers from less than 10% (with 23 published papers) in the 1980s to more than 20% (207 published papers) in the 2000s (Figs. 6a–8a). According to the gathered data, in the 1980s more that 90% of the collaborative papers (in terms of different countries) were written by people from just two different countries (Fig. 6b). However, those numbers have been decreasing from 82.7% in the 1990s (Fig. 7b) to 78.5% in the 2000s (Fig. 8b). This reduction means that multiple country consortia have increased over the years, and more laboratories around the world have joined efforts to study and research EPN. In fact, another way to look at this is by observing the increasing number of participant countries in those networks between 1980 and 2010, from 20 in the 1980s, to 58 in the last decade (Figs. 6–8). One of the most prominent consortiums in the field was that of Hominick et al. (1997) who, in 1997, published a paper with 14 entomopathogenic nematologists from 10 different countries, in which they set the basis of biosystematic and taxonomic protocols for describing new EPN species; also, the Kaya et al. (2006) review grouped together 14 scientists from 11 countries to evaluate the status of EPN and their symbiotic bacteria around the world. The international cooperativeness of each country can be measured according to the percentage of participation of a given country in a given period of time (Figs. 6c–8c) and the number of partners (different countries) which a given country has worked with (Fig. 6d). Although the values of the international cooperativeness have changed during the last three decades, countries like USA and UK have always been at the top of the list as cooperative countries. Historically, between 40% and 50% of the cooperative papers had the participation of USA scientists; they have also participated in projects with more countries than any other (Figs. 6d–8d).

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The beneficial effect of the international coauthorship networks on underdeveloped/developing countries was evident in Argentina, Cuba and Mexico in the 1980s, where papers published with other partners represented 33% (Poinar et al., 1988), 100% (Mrácek et al., 1984) and 100% (Gaugler et al., 1983; Alatorre-Rosas and Kaya, 1990) of their total peer reviewed production. Additionally, India in the 1990s and Turkey in 2000s took advantage of the international coauthorship networks to produce 40% (Poinar et al., 1992; Ehlers et al., 2000; Koppenhöfer et al., 2000a; Stack et al., 2000) and 46% of their total article production, respectively (Susurluk et al., 2001; Hazir et al., 2003; Kaya et al., 2006; Unlu et al., 2007). 6. Moving through disciplines The value of EPN as biopesticides is unquestionable. Nevertheless, the path from discovery to mass production and later field applications, has not been straightforward, and many aspects (basic and applied) have been neglected or remain unknown (Lewis et al., 2006); a problem that limits the development of biological control techniques, and is detrimental to commercial success, as evidenced by numerous attempts to control insect pests with EPN (McCoy et al., 2002; Shapiro-Ilan et al., 2002b; Georgis et al., 2006). Recent awareness of these limitations has led the EPN community to approach research towards the understanding of EPN as a whole and not only as biological control agents per se. As an example, the proportion of publications related to behaviour and the effect of biotic and abiotic factors have increased in the last two decades (Figs. 9a–11a), leading to a greater understanding of EPN biology and ecology, and therefore, to a more efficient use of such parameters to predict or improve their performance as biological control agents in the field. 6.1. Behaviour Probably, the most comprehensive compendium of knowledge about EPN is that related with the effect of different soil parameters (type, texture, pH, salinity, etc.) on the behaviour (effectiveness, movement, orientation, virulence, persistence, etc.) of infective juveniles (IJ). The category of ‘behaviour’ represents more than a quarter of the total publications on EPN, 24.9% in the 1980s, 35% in the 1990s and 26.8% in the 2000s (Figs. 9a–11a). 6.1.1. Abiotic factors Studies of the aforementioned parameters and other abiotic factors were heavily studied in the 1980s, representing 37.9% (Fig. 9b) of publications within ‘behaviour’. Some works unveiled information of great interest for experimental design, teaching processes and EPN application in the field. Some of these works have in turn become ‘‘classical’’, because of the impact the information had. Amongst them, Gaugler et al. (1980) described the orientation of EPN to carbon dioxide; Burman and Pye (1980, 1981) tested the movement of Steinernema carpocapsae Weiser in thermal, chemical and bacterial gradients; the dispersal patterns, persistence and host infection of EPN were determined in different substrates (Moyle and Kaya, 1981) and soils (Poinar and Hom, 1986; Schroeder and Beavers, 1987), under various moisture levels (Gray and Johnson, 1983), pH (Fischer and Führer, 1990; Kung et al., 1990), textures (Georgis and Poinar, 1983a), temperature (Molyneux, 1985; Blackshaw and Newell, 1989) and depths (Georgis and Poinar, 1983b; Nguyen and Smart, 1990). In the following decade, publications related to abiotic factors and their effects on EPN dropped to 29.6% in the ‘behaviour’ category, but many advances were accomplished (Fig. 10b). More information was produced on the relationship between EPN and soil characteristics, whilst new approaches focused on extreme

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conditions to improve biological control programmes for use on the aerial parts of the plants, and in soils with particular conditions. As a consequence, publications appeared on the effects of UV light (Gaugler et al., 1992; Fujiie and Yokoyama, 1998), gamma irradiation (Salam et al., 1995), metal ions (Jaworska et al., 1996, 1997; Jaworska and Tomasik, 1999), low temperatures (Griffin and Downes, 1991; Wharton and Surrey, 1994), heat tolerance (Selvan et al., 1996), seawater (Griffin et al., 1994; Finnegan et al., 1999), soil salinity (Thurston et al., 1994) and desiccation (Surrey and Wharton, 1995; Koppenhöfer et al., 1997; Patel et al., 1997a,b) on EPN. Nematode regulation mechanisms for adaptation to extreme conditions were investigated in the 2000s, and the functions of some cellular molecules were elucidated. Advances in this field were related to studies on the expression of different genes for EPN tolerance to environmental stress (Gal et al., 2001; Chen and Glazer, 2005). For example, the role of trehalose (a disaccharide) as one of the most important factors for both low and high temperature resistance was determined (Grewal and Jagdale, 2002; Jagdale and Grewal, 2003; Jagdale et al., 2005); additionally, works were done to prove not only the role of glycogen synthase genes in the desiccation survival of EPN through the degradation of glycogen and further transformation into a substrate for trehalose, but also that in the reverse rehydration process, trehalose is converted into glucose, as a substrate for glycogen synthesis (Gal et al., 2001). 6.1.2. Biological and ecological factors Since the discovery of EPN and their subsequent postulation as biological control agents, many researchers have tried to understand the biology of these organisms. The knowledge that has been generated has helped us to better understand a range of EPN topics, such as behaviour in the field, mass production, persistence, etc. and has identified some of the mechanisms by which EPN behave in a given way. More than two thirds of publications on behaviour are related to biology (e.g. sexual behaviour, developmental, life cycles, biochemical composition, penetration routes, etc.) and ecology (e.g. relationship between different species, parameters of infections, interaction with plant roots, etc.) (Figs. 9b–11b). Many fundamental aspects of EPN biology were described in the 1980s; their life cycles were evaluated, including details such as embryogenesis in Steinernema sp. (Madikhanov, 1982) and spermatogenesis in Heterorhabditis sp. (Poinar, 1985). The IJ stage is a developmentally arrested form of J3 larvae (Poinar and Leutenegger, 1968) and Popiel et al. (1989) postulated the responsibility of different environmental factors (food depletion, population density, etc.) in the induction of this arrested stage. The penetration of Heterorhabditis sp. through the insect cuticle by means of a toothlike external plaque was a discovery with relevant implications in choosing EPN for biological control programmes (Bedding and Molyneux, 1982). Additionally, some mechanisms for host location were studied and extended in the 1990s. Byers and Poinar (1982) proposed a two way theory in which stimuli could be effective for ‘‘short range’’ attraction, such as thermal gradients (Burman and Pye, 1980) or ‘‘long range’’ attraction, like CO2 (Gaugler et al., 1980) and chemicals (Pye and Burman, 1981) released by potential hosts. Due to the fact that the meristematic area of the root tips attracted EPN (Bird and Bird, 1986); Choo et al. (1989) investigated the relationship between host location and presence of plant roots in the soil. Research on the defence mechanisms of insects and their immune responses to infecting EPN started in the 70’s, but many of the observations were qualitative or inexact. Later on, Matha and Mráceˇk (1984) and Dunphy and Webster (1985) measured the increase of haemocytes in the host haemolimph after infection, whilst Götz et al. (1981) analysed the destruction of antibacterial

proteins from Hyalophora cecropia Linnaeus, and Dunphy and Webster (1987) determined the protective role of the lipoidal nature of the EPN epicuticule against the insect immune system. Between 1991 and 2000, very important biological and ecological characteristics were described. Studies on the movement of EPN due to host-associated cues were numerous, and produced some well-known papers in which differences in nematode movements to contact cues, e.g. gut content, faeces, insect cuticles, were spotted (Lewis et al., 1992; Grewal et al., 1993), and ‘‘ambusher’’ or ‘‘cruiser’’ strategies for host finding were proposed (Lewis et al., 1992, 1993). The discussion about which sex of the EPN was the colonizer was very intense in the 1990s. Males acting as the infecting agent in insects were proposed for the first time by Grewal et al. (1993), a hypothesis that was refuted by Bohan and Hominick (1997) and Stuart et al. (1998), who found no differences between sexual specimens in the colonization process, measured by time of exposure. However, the dynamics of invasion related to sexual components interconnected with many factors like nematode species (Lewis and Gaugler, 1994), nature of host, environmental factors (Bohan and Hominick, 1997), early or late emerging time (Fujimoto et al., 2007) and dispersal behaviour (Alsaiyah et al., 2009). The biochemical composition of EPN was also well studied in the 1990s. Some partial studies on the epicuticle of EPN were done in the 1980s (Dunphy and Webster, 1987). The composition and functionability of the nematode cuticle were revised by Sharon and Spiegel (1996), basically to understand the protective purpose to environmental stressors (Fodor et al., 1994) and the role of its components to evade the immune system of the host (Wang and Gaugler, 1999). Many works were also published concerning the energy reserves of lipids and glycogen (Selvan et al., 1993; Patel and Wright, 1997a,b,c; Wright et al., 1993) as decisive factors on long survival strategies (Qiu and Bedding, 2000), thermal tolerance (Abu Hatab and Gaugler 1997; Jagdale and Gordon, 1997) and infectivity (Patel et al., 1997b) of IJ when searching for a new host. How can the IJ survive for long periods of time in natural environments? This is one of the most important questions, yet for some time it received little attention in entomopathogenic nematology (Preisser et al., 2005). It was really in the last decade that works have been published on the subject. Genetic variability of the EPN populations (Grewal et al., 2002; Somasekhar et al., 2002a,b), recycling of EPN in their insect host (Loya and Hower, 2002; Nielsen and Philipsen, 2004 to mention but a few), the host cadaver as a protectant environment for IJ (Lewis and Shapiro-Ilan, 2002; Pérez et al., 2003; Pu˚zˇa and Mrácˇek, 2007), scavenging (San-Blas and Gowen; 2008), lipid composition (Hass et al., 2002), behavioural plasticity (Cohen et al., 2002), metapopulation dynamics (Ram et al., 2008) and adaptation processes to environment factors (mentioned previously) are now included in the network of behavioural responses for long time survival of EPN. Proteomic studies and gene expression mechanisms of proteins for different cellular processes of EPN have been on the increase since 2001. Results on this field include host invasion (Toubarro et al., 2010) or parasitic processes (Brivio et al., 2006; Bai and Grewal, 2007; Jing et al., 2010; Hao et al., 2010), insect immune suppression through proteases secreted by the nematodes (Balasubramanian et al., 2010), either for prophenoloxidase suppression activity (Balasubramanian et al., 2009) or by inducing apoptosis in the pathogenesis progression (Toubarro et al., 2009), as well as the genetic expression of EPN under desiccation (Chen et al., 2009; Tyson et al., 2007; Somvanshi et al., 2008). Additionally, cDNA libraries were built for Heterorhabditis (Adhikari et al., 2009) and Steinernema (Hao et al., 2010), and predictions of genes encoding proteins or gene ontology which could participate in many aspects of the EPN life cycle (from the host invasion to environmental responses) were calculated.

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6.2. Biological control In the 1980s, papers linked with biological control and application methods (mixed technologies), (Fig. 9a) were almost half of the total publications (47.6%); whereas in the 1990s and 2000s the percentage of publications representing these themes was reduced to 36.3% and 39%, respectively. However the number of papers increased per decade (117, 203 and 250) because the relative participation of other areas like biogeography, symbiotic interaction and/or mass production rose significantly. Examining the biological control publications involving EPN provides an indication of how biopesticides have evolved. At first, researchers conducted their experiments in laboratories but gradually moved to greenhouses and field experiments as the 1980s moved into the 1990s and the 2000s. In the 1980s, 64.5% of publications originated from a number of groups around the world, were conducted as laboratory trials; this number was reduced to less than half (47.5%) in the 2000s. The number of papers publishing field trials increased from 22 in the1980s to 94 (52.5% of the category) in the 2000s (Figs. 9b–11b). Two good examples of the evolutionary pathway of biopesticide development since the 1980s are the development of complete technical packages in use around the globe to control Otiorhynchus sulcatus Fabricius, a pest in cranberries and strawberries (e.g., Bedding and Miller, 1981; Georgis and Poinar, 1984; Klingler, 1988; Kakouli-Duarte et al., 1993, 1997; Lola-Luz and Downes, 2007; Ansari et al., 2010; Ansari and Butt, 2011) and Diaprepes abreviatus Linnaeus in citrus orchards (e.g., Román and Beavers, 1983; Figueroa and Román, 1990; Schroeder, 1990a,b; Duncan et al., 1996; Shapiro-Ilan and McCoy, 2000a,b,c; Stuart et al., 2008; Ali et al., 2010). Other interesting uses of EPN to control pests include their use against ticks (Samish and Glazer, 1991), a new line in biological control developed by a number of research groups (Samish and Glazer, 1992, 1993; Mauleon et al., 1993; Kocan et al., 1998; Samish et al., 1999, 2000a,b), and taken as an established technology in many laboratories around the world in the 2000s (Glazer et al., 2001; Samish and Glazer, 2001; Samish et al., 2004; Alekseev et al., 2006; Molina-Ochoa et al., 2009). EPN were also tested for their ability to suppress infestations by plant parasitic nematodes in different crops, e.g. to suppress Pratylenchus penetrans Cobb in strawberries (LaMondia and Cowles, 2002), Meloidogyne javanica (Treub) Chitwood, M. enterolobii (syn M. mayaguensis) Yang and Eisenback, M. incognita (Kofoid and White) Chitwood 1949 and M. hapla Chitwood in tomatoes (Fallon et al., 2002; Pérez and Lewis, 2002, 2004; Molina et al., 2007) and Ditylenchus dipsaci Kühn in garlic (Lopez-Robles and Hague, 2003). 6.3. Mixed technologies 6.3.1. Chemical pesticides Due to the rising interest in incorporating EPN in biological control programs, different modes of application and combinations of EPN with other agricultural pesticides have been studied, in an attempt to improve the efficiency of EPN in the field. The proportion of papers produced on these mixed technologies has grown from 6% to 11.1% in the period of time under analysis (Figs. 9a–11a), and the nature of those combinations has also changed. Early in the 1980s, studies on the relationships between EPN and other products or techniques were primarily focused on the effects that different combinations of agrochemicals had on the performance and survival of EPN (46.7% of total publications). Much of the published works included more than 100 chemical pesticides, including organophosphates, carbamates, pyrethroids, mancozeb, and copper sulphate (Hara and Kaya, 1982; Rovesti et al., 1988; Kaya and Burlando, 1989; Rovesti and Deseö, 1990) as well as herbicides such as glyphosate, alachlor and 2,4 D (Forschler et al., 1990).

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Through the 1990s, research on combining chemical products and EPN was reduced to 25.5% of the total publications in the mixed technologies category (Fig. 10b), due to the popularization of other biological control techniques (explained below). Experiments on the use of chemical pesticides in combination with EPN to asses compatibility were still performed (Gordon et al., 1996; Nishimatsu and Jackson, 1998; Kain and Agnello, 1999; Head et al., 2000); there was also a rising interest in the use of a new generation (in that time) systemic insecticide based on neonicotinoids (Koppenhöfer and Kaya, 1998; Koppenhöfer et al., 2000b). From 2001 to 2010, the amount of published work relating to pesticides in combination with EPN was 33% of the mixed technologies category (Fig. 11b), A considerable proportion of the research was focused on improving the control of a number of pests using neonicotinoids and EPN (Grewal et al., 2001; Alumai and Grewal, 2004; Barbara and Buss 2005; Polavarapu et al., 2007; Cuthbertson et al., 2008; Koppenhöfer and Fuzy, 2008; Morales-Rodriguez and Peck, 2009; Koppenhöfer et al., 2010), mostly because of the perceived innocuousness of the former on non-target insects. However in recent years the pesticide has been banned in some countries because it has shown adverse effects on some beneficial insects, including honey bees and bumble bees (Henry et al., 2012; Whitehorn et al., 2012). 6.3.2. Other biological control agents The increasing use of biological control agents since 1980 has motivated research on how to improve the control of insect pests by means of EPN combined with other biological agents. Over the last three decades the proportion of publications on this theme, within the mixed technologies category, has risen from 26.7% in the 1980s to 39.1% in the 2000s (this is also around 5% of the total EPN research, based on publication output) (Figs. 9b–11b). In the 1980s possible combined applications were directed at EPN + Bacillus thuringiensis Berliner (Gaugler et al., 1983; Poinar et al., 1990), Beavueria bassiana (Balsamo) Vuillemin (Barbercheck and Kaya, 1990) and also parasitoid insects such as Compsilura concinnata Meigen (Kaya, 1984); most of the research was conducted in the laboratory. The potential use of neem extracts (Azadirachta indica Jussieu) was evaluated for the first time by Rovesti and Deseö (1989). Research done in the following decade, was characterized by the beginning of field applications and the understanding of EPN synergy in combination with B. thuringiensis (Kaya et al., 1995; Koppenhöfer and Kaya, 1997; Baur et al., 1998; Koppenhöfer et al., 1999) and Paenibacillus (Bacillus) popilliae (Dutky) Pettersson, Ripere, Yousten and Priest (Kaya et al., 1993), for the purpose of controlling scarab grubs and some lepidopteran pests, with variable results and efficiency rates. Studies on entomopathogenic fungi (EPF) mixed with EPN increased in a number of papers and in a number of fungi species. Before 1990, research relating to compatibility between EPF and EPN was limited to EPN + B. bassiana; but in the 1990s other options were investigated, e.g., Metarhizium anisopliae (Metsch) Sorokin (Ellis and Emmett, 1993; Vänninen and Hokkanen, 1997), and Lecanicillim (Verticillium) lecanii (Zimmerman) Zare and Gams (Nilsson and Gripwall, 1999). The interest in evaluating parasitoids and their compatibility with EPN produced a number of publications that focused on controlling pests such as Cephalcia arvensis Panzer (Battisti, 1994), Agrotis ipsilon Hufnaagel (Zaki et al., 1997) and Liriomyza trifolii Burgess (Sher et al., 2000). In addition, nucleopolyhedroviruses were tested for the first time, and an additive effect was shown between the virus and S. carpocapsae, in the mortality of Spodoptera exigua Hübner larvae (Agra-Gothama et al., 1995, 1996). The use of neem extracts continued, particularly in Stark’s (1996) group. In the first decade of the 21th century, more research on the compatibility of various agents was performed within established

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biological control techniques and within completely new techniques. New discoveries and ideas of how to use EPN in different ways emerged, amongst them, the combination of EPN with predatory mites to control the western flower thrip Frankliniella occidentalis Pergande (Premachandra et al., 2003; Ebssa et al., 2006) as well as sciarid and phorid pests of mushrooms (Jess and Bingham, 2004). The direct use of EPN + plant extracts was researched and some advances were published for improving control methods. Plant extracts from neem to control the peach fruit fly, Bactrocera zonata Saunders (Mahmoud, 2007) and also Plutella xylostella Linnaeus in Chinese cabbage (Abdel-Razek and Gowen, 2002), as well as marigolds (Tagetes spp.) to control the cabbage maggot Delia radicum Linnaeus (Leger and Riga, 2009) were the most common; also, interesting progress was made in alkaloid manipulation to improve the control of the Colorado potato beetle (Leptinotarsa decemlineata Say) (Armer et al., 2004); however there was also a discovery that mustard incorporated into soils as biofumigants was harmful to EPN (Henderson et al., 2009; Ramírez et al., 2009). The published papers combining bacteria, fungi or viruses with EPN comprised 53.5% of the total publications on the sub-category ‘‘other biocontrol agents’’ in the decade of 2000s (23 out of 43). Basically, the studies on the use of those microorganisms reported their feasibility as depurated techniques to be used in commercial crops. Beauveria fungi were used (amongst others) in golf courses to eradicate white grubs (Choo et al., 2002), the plum curculio (Conotrachelus nenuphar Herbst) in apple and cherry orchards (Pereault et al., 2009), and to control the bark borer Indarbela dea Swinhoe in litchi trees (Schulte et al., 2009). Biological control using M. anisopliae included the control of Hoplia philanthus Fuessly, a pest of grasses (Ansari et al., 2004, 2006) and the sugar cane borer Diatraea saccharalis Fabricius (Molina-Acevedo et al., 2007). Another interesting use of fungi to improve insect control was the use of endophytic fungi to control white grubs in turf grass (Koppenhöfer and Fuzy, 2003). Some of the publications related to the combining of EPN and Bacillus bacteria included the control of shore flies (Scatella tenuicosta Collin) (Vänninen and Koskula, 2003), P. xylostella in cabbage crops (Schroer et al., 2005a), and Tipula paludosa Meigen in turf grass (Oestergaard et al., 2006). Parasitoid insects and EPN compatibility have been a big theme of discussion in the 2000s, that has led to an increase in publications (14% of the total in the category). Those papers were directed to (a) understanding how to apply both organisms without any significant negative interactions that do occur under some conditions, particularly predation and competition (Lacey et al., 2003; Leppla et al., 2007; Everard et al., 2009) and (b) to inquire on the performance of these combinations of organisms in either the laboratory or the field; some of the research included the control of corn borers using EPN and Trichogramma evanescens Westwood (El-Wakeil and Hussein, 2009) and the potential use of Heterorhabditis indica Poinar, Karunakar and David together with the braconid wasp Habrobracon hebetor Say in the management of the Indian meal moth, Plodia interpunctella Hubner (Mbata and Shapiro-Ilan, 2010). 6.3.3. Irrigation and delivery systems One of the advantages of EPN is the feasibility of application with unmodified traditional agriculture equipment, e.g., manual backpack-type sprayers and self-propelled agricultural sprayers. Research publications relating to delivery systems of EPN were almost nonexistent in the 1980s (1 paper), but in the 1990s, publications increased to 18%, or 24% within the ‘‘mixed technologies’’ category, with a further 21 publications in the proceeding decade (18.3%) (Figs. 9b–11b). Traditionally EPN have been applied in liquid formulation, however, different ideas have been developed to deliver EPN in the field in a cheaper and more creative manner. One of the pioneering works on EPN delivery via irrigation systems was that of Reed

et al. (1986), for control of the stripped cucumber beetle Acalymma vittatum Fabricius, although the authors failed to demonstrate good control. Another noteworthy paper was that of Curran and Patel (1988) to manage O. sulcatus in strawberry fields. The standardization in the 1980s of commercial strawberry production in Australia, included the use of plastic mulches, in combination with trickle irrigation; factors that were both costly and time consuming with respect to applying EPN (a need to apply manually around every plant). Finding an easier and cheaper method of delivering EPN into the field through that particular system resulted in increased effectiveness of the EPN (Curran and Patel, 1988). In subsequent years, the viability of delivering EPN in irrigation systems was evaluated (with a variety of equipment), to assess the infectivity, distribution and persistence of the EPN, e.g., CO2 backpack sprayers tested against different irrigation parameters (Downing, 1994; Cabanillas and Raulston, 1996), central pivots (Wright et al., 1993), stemflow systems (Ellsbury et al., 1996), spinning disc technology for micro sprayers (Mason et al., 1998a,b), drip irrigation (Conner et al., 1998) and sprinklers or boom sprayers (Hayes et al., 1999). Experiments in the past decade differ from previous studies as they focused on more accurate measurements of factors implicated directly in irrigation; for example, calculations of ideal operating pressure for application in numerous EPN species (Fife et al., 2003), the effect of static pressure on S. feltiae Filipjev (Chojnacki et al., 2010), pumping and temperature effects on EPN (Fife et al., 2007), hydraulic lift considerations to increase the persistence of S. riobrave Cabanillas, Poinar and Raulston in the rizosphere of citrus (Duncan and McCoy, 2001) as well as air injection and agitation effects on the viability of H. bacteriophora Poinar (Łaczynski et al., 2007). The expanded use of drip or mini sprinkler irrigation systems for the purpose of water economy, lead some researchers to examine the distribution patterns of the delivered EPN (Wennemann et al., 2003; Lara et al., 2008). Experiments to evaluate the potential of delivering EPN-infected cadavers of Galleria mellonella Linnaeus in the field, as a vehicle to protect the EPN and make the releasing of IJ more ‘‘natural’’, were done by Welch and Briand (1960); it was not until the early 1990s that this method gained further support, with interest in cadaver application on a range of crops and pests. Jansson et al. (1993) and Jansson and Lecrone (1994) measured the efficacy and persistence of Heterorhabditis sp. in the field to manage the sweet potato weevil (Cylas formicarius Fabricius). Meanwhile, other research groups studied characteristics related to the performance of EPN dispersal (Shapiro-Ilan and Glazer, 1996), or infectivity of the emerging IJ from insect cadavers vs. nematodes from aqueous suspensions (Shapiro-Ilan and Lewis, 1999). 6.3.4. Fertilizers and other additives The effect of fertilization on the viability of EPN has been an aspect of concern for many years and a subject of study, particularly fertilizers incorporated directly into the soil (the natural habitat of EPN). Pioneers in the field were Georgis and Gaugler (1991). The use of other additives (especially, anti-desiccants and UV protectants) opened the way to a rapid development of technology to apply EPN in the foliar environment. However, studies on this subject have been in decline in the past decade. In the 1980s and 1990s published papers in this sub-area represented 20% and 21.3% of the ‘‘mixed technologies’’ category, respectively, but between 2001 and 2010 this number dropped to less than half (9.6% or 11% published papers) (Figs. 9b–11b). Loss of EPN fitness caused by nitrogenous fertilizers (urea and fresh manures) was determined by Shapiro-Ilan et al. (1996); however, further research suggested that inconsistencies in results and the possible effect of specific fertilizer/EPN species could be the

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reason for such a loss of fitness (Bednarek and Gaugler, 1997; Shapiro-Ilan et al., 1999). On the other hand, many of the publications in the 1990s and 2000s on the combination of additives and EPN were directed to the use of surfactants and protectants, for the control of foliar pests (Glazer et al., 1992; Spaull, 1992; Nickle and Shapiro, 1992, 1994; Baur et al., 1997; Mason et al., 1998a,b; Schroeder and Sieburth, 1997; Jin et al., 2004; Schroer et al., 2005b; amongst others). Advances on the foliar application of EPN have been evident, especially with the incorporation of surfactants and UV protectants, however much research is ongoing to improve methods designed to control foliar pests, for further application under field conditions. 6.4. Mass production The development of techniques for the production of EPN in vitro has been one of the most remarkable achievements in entomopathogenic nematology. The relative simplicity to cultivate the symbiotic bacteria and the nematodes, has enabled researchers to test a large number of prospective production materials, to test additives or processes that could increase shelf life, to incorporate selective breeding into the production system and to assess more readily new formulations that improve effectiveness and decrease labour costs in the field. Topics related to the mass production of EPN, despite the importance of the mass production process to the commercial success of EPN, represented just a small proportion of the total EPN publications, that is, 4.3% (12 peer reviewed papers) in the 1980s and 5.8% (52 papers) in the last decade (Figs. 9a–11a). The vast majority of the publications in this category were associated with culture methods and relevant parameters regarding mass production (58.3% in the 1980s, 70.8% in the 1990s and 59.6% in the 2000s), followed by quality control and formulation (25% in the 1980s, 16.7% in the 1990s and 21.1% in the 2000s) and then storage and transportation of the finished product (16.6% in the 1980s, 12.5% in the 1990s and 19.2% in the 2000s) (Figs. 9b–11b). 6.4.1. Culture media and production parameters Before 1980 few attempts to produce EPN with artificial media were done; the lack of knowledge about the physiology of the symbiotic bacteria (which limited the quantities of IJ recovered in the process) and the very high costs of the required ingredients, made such initiatives hugely uneconomical (Poinar, 1972). In 1981 Robin Bedding published a novel method for producing EPN which was considered at the time a low cost yet highly efficient method to produce high numbers of IJ. The idea was based on the use of blended pig kidneys and beef fat imbibed in pieces of sponge, contained within a glass flask (Bedding, 1981). The same year Wouts published a paper, in which he proposed a recipe suitable for the mass production of Heterorhabditis heliothidis, using flour, nutrient broth, vegetable oil and yeast extract that were mixed and coated onto sponges (Wouts, 1981). Liquid mass culturing of EPN in the 1980s came from ideas proposed some years before, using small volumes (Stoll, 1953; Buecher and Hansen, 1971). Buecher and Popiel (1989) optimized the production of EPN in 250 ml flasks by adding and adjusting aeration; this method marked the basis for fermentor production of EPN. From late 1980s through the 1990s, a number of publications were devoted to the optimization of the chemical and physical parameters of liquid mass production (such as temperature, time, pH, additives), using commercial broth as the basal media (Dunphy and Webster, 1989; Han et al., 1993) as well as some new raw materials (Ogura and Haraguchi, 1994). Parameters relating to optimizing bacterial conditions and to developmental effects on EPN, e.g., inoculum size, physiological phase, non-symbiotic bacteria, sex ratios, recovery of IJ, etc., were investigated by a German

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group led by Ralf Ehler (Ehlers et al., 1990; Lunau et al., 1993; Strauch et al., 1994, amongst others). Further research in the 1990s was oriented towards conditions to culture specific EPN species or strains (Han, 1996; Ehlers et al., 1998, 2000); pilot-scale projects were designed (Surrey and Davies, 1996). Some components for culturing EPN that were considered inexpensive between 1980 and 2000 were by-products from other industries, e.g., offal from poultry, pork or beef industries. However, due to the relatively high levels of proteins and other compounds within these by-products, prices began to rise so much so, that nowadays the mass production of EPN with these products has become considerably more expensive. During the last decade new alternatives for preparing basal media with inexpensive products such as agave juice (from tequila production) and whey (from cheese industries) have been published (Chavarría-Hernández et al., 2005; Islas-López et al., 2005). Automation for in vivo mass production in G. mellonella (Gaugler et al., 2002), improvements on the inner design of fermentors (Chavarría-Hernández et al., 2007, 2010) and parameter settings (Shapiro-Ilan et al., 2002a; Young et al., 2002; David and Hugh, 2007) also contributed to reducing costs and maximizing EPN yield. 6.4.2. Quality control and Formulation As in any other industry, quality control of nematodes is mandatory to ensure success in biological control programs, and researchers involved in the development of mass production techniques were aware of this from the beginning. Whilst the number of papers produced on quality control, in the last three decades, appears relatively low (there were less than 10 papers), all of them set the protocols and principles for quality control measurements used today in mass production, field application and laboratory experimentation involving EPN (Yang et al., 1997; Converse and Miller, 1999; Brusselman et al., 2010; Caamano et al., 2010; Gaugler et al., 2000). The formulation of EPN for field applications has been closely related to quality control. When Bedding (1984) produced millions of IJ for the control of insect pests in Australia, he proposed to concentrate them in water to form a sludge-like mass, then then to load onto a polyurethane sponge. In the 1980s some attempts were done to create better formulae to improve the shelf life of the harvested infective IJ. Poinar et al. (1985) to embed the IJ in hydrogels; Kaya and Nelsen (1985) and to encapsulate IJ in baiting and edible capsules of calcium alginate developed later on by Navon et al., 1998 for the control of ants, cutworms and grasshoppers, the capsules allowed a gradual release of the IJ into the soil as they became moist. Covering seeds with the mixture was a novel way to protect seedling roots once germination had started (Kaya et al., 1987). In 1993 a new granular formulation based on dough composed by flour, kaolin and peat moss appeared under the name of ‘‘Pesta’’ (Connick et al., 1993), with a performance similar to that of the calcium alginate capsules, proposed almost 10 years before. Throughout the 1990s, improved formulas appeared which incorporated additives to control microflora responsible for the deterioration of the IJ (Connick et al., 1994; Georgis et al., 1995; Strauch et al., 2000). Solid formulations of EPN have a number of disadvantages when not applied directly into the soil, including poor nematode survival, difficulty in handling, carriers that block the spray or dripping nozzles during application. For these reasons, research groups in the 2000s sought to improve liquid formulation. Wilson and Ivanova (2004) formulated S. glaseri (Steiner) Wouts, Mracek, Gerdin & Bedding IJ (which are around 1 mm in length), suspending it in neutral density colloidal silica, that was more effective in IJ survival than aerated water suspensions. As mentioned before, the idea of using G. mellonella cadavers infected with EPN was not new,

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but the formulation of the cadavers coated with a series of additives proved that the cadavers retained IJ for longer periods of time and, as a consequence, also prolonged their shelf life (Shapiro-Ilan et al., 2001). 6.4.3. Storage and transport Once EPN are mass produced, a considerable challenge is to keep the product alive and if possible improve its long shelf life. Two strategies have generally been applied (alone or in combination) to extend the shelf life of EPN: temperature management (to slow down the EPN metabolism) and dehydration. Research on improving shelf life has the lowest publication record in the category (Figs. 9b–11b), but many advances have indeed been achieved. Thirty years ago, aeration was the method of choice to keep the nematodes alive (Bedding, 1984). The use of low temperatures to store and ship nematodes began in the late 1980s and early 1990s (Sunderababu et al., 1985; Westerman, 1992), but soon it was realized that many other factors influenced the viability of EPN, experiments with additional additives were proven unsuccessful (Strauch et al., 2000). Meanwhile, Grewal (2000a,b) postulated the use of anhydrobiosis after low temperature acclimation, to improve the viability of EPN; this set the basis for long term storage methods and is still in use today. Another important success in keeping nematodes alive at room temperature was achieved by Chen and Glazer (2005), who induced an osmotical reduction of their metabolism, similar to dehydration. 6.5. Relationships with other organisms The study of relationships between EPN and non-target organisms has produced a series of interesting papers. The proportion of publications within entomopathogenic nematology has remained unchanged during the last three decades (Fig. 9a and b), though their absolute number has almost tripled from the 1980s to the 2000s (from 18 to 59 papers). In the 1980s much of the research in this area was focused on demonstrating the innocuousness of EPN to non-target organisms, including beneficial insects (Georgis and Hague, 1982; Mrácˇek and Spitzer, 1983), collembolans (Ireson and Miller, 1983), isopods (Poinar and Paff, 1985), amphibians (Kermarrec and Mauleon; 1985), annelids (Capinera et al., 1992), gastropods (Poinar, 1989), spiders and opiliones (Poinar and Thomas, 1985). The susceptibility of EPN to nematophagous fungi was also an important theme of investigation (representing 16.7% of published records within this category, Fig. 9b) (Poinar and Jansson, 1986a,b; Van Sloun et al., 1990). In these and in later research, EPN were repeatedly reported as harmless to non-target organisms (Lynch and Thomas, 2000; Somasekhar et al., 2002a,b; Zoltowska et al., 2003). The effect of more species of namatophagous fungi on EPN, e.g., Timper et al. (1991), Koppenhöfer et al. (1996), Jaffee and Strong (2005), and the role of different organisms in the dispersal of EPN (Shapiro-Ilan et al. (1993), Eng et al., 2005) were further investigated between 1990 and 2010. Between 1990 and 2010, there were at least 20 records which addressed the relationships between EPN in soils and the population dynamics of other nematodes (Figs. Fig. 10b and Fig. 11b). Some of those publications were dedicated to understanding the capability of EPN to reduce specific plant parasitic nematodes, in order to establish methodologies for crop protection (Grewal et al., 1997; Perry et al., 1997; Molina et al., 2007; Jagdale and Grewal, 2008; amongst others). Other research was focused, arguably for the first time, on the effect of EPN in the whole community of nematodes, under different soil conditions (Wang et al., 2001; Somasekhar et al., 2002a,b), in microcosm environments (De Nardo et al., 2006) and on the natural populations of other EPN species (Danilov et al., 2008).

Research on the ecological significance of interactions between EPN and other nematodes was an important issue in this period, and represented 23.8% of published records in the 1990s and 25.4% in the 2000s, within this category (Fig. 10b and c). The function of plants roots (Kanagy and Kaya, 1996) and plant endophytes (Grewal et al., 1995; Kunkel and Grewal, 2003; Richmond et al., 2004) were tested, with respect to the susceptibility of different insects to EPN in the presence or absence of plants roots (Jaworska and Ropek, 1994). Attraction of EPN by damaged roots (root exudates) due to subterranean herbivory has been demonstrated by some researchers (Choo et al., 1989; Choo and Kaya, 1991; van Tol et al., 2001), but none of them could identify the nature of those exudates. A major breakthrough was accomplished when Rasmann et al., 2005 discovered that some plants exude (E)-b-caryophyllene when under insect attack, which subsequently attracts EPN to the rhizosphore. As a consequence, the perception of the scientific community to the interaction between plants, herbivorous insects and EPN (tritrophic interactions) changed; great progress within this field has been made since then, e.g., Gassmann et al. (2010), Hiltpold and Turlings (2008), Jagdale et al. (2009). 6.6. Symbiotic interaction The discovery of Xenorhabdus (Thomas and Poinar, 1979) and Photorhabdus (Boemare et al., 1993) as symbionts of Steinernema and Heterorhabditis, respectively, took a dramatic turn in the entire discipline, inasmuch as EPN were now perceived as a complex of organisms that deserved new lines of research (Burnell and Stock, 2000). The biological and ecological role of bacteria, new lines of biological control, symbiotic interactions between EPN and bacteria, improvement of mass production techniques and genetic regulation of their physiology, were some examples of the sudden increase of novel disciplines. Between 1980 and 2000, studies on the symbiotic relationship between EPN and bacteria addressed characterization and some basic facts; however the total contribution of this sub category to publication output was never higher than 1.1% of total output (Figs. Fig. 9a and 10a). Despite this low figure, solid contributions by a number of research groups, like the one lead by Noel Boemare at the University of Montpellier, France, pioneered research on the bacterial functions within the EPN complex, as well as on the biochemical characterization of the bacterial components and their physiological phase regulation (Boemare et al., 1996; Moureaux et al., 1995; Smigielski et al., 1994, to mention but a few). From 2000 to 2010, thanks to the incorporation of more research groups, led mainly by Heidi Goodrich-Blair (University of Wisconsin-Madison, USA) and Mathieu Sicard (University of Poitiers, France), publication output on this subject rose to almost 5% (Fig. 11a). More important than the proportion of published papers was the information that these outputs actually contained: in them, the discovery of new gene mechanisms responsible for the bacterial colonization (Herbert Tran et al., 2007, 2009), the function of the bacteria in fitness and development of EPN (Sicard et al., 2005a,b; Emelianoff et al., 2007) and the co-evolution processes of mutualism (Sicard et al., 2005a,b) were described. 7. The publishing issue Many journals have engaged in the publication of papers related to entomopathogenic nematology. Nevertheless, the number and participation of those specialized and non-specialized journals have changed in the last decades. Thirty years ago, between 1980 and 1990, 72 journals were responsible for disseminating information about EPN, but this number almost tripled to 210 in 2010 (Fig. 12).

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The ten most important sources for EPN publications, per decade, can be seen in Fig. 12. In the 1980s they gathered almost 60% of the publications, of which 32.0% (76 papers) were in journals specialized in nematology (Fig. 12a). The most prominent was the Journal of Nematology (16.4%, 39 papers, mainly on ‘‘mixed technology’’), followed by Revue de Nematologie (8.4%, 20 papers, mainly on ‘‘taxonomy’’ and ‘‘behavior’’) and Nematologica (7.1%, 17 papers). Important journals like Journal of Invertebrate Pathology (10.5%, 25 papers), IRCS Medical science. Key reports in human and animal physiology (5.0%, 12 papers) and Environmental Entomology (3.8%, 9 papers), as well as Canadian Entomologist, Journal of Economic Entomology and Entomophaga, were dedicated mainly to advances in EPN potential for biological control (Fig. 13). Ten years later, 10 most important journals contributed to 57.8% of the EPN-related publications, but despite increasing the number of EPN papers in nematology journals to 165, their relative participation declined to 22.5% (Fig. 12b); in fact, the Journal of Nematology, which again was the most important journal in the 1990s, reduced its weightage to 10.7%. At the same time some important journals such as the Journal of Invertebrate Pathology kept its relative importance for entomopathogenic nematology research with 10.1% (75 papers) of the whole EPN publications, and some journals that specialized in biological control began to give some weightage to the theme of EPN as controls, e.g., Biocontrol Science and Technology (5.5%, 40 papers), Biological Control (3.8%, 28 papers). In the 1990s, preferences of journals to publish papers on specific fields were defined into two groups: the firston ‘‘biocontrol’’ and ‘‘mixed technologies’’ themes, which have been predominantly published in journals devoted to entomology, crop protection and biocontrol, and the second in which all other themes are grouped together, predominantly published in nematological and parasitological journals. In the last decade, nematologists started to publish in journals with higher impact factors. The most important nematology journals were relegated to a secondary position, to publish only 15.6% of the total production, less than those published in the previous decade in absolute numbers (156; Fig. 12c). Interestingly, the Journal of Nematology dropped its participation to the 5th place (44 articles) whereas Nematology rose to the 2nd place (9.2%, 92 papers). Biological Control became a prominent journal between 2001 and 2010, publishing 100 EPN-related papers (10.0%). Other journals, related to biological control or entomology, published 31.2% with 313 papers. In the last decade, ‘‘biocontrol’’ and ‘‘mixed technologies’’ papers are still published in the usual journals, e.g., Biological Control, Journal of Economic Entomology, etc. Authors preferred to publish papers on ‘‘biogeography’’ in Nematology, Russian Journal of Nematology and Journal of Parasitology; a relationship between ‘‘behavior’’ articles and Journal of Invertebrate Pathology, International Journal for Parasitology, Applied Soil Ecology and Phytoparasitica was found. Interestingly, in the last 10 years the Journal of Nematology published many articles related to EPN relationships with other organisms, whilst many others were dedicated to future perspectives on the use of EPN. The increased importance of research on the symbiotic interaction in the EPN-bacteria complex grouped the majority of those publications in several microbiological journals, such as the Journal of Bacteriology, Molecular Microbiology and Applied and Environmental Microbiology. Additionally, Zootaxa and Sytematic Parasitology were devoted exclusively to publish new species of EPN and taxonomy issues (Fig. 13).

8. The next 10 years The increasing interest in using biological control agents in crops, combined with new policies and regulations in international

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markets on agricultural products, have changed the perspectives of farming in the world. Many less developed countries have found an opportunity to participate, and have therefore started or will start soon their own research in EPN and other biocontrol organisms, as an alternative to reduce the use of agrochemicals and, at the same time, to guarantee better opportunities for trading by small farmers and improving their standard of living. New raw materials derived from local by-products and less sophisticated techniques for mass production could be designed for their use in countries with less expanded agricultural systems. Also, research on the application of new technologies (irrigation systems, fertilizers, protectants and other agrochemicals) will keep pace. The discovery of a new EPN species and its use in controlling neglected insect pests is expected, especially in the tropics where efforts are being made to establish biological control programmes. New research in biogeography may appear in the near future thanks to the ease of EPN sampling using G. mellonella traps. For those reasons, the participation of Latin American, African and Asian countries in entomopathogenic nematology research should increase in the next decade. For these efforts to be successful, investment by public and private bodies, as well as collaboration via networking provided by institutions from richer countries, are mandatory. The exponential developments on science and technology in the 21st century, particularly in developed countries, will secure a rapid growth of our discipline. Proteomics, new tools in genomics and other molecular approaches have appeared and many more will emerge, not only to help in a better understanding of the biology and ecology of EPN, but also to improve biological control programmes. Pressure to publish in journals with high impact factors or other measurements of quality is to be maintained. This scenario has made nematology journals the second or third choice when authors look for more visibility for their publications. To change that picture, relevant reviews in every issue to increase the journal number of citations, efforts to promote international workshops on state of the art techniques, followed by publication of their proceedings, and other options to make the journal more attractive to researchers, should be implemented. Many areas of entomopathogenic nematology are far from being fully understood. However, currently there are many laboratories working in this field and many more will join in the future, from different nationalities and backgrounds, to place EPN as one of the most reliable biocontrol agents. For this to become true, efforts need to be done to ensure that new knowledge and applications (on ignored crops) are published, in order to provide information to new generations of scientist from countries outside the developed world. Acknowledgments The author thanks Dr. Gioconda San-Blas (Instituto Venezolano de Investigaciones Científicas (IVIC), Caracas, Venezuela) and Dr. Steve Edgington (CABI Europe-UK, Egham, UK) for their valuable comments and suggestions. Also, thanks to the staff of Bibiloteca Marcel Roche (http://www.biblioteca.ivic.ve/; IVIC), for helping in the provision of papers used for building the data sets of this study. References Abdel-Razek, A.S., Gowen, S., 2002. The integrated effect of the nematode–bacteria complex and neem plant extracts against Plutella xylostella (L.) larvae (Lepidoptera: Yponomeutidae) on Chinese cabbage. Arch. Phytopathol. Plant Protect. 35, 181–188. Abu Hatab, M.A., Gaugler, R., 1997. Influence of growth temperature on fatty acids and phospholipids of Steinernema riobravis infective juveniles. J. Therm. Biol. 22, 237–244.

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Adhikari, B.N., Lin, C.-Y., Bai, X., Ciche, T.A., Grewal, P.S., Dillman, A.R., Chaston, J.M., Shapiro-Ilan, D.I., Bilgrami, A.L., Gaugler, R., Sternberg, P.W., Adams, B.J., 2009. Transcriptional profiling of trait deterioration in the insect pathogenic nematode Heterorhabditis bacteriophora. BMC Genomics 10, 609. Agra-Gothama, A.A., Lawrence, G.W., Sikorowski, P.P., 1996. Activity and persistence of Steinernema carpocapsae and Spodoptera exigua nuclear polyhedrosis virus against S. exigua larvae in soybean. J. Nematol. 28, 68–74. Agra-Gothama, A.A., Sikorowski, P.P., Lawrence, G.W., 1995. Interactive effects of Steinernema carpocapsae and Spodoptera exigua nuclear polyhedrosis virus on Spodoptera exigua larvae. J. Invertebr. Pathol. 66, 270–276. Agüera De Ducet, M.M., 1986. A new species of Neoaplectana Steiner, 1929 (Nematoda: Steinernematidae) from Córdoba, Argentina. Rev. Nématol. 9, 317– 323. Akhurst, R.J., Bedding, R.A., 1986. Natural occurrence of insect pathogenic nematodes (Steinernematidae and Heterorhabditidae) in soil in Australia. Aust. J. Entomol. 25, 241–244. Akhurst, R.J., Brooks, W.N., 1984. The distribution of entomophilic nematdes (Heterorhabditidae and Steinernematidae) in North Carolina. J. Invertebr. Pathol. 44, 140–145. Alatorre-Rosas, R., Kaya, H.K., 1990. Interspecific competition between entomopathogenic nematodes in the genera Heterorhabditis and Steinernema for an insect host in sand. J. Invertebr. Pathol. 55, 179–188. Alekseev, E., Glazer, I., Samish, M., 2006. Effect of soil texture and moisture on the activity of entomopathogenic nematodes against female Boophilus annulatus ticks. Biocontrol 51, 507–518. Ali, J.G., Alborn, H.T., Stelinski, L.L., 2010. Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes. J. Chem. Ecol. 36, 361–368. Alsaiyah, M.A.M., Ebssa, L., Zenner, A., O’Callaghan, K.M., Griffin, C.T., 2009. Sex ratios and sex-biased infection behaviour in the entomopathogenic nematode genus Steinernema. Int. J. Parasitol. 39, 725–734. Alumai, A., Grewal, P.S., 2004. Tank-mix compatibility of the entomopathogenic nematodes, Heterorhabditis bacteriophora and Steinernema carpocapsae, with selected chemical pesticides used in turfgrass. Biocontrol Sci. Tech. 14, 725– 730. Ansari, M.A., Butt, T.M., 2011. Effect of potting media on the efficacy and dispersal of entomopathogenic nematodes for the control of black vine weevil, Otiorhynchus sulcatus (Coleoptera: Curculionidae). Biol. Control 58, 310–318. Ansari, M.A., Shah, F.A., Butt, T.M., 2010. The entomopathogenic nematode Steinernema kraussei and Metarhizium anisopliae work synergistically in controlling overwintering larvae of the black vine weevil, Otiorhynchus sulcatus, in strawberry grow bags. Biocontrol Sci. Tech. 20, 99–105. Ansari, M.A., Shah, F.A., Tirry, L., Moens, M., 2006. Field trials against Hoplia philanthus (Coleoptera: Scarabaeidae) with a combination of an entomopathogenic nematode and the fungus Metarhizium anisopliae CLO 53. Biol. Control 39, 453–459. Ansari, M.A., Tirry, L., Moens, M., 2004. Interaction between Metarhizium anisopliae CLO 53 and entomopathogenic nematodes for the control of Hoplia philanthus. Biol. Control 31, 172–180. Armer, C.A., Berry, R.E., Reed, G.L., Jepsen, S.J., 2004. Colorado potato beetle control by application of the entomopathogenic nematode Heterorhabditis marelata and potato plant alkaloid manipulation. Entomol. Exp. Appl. 111, 47–58. Artyukhovsky, A.K., 1967. Neoaplectana arenaria nov. sp. (Steinernematidae, Nematoda) inducing disease in chafers of the Voronezh region. Trudy Voroneszhskogo Gosudarstvennego Zapovednika 15, 94–100. Bai, X., Grewal, P.S., 2007. Identification of two down-regulated genes in entomopathogenic nematode Heterorhabditis bacteriophora infective juveniles upon contact with insect hemolymph. Mol. Biochem. Parasitol. 156, 162–166. Balasubramanian, N., Hao, Y.-J., Toubarro, D., Nascimento, G., Simões, N., 2009. Purification, biochemical and molecular analysis of a chymotrypsin protease with prophenoloxidase suppression activity from the entomopathogenic nematode Steinernema carpocapsae. Int. J. Parasitol. 39, 975–984. Balasubramanian, N., Toubarro, D., Simões, N., 2010. Biochemical study and in vitro insect immune suppression by a trypsin-like secreted protease from the nematode Steinernema carpocapsae. Parasite Immunol. 32, 165–175. Barbara, K.A., Buss, E.A., 2005. Integration of insect parasitic nematodes (Rhabditida Steinernematidae) with insecticides for control of pest mole crickets (Orthoptera: Gryllotalpidae: Scapteriscus spp.). J. Econ. Entomol. 98, 689–693. Barbercheck, M.E., Kaya, H.K., 1990. Interactions between Beauveria bassiana and the entomogenous nematodes, Steinernema feltiae and Heterorhabditis heliothidis. J. Invertebr. Pathol. 55, 225–234. Battisti, A., 1994. Effect of the entomopathogenic nematodes on the spruce webspinning sawfly Cephalcia arvensis Panzer and its parasitoids in the field. Biocontrol Sci. Tech. 4, 95–102. Baur, M.E., Kaya, H.K., Gaugler, R., Tabashnik, B., 1997. Effects of adjuvants on entomopathogenic nematode persistence and efficacy against Plutella xylostella. Biocontrol Sci. Tech. 7, 513–525. Baur, M.E., Kaya, H.K., Gaugler, R., Tabashnik, B., Chilcutt, C.F., 1998. Suppression of diamondback moth (Lepidoptera: Plutellidae) with an entomopathogenic nematode (Rhabditida: Steinernematidae) and Bacillus thuringiensis Berliner. J. Econ. Entomol. 91, 1089–1095. Bedding, R.A., 1981. Low cost in vitro mass production of Neoaplectana and Heterorhabditis species (Nematoda) for field control of insect pests. Nematologica 27, 109–114.

Bedding, R.A., 1984. Large scale production, storage and transport of the insect parasitic nematodes Neoaplectana spp. and Heterorhabditis spp. Ann. Appl. Biol. 104, 117–120. Bedding, R.A., Miller, L.A., 1981. Use of a nematode, Heterorhabditis heliothidis, to control black vine weevil, Otiorhynchus sulcatus, in potted plants. Ann. Appl. Biol. 99, 211–216. Bedding, R.A., Molyneux, A.S., 1982. Penetration of insect cuticle by infective juveniles of Heterorhabditis spp. (Heterorhabditidae: Nematoda). Nematologica 28, 354–359. Bednarek, A., Gaugler, R., 1997. Compatibility of soil amendments with entomopathogenic nematodes. J. Nematol. 84, 713–720. Bird, A.F., Bird, J., 1986. Observations on the use of insect parasitic nematodes as a means of biological control of root-knot nematodes. J. Parasitol. 16, 511–516. Brivio, M.F., Moro, M., Maristella, M., 2006. Down-regulation of antibacterial peptide synthesis in an insect model induced by the body-surface of an entomoparasite (Steinernema feltiae). Dev. Comp. Immunol. 30, 627–638. Blackshaw, R.P., 1988. A survey of insect parasitic nematodes in Northern Ireland. Ann. Appl. Biol. 113, 561–565. Blackshaw, R.P., Newell, C.R., 1989. Studies on temperature limitations to Heterorhabditis heliothidis activity. Nematologica 33, 180–185. Boemare, N.E., Akhurst, R.J., Mourant, R.G., 1993. DNA relatedness between Xenorhabdus spp. (Enterorbacteriaceae) symbiotic bacteria of entomopathogenic nematodes, and proposal to transfer Xenorhabdus luminescens to a new genus, Photorhabdus gen. nov. Int. J. Syst. Bacteriol. 43, 249–255. Boemare, N., Laumond, C., Mauleon, H., 1996. The entomopathogenic nematode– bacterium complex: biology, life cycle and vertebrate safety. Biocontrol Sci. Tech. 6, 333–345. Bohan, D.A., Hominick, W.M., 1997. Sex and the dynamics of infection in the entomopathogenic nematode Steinernema feltiae. J. Helminthol. 71, 197–202. Bovien, P., 1937. Some types of association between nematodes and insects. Videnskabelige Meddelelser Dansk Naturhistorisk Forening 101, 1–114. Brusselman, E., Nuyttens, D., Steurbaut, W., Messens, W., De Sutter, N., Viaene, N., Moens, M., 2010. An image processing technique for the observation of the viability of Steinernema carpocapsae in spray application research. Nematology 12, 105–113. Buecher, E.J., Hansen, E.L., 1971. Mass culture of axenic nematodes using continuous aeration. J. Nematol. 3, 199–200. Buecher, E.J., Popiel, I., 1989. Liquid culture of entomogenous nematode Steinernema feltiae with its bacterial symbiont. J. Nematol. 21, 500–504. Burman, M., Pye, A.E., 1980. Neoaplectana carpocapsae: movements of nematode populations on a thermal gradient. Exp. Parasitol. 49, 258–265. Burnell, A.M., Stock, S.P., 2000. Heterorhabditis, Steinernema and their bacterial symbionts-lethal patogen of insects. Nematology 2, 31–42. Byers, J.A., Poinar Jr., G.O., 1982. Location of insect hosts by the nematode Neoaplectana carpocapsae, in response to temperature. Behaviour 79, 1–10. Caamano, E.X., Cloyd, R.A., Solter, L.F., Fallon, D.J., 2010. Quality assessment of two commercially available species of entomopathogenic nematodes: Steinernema feltiae and Heterorhabditis indica. HortTechnology 18, 85–89. Cabanillas, H.E., Raulston, J.R., 1996. Effects of furrow irrigation on the distribution and infectivity of Steinernema riobravis against corn earworm in corn. Fund. Appl. Nematol. 19, 273–281. Capinera, J.L., Blue, S.L., Wheeler, G.S., 1992. Survival of earthworms exposed to Neoaplectana carpocapsae nematodes. J. Invertebr. Pathol. 39, 419–421. Chavarría-Hernández, N., Espino-García, J.J., Sanjuan-Galindo, R., RodríguezHernández, A.I., 2005. Monoxenic liquid culture of the entomopathogenic nematode Steinernema carpocapsae using a culture medium containing whey kinetics and modeling. J. Biotechnol. 125, 75–84. Chavarría-Hernández, N., Ortega-Morales, E., Vargas-Torres, A., ChavarríaHernández, J.C., Rodríguez-Hernández, A.I., 2010. Submerged monoxenic culture of the entomopathogenic nematode, Steinernema carpocapsae CABA01, in a mechanically agitated bioreactor: evolution of the hydrodynamic and mass transfer conditions. Biotechnol. Bioprocess Eng. 15, 580–589. Chavarría-Hernández, N., Sanjuan-Galindo, R., Rodríguez-Pastrana, B.R., MedinaTorres, L., Rodríguez-Hernández, A.I., 2007. Submerged monoxenic culture of the entomopathogenic nematode Steinernema carpocapsae in an internal-loop airlift bioreactor using two configurations of the inner tube. Biotechnol. Bioeng. 98, 167–176. Chen, S., Glazer, I., 2005. A novel method for long-term storage of the entomopathogenic nematode Steinernema feltiae at room temperature. Biol. Control 32, 104–110. Chen, S., Glazer, I., Gollop, N., Cash, P., Argo, E., Innes, A., Stewart, E., Davidson, I., Wilson, M.J., 2009. Proteomic analysis of the entomopathogenic nematode Steinernema feltiae IS-6 IJs under evaporative and osmotic stresses. Mol. Biochem. Parasitol. 145, 195–204. Chojnacki, J., Dulcet, E., Grieger, A., 2010. Influence of static pressure on viability of entomopathogenic nematodes – Steinernema feltiae. Proc. World Acad. Sci. Eng. Technol. 65, 471–473. Choo, H.Y., Kaya, H.K., 1991. Influence of soil texture and presence of roots on host finding by Heterorhabditis bacteriophora. J. Invertebr. Pathol. 58, 279–280. Choo, H.Y., Kaya, H.K., Burlando, T.M., Gaugler, R., 1989. Entomopathogenic nematodes: host-finding ability in the presence of plant roots. Environ. Entomol. 18, 1136–1140. Choo, H.Y., Kaya, H.K., Huh, J., Lee, D.W., Kim, H.H., Lee, S.M., Choo, Y.M., 2002. Entomopathogenic nematodes (Steinernema spp. and Heterorhabditis bacteriophora) and a fungus Beauveria brongniartii for biological control of the

E. San-Blas / Biological Control 66 (2013) 102–124 white grubs, Ectinohoplia rufipes and Exomala orientalis, in Korean golf courses. Biocontrol 47, 177–192. Cohen, N.E., Brown, I.M., Gaugler, R., 2002. Physiological ageing and behavioural plasticity of Heterorhabditis bacteriophora infective juveniles. Nematology 4, 81– 87. Connick, W.J., Nickle, W.R., Vinyard, B.T., 1993. ‘‘Pesta’’: new granular formulations for Steinernema carpocapsae. J. Nematol. 25, 198–210. Connick, W.J., Nickle, W.R., Williams, K.S., Vinyard, B.T., 1994. Granular formulations of Steinernema carpocapsae (strain AII) (Nematoda: Rhabditida) with improved shelf life. J. Nematol. 26, 352–359. Conner, J.M., McSorley, R., Stansly, P.A., Pitts, D.J., 1998. Delivery of Steinernema riobravis through a drip irrigation system. Nematropica 28, 95–100. Converse, V., Miller, R.W., 1999. Development of the one-to-one quality assessment assay for entomopathogenic nematodes. J. Invertebr. Pathol. 74, 143–148. Curran, J., Patel, V., 1988. Use of a trickle irrigation system to distribute entomopathogenic nematodes (Nematoda: Heterorhabditidae) for the control of weevil pests (Coleoptera: Curculionidae) of strawberries. Aust. J. Exp. Agric. 28, 639–643. Cuthbertson, A.G.S., Mathers, J.J., Northing, P., Prickett, A.J., Walters, K.F.A., 2008. The integrated use of chemical insecticides and the entomopathogenic nematode, Steinernema carpocapsae (Nematoda: Steinernematidae), for the control of sweetpotato whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). Insect Sci. 15, 447–453. Danilov, L.G., Makhotkin, A.G., Vasiliev, S.V., Turitsyn, V.S., 2008. Interaction between Steinernema carpocapsae with the arthropod fauna and natural populations of entomopathogenic nematodes in orchard biotope. Parazitologiya 42, 129–138 [Abstr.]. De Nardo, E.A.B., Grewal, P.S., McCartney, D., Stinner, B.R., 2006. Non-target effects of entomopathogenic nematodes on the soil nematode community cycling processes: a microcosm study. Appl. Soil Ecol. 34, 250–257. Downing, A.S., 1994. Effect of irrigation and spray volume on efficacy of entomopathogenic nematodes (Rhabditida: Heterorhabditidae) against white grubs (Coleoptera: Scarabaeidae). J. Econ. Entomol. 87, 643–646. Duncan, L.W., McCoy, C.W., 2001. Hydraulic lift increases herbivory by Diaprepes abbreviatus larvae and persistence of Steinernema riobrave in dry soil. J. Nematol. 33, 142–146. Duncan, L.W., McCoy, C.W., Terranova, A.C., 1996. Estimating sample size and persistence of entomogenous nematodes in sandy soil and their efficacy against the larvae of Diaprepes abbreviatus in Florida. J. Nematol. 28, 56–67. Dunphy, G.B., Webster, J.M., 1985. Influence of Steinernema feltiae (Filipjev) Wouts, Mracek, Gerdin and Bedding DD136 strain on the humoral and haemocytic responses of Galleria mellonella (L.) larvae to selected bacteria. Parasitology 91, 369–380. Dunphy, G.B., Webster, J.M., 1987. Partially characterized components of the epicuticle of dauer juvenile Steinernema feltiae and their influence on hemocyte activity in Galleria mellonella. J. Parasitol. 73, 584–588. Dunphy, G.B., Webster, J.M., 1989. The monoxenic culture of Neoaplectana carpocapsae DD136 and Heterorhabditis heliothidis. Rev. Nématol. 12, 113–123. Ebssa, L., Borgemeister, C., Poehling, H.M., 2006. Simultaneous application of entomopathogenic nematodes and predatory mites to control western flower thrips Frankliniella occidentalis. Biol. Control 39, 66–74. Ehlers, R.-U., Lunau, S., Krasomil-Osterfeld, K., Osterfeld, K.H., 1998. Liquid culture of the entomopathogenic nematode bacterium-complex Heterorhabditis megidis/Photorhabdus luminescens. Biocontrol 43, 77–86. Ehlers, R.U., Niemann, I., Hollmer, S., Strauch, O., Jende, D., Shanmugasundaram, M., Mehta, U.K., Easwaramoorthy, S.K., Burnell, A., 2000. Mass production potential of the bacto-helminthic biocontrol complex Heterorhabditis indica-Photorhabdus luminescens. Biocontrol Sci. Tech. 10, 607–616. Ehlers, R.U., Stoessel, S., Wyss, U., 1990. The influence of phase variants of Xenorhabus spp. and Escherichia coli (Enterobacteriaceae) on the propagation of entomopathogenic nematodes of genera Steinernema and Heterorhabditis. Rev. Nématol. 13, 417–424. Ellis, S.A., Emmett, B.J., 1993. A comparison of Metarhizium anisopliae, insect parasitic nematodes and fonofos against vine weevil in cyclamen. Tests Agrochem. Cultiv. 14, 188–189 [Abstr.]. Ellsbury, M.M., Jackson, J.J., Woodson, W.D., Beck, D.L., Stange, K.A., 1996. Efficacy, application distribution, and concentration by stemflow of Steinernema carpocapsae (Rhabditida: Steinernematidae) suspensions applied with a lateral-move irrigation system for corn rootworm (Coleoptera: Chrysomelidae) control in maize. J. Econ. Entomol. 89, 74–81. El-Wakeil, N.E., Hussein, M.A., 2009. Field performance of entomopathogenic nematodes and an egg parasitoid for suppression of corn borers in Egypt. Arch. Phytopathol. Plant Protect. 42, 228–237. Emelianoff, V., Sicard, M., Le Brun, N., Moulia, C., Ferdy, J.B., 2007. Effect of bacterial symbionts Xenorhabdus on mortality of infective juveniles of two Steinernema species. Parasitol. Res. 100, 657–659. Eng, M.S., Preisser, E.L., Strong, D.R., 2005. Phoresy of the entomopathogenic nematode Heterorhabditis marelatus by a non-host organism, the isopod Porcellio scaber. J. Invertebr. Pathol. 88, 173–176. European Commission, 1988. Environment and Agriculture. Commission Document COM 88, p. 338. Everard, A., Griffin, C.T., Dillon, A.B., 2009. Competition and intraguild predation between the braconid parasitoid Bracon hylobii and the entomopathogenic nematode Heterorhabditis downesi, natural enemies of the large pine weevil, Hylobius abietis. Bull. Entomol. Res. 99, 151–161.

119

Fallon, D.J., Kaya, H.K., Gaugler, R., Sipes, B.S., 2002. Effects of entomopathogenic nematodes on Meloidogyne javanica on tomatoes and soybeans. J. Nematol. 34, 239–245. Fife, J.P., Derksen, R.C., Ozkan, H.E., Grewal, P.S., 2003. Effects of pressure differentials on the viability and infectivity of entomopathogenic nematodes. Biol. Control 27, 65–72. Fife, J.P., Ozkan, H.E., Derksen, R.C., Grewal, P.S., 2007. Effects of pumping on entomopathogenic nematodes and temperature increase within a spray system. Appl. Eng. Agric. 23, 405–412. Figueroa, W., Román, J., 1990. Parasitism of entomophilic nematodes on the sugar cane rootstalk borer, Diaprepes abbreviatus (L.) (Coleoptera: Curculionidae), larvae. J. Agric. Univ. Puerto Rico 74, 197–202. Filipjev, I.N., 1934. Miscellanea nematodologica, I. Eine neue Art der Gattung Neoaplectana Steiner nebst Bemerkungen über die systematische Stellung der letzten. Parazitologichesky Sbornik 4, 229–239. Finnegan, M.M., Downes, M.J., O’regan, M., Griffin, C.T., 1999. Effect of salt and temperature stresses on survival and infectivity of Heterorhabditis spp. Nematology 1, 69–78. Fischer, P., Führer, E., 1990. Effect of soil acidity on the entomophilic nematode Steinernema kraussei Steiner. Biol. Fertil. Soils 9, 174–177. Fodor, A., Dey, I., Farkas, T., Chitwood, D.J., 1994. Effects of temperature and dietary lipids on phospholipid fatty acids and membrane fluidity in Steinernema carpocapsae. J. Nematol. 26, 278–285. Forschler, B.T., All, J.N., Gardner, W.A., 1990. Steinernema feltiae activity and infectivity in response to herbicide exposure in aqueous and soil environments. J. Invertebr. Pathol. 55, 375–379. Fowler, H.G., 1988. Occurrence and infectivity of entomogenous nematodes in mole crickets in Brazil. Int. Rice Res. Newsletter 13, 34–35. Fujiie, A., Yokoyama, T., 1998. Effects of ultraviolet light on the entomopathogenic nematode, Steinernema kushidai and its symbiotic bacterium, Xenorhabdus japonicus. Appl. Entomol. Zool. 33, 263–269. Fujimoto, A., Lewis, E.E., Cobanoglu, G., Kaya, H.K., 2007. Dispersal, infectivity and sex ratio of early- or late-emerging infective juveniles of the entomopathogenic nematode Steinernema carpocapsae. J. Nematol. 39, 333–337. Gal, T.Z., Solomon, A., Glazer, I., Koltai, H., 2001. Alterations in the levels of glycogen and glycogen synthase transcripts during desiccation in the insect-killing nematode Steinernema feltiae IS-6. J. Parasitol. 87, 725–732. Gassmann, A.J., Stock, P., Tabashnik, B.E., Singer, M.S., 2010. Tritrophic effects of host plants on an herbivore–pathogen interaction. Ann. Entomol. Soc. Am. 103, 371– 378. Gaugler, R., 2002. Preface. In: Gaugler, R. (Ed.), Entomopathogenic Nematology. CAB International, Wallingford, UK, pp. IX–X. Gaugler, R., Bednarek, A., Campbell, J.F., 1992. Ultraviolet inactivation of heterorhabditid and steinernematid nematodes. J. Invertebr. Pathol. 59, 155– 160. Gaugler, R., Brown, I., Shapiro-Ilan, D., Atwa, A., 2002. Automated technology for in vivo mass production of entomopathogenic nematodes. Biol. Control 24, 199– 206. Gaugler, R., Grewal, P., Kaya, H.K., Smith-Fiola, D., 2000. Quality assessment of commercially produced entomopathogenic nematodes. Biol. Control 17, 100– 109. Gaugler, R., Kaplan, B., Alvarado, C., Montoya, J., Ortega, M., 1983. Assessment of Bacillus thuringiensis serotype 14 and Steinernema feltiae (Nematoda: Steinernematidae) for control of the Simulium vectors of onchocerciasis in Mexico. Entomophaga 28, 309–315. Gaugler, R., LeBeck, L., Nakagaki, B., Boush, G.M., 1980. Orientation of the entomogenous nematode Neoaplectana carpocapsae to carbon dioxide. Environ. Entomol. 9, 649–652. Georgis, R., Dunlop, D.B., Grewal, P.S., 1995. Formulation of entomopathogenic nematodes. In: Hall, F.R., Barry, J.W. (Eds.), Biorational Pest Control Agents: Formulation and Delivery. American Chemistry Society, Washington, DC, pp. 197–205. Georgis, R., Gaugler, R., 1991. Predictability of biological control using entomopathogenic nematodes. J. Econ. Entomol. 84, 713–720. Georgis, R., Hague, N.G.M., 1982. Interactions between Neoaplectana carpocapsae (Nematoda) and Olesicampe monticola, a parasitoid of the larch sawfly Cephalcia lariciphila biological control. Key Rep. Human Animal Physiol. 10, 617. Georgis, R., Koppenhöfer, A.M., Lacey, L.A., Bélair, G., Duncan, L.W., Grewal, P.S., Samish, M., Tan, L., Torr, P., Van Tol, R.W.H.M., 2006. Successes and failures in the use of parasitic nematodes for pest control. Biol. Control 38, 103–123. Georgis, R., Poinar Jr., G.O., 1983a. Effect of the soil texture on the distribution and infectivity of Neoaplectana glaseri (Nematoda: Steinernematidae). J. Nematol. 15, 329–332. Georgis, R., Poinar Jr., G.O., 1983b. Vertical migration of Heterorhabditis nematophilus and H. heliothidis (Nematoda: Heterorhabditidae) in sandy loam soil. J. Nematol. 15, 652–654. Georgis, R., Poinar Jr., G.O., 1984. Greenhouse control of black vine weevil Otiorhynchus sulcatus (Coleoptera: Curculionidae). Environ. Entomol. 13, 1138–1140. Glänzel, W., Schubert, A., 2004. Analysing scientific networks through coauthorship. In: Moed, H.F., Glänzel, W., Schmoch, U. (Eds.), Handbook of Quantitative Science and Technology Research. Kluwer Academic Publishers, The Netherlands, pp. 257–276. Glaser, R.W., 1940. The bacteria-free culture of a nematode parasite. Proc. Soc. Exp. Biol. Med. 43, 512–514.

120

E. San-Blas / Biological Control 66 (2013) 102–124

Glaser, R.W., McCoy, E.E., Girth, H.B., 1940. The biology and economic importance of a nematode parasitic in insects. J. Parasitol. 27, 123–126. Glaser, R.W., McCoy, E.E., Girth, H.B., 1941. The biology and culture of Neoaplectana chresima, a new nematode parasitic in insects. J. Parasitol. 27, 123–126. Glazer, I., Alekseev, E., Samish, M., 2001. Factors affecting the virulence of entomopathogenic nematodes to engorged female Boophilus annulatus ticks. J. Parasitol. 87, 808–812. Glazer, I., Klein, M., Navon, A., Nakache, Y., 1992. Comparison of efficacy of entomopathogenic nematodes combined with antidesiccants applied by canopy sprays against three cotton pests (Lepidoptera: Noctuidae). J. Econ. Entomol. 85, 1636–1646. Gordon, R., Chippett, J., Tilley, J., 1996. Effects of two carbamates on infective juveniles of Steinernema carpocapsae AII strain and Steinernema feltiae Umea strain. J. Nematol. 28, 310–317. Götz, P., Boman, A., Boman, H.G., 1981. Interaction between insect immunity and an insect-pathogenic nematode with symbiotic bacteria. Proc. R. Soc. Lond. B 212, 334–350. Grewal, P.S., 2000a. Anhydrobiotic potential and long-term storage of entomopathogenic nematodes (Rhabditida: Steinernematidae). Int. J. Parasitol. 30, 995–1000. Grewal, P.S., 2000b. Enhanced ambient storage stability of an entomopathogenic nematode through anhydrobiosis. Pest Manag. Sci. 56, 401–406. Grewal, P.S., Gaugler, R., Lewis, E.E., 1993. Host recognition behavior by entomopathogenic nematodes during contact with insect gut content. J. Parasitol. 79, 495–503. Grewal, P.S., Jagdale, G.B., 2002. Enhanced trehalose accumulation and desiccation survival of entomopathogenic nematodes through cold preacclimation. Biocontrol Sci. Tech. 12, 533–545. Grewal, P.S., Martin, W.R., Miller, R.W., Lewis, E.E., 1997. Suppression of plantparasitic nematode populations in turfgrass by application of entomopathogenic nematodes. Biocontrol Sci. Tech. 7, 393–400. Grewal, P.S., Power, K.T., Shetlar, D.J., 2001. Neonicotinoid insecticides alter diapause behavior and survival of overwintering white grubs (Coleoptera: Scarabaeidae). Pest Manag. Sci. 57, 852–857. Grewal, P.S., Selvan, S., Lewis, E.E., Gaugler, R., 1993. Male insect-parasitic nematodes: a colonizing sex. Experientia 49, 605–608. Grewal, P.S., Wang, X., Taylor, R.A.J., 2002. Dauer juvenile longevity and stress tolerance in natural populations of entomopathogenic nematodes: is there a relationship? Int. J. Parasitol. 32, 717–725. Grewal, S.K., Grewal, P.S., Gaugler, R., 1995. Endophytes of fescue grasses enhance susceptibility of Popillia japonica larvae to an entomopathogenic nematode. Entomol. Exp. Appl. 74, 219–224. Griffin, C.T., Downes, M.J., 1991. Low temperature activity in Heterorhabditis sp. (Nematoda: Heterorhabditidae). Nematologica 37, 83–91. Griffin, C.T., Downes, M.J., Block, W., 1990. Tests of Antarctic soils for insect parasitic nematodes. Antarct. Sci. 2, 221–222. Griffin, C.T., Finnegan, M.M., Downes, M.J., 1994. Environmental tolerances and the dispersal of Heterorhabditis: survival and infectivity of European Heterorhabditis following prolonged immersion in seawater. Fund. Appl. Nematol. 17, 415–442. Gray, P.A., Johnson, D.T., 1983. Survival of the nematode Neoaplectana carpocapsae in relation to soil temperature, moisture and time. J. Georgia Entomol. Soc. 18, 454–460. Gullino, M.L., Kuipjers, L.A.M., 1994. Political and social implications of managing plants diseases with restricted fungicides in Europe. Annu. Rev. Phytopathol. 32, 559–579. Han, R.C., 1996. The effects of the inoculum size on yield of Steinernema carpocapsae and Heterorhabditis bacteriophora in liquid culture. Nematologica 42, 546–553. Han, R., Cao, L., Liu, X., 1993. Effects on inoculum size, temperature and time on in vitro production of Steinernema carpocapsae agriotos. Nematologica 39, 366– 375. Hao, Y.-J., Montiel, R., Abubucker, S., Mitreva, M., Simões, N., 2010. Transcripts analysis of the entomopathogenic nematode Steinernema carpocapsae induced in vitro with insect haemolymph. Mol. Biochem. Parasitol. 169, 79–86. Hara, A.H., Kaya, H.K., 1982. Effects of selected insecticides and nematicides on the in vitro development of the entomogenous nematode Neoaplectana carpocapsae. J. Nematol. 14, 486–491. Hass, B., Downes, M.J., Griffin, C.T., 2002. Persistence of four Heterorhabditis spp. isolates in soil: role of lipid reserves. J. Nematol. 34, 151–158. Hayes, A.E., Fitzpatrick, S.M., Webster, J.M., 1999. Infectivity, distribution, and persistence of the entomopathogenic nematode Steinernema carpocapsae all strain (Rhabditida: Steinernematidae) applied by sprinklers or boom sprayer to dry-pick cranberries. J. Econ. Entomol. 92, 539–546. Hazir, S., Stock, S.P., Keskin, N., 2003. A new entomopathogenic nematode, Steinernema anatoliense n. sp. (Rhabditida: Steinernematidae), from Turkey. Syst. Parasitol. 55, 211–220. Head, J., Walters, K.F.A., Langton, S., 2000. The compatibility of the entomopathogenic nematode, Steinernema feltiae, and chemical insecticides for the control of the South American leafminer, Liriomyza huidobrensis. Biocontrol 45, 345–353. Hebert Tran, E.E., Andersen, A.W., Goodrich-Blair, H., 2009. CpxRA Influences Xenorhabdus nematophila colonization initiation and outgrowth in Steinernema carpocapsae nematodes through regulation of the nil locus. Appl. Environ. Microbiol. 75, 4007–4014. Herbert Tran, E.E., Cowles, K.N., Goodrich-Blair, H., 2007. CpxRA regulates mutualism and pathogenesis in Xenorhabdus nematophila. Appl. Environ. Microbiol. 73, 7826–7836.

Henderson, D.R., Riga, E., Ramirez, R.A., Wilson, J., Snyder, W.E., 2009. Mustard biofumigation disrupts biological control by Steinernema spp. nematodes in the soil. Biol. Control 48, 316–322. Henry, M., Béguin, M., Requier, F., Rollin, O., Odoux, J.-F., Aupinel, P., Aptel, J., Tchamitchian, S., Decourtye, A., 2012. A common pesticide decreases foraging success and survival in honey bees. Science 336, 348–350. Hiltpold, I., Turlings, T.C.J., 2008. Belowground chemical signalling in maize: when simplicity rhymes with efficiency. J. Chem. Ecol. 34, 628–635. Hominick, W.M., Briscoe, B.R., 1990a. Occurrence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in British soils. Parasitology 100, 295–302. Hominick, W.M., Briscoe, B.R., 1990b. Survey of 15 sites over 28 months for entomopathogenic nematodes (Rhabditida: Steinernematidae). Parasitology 100, 289–294. Hominick, W.M., Briscoe, B.R., Del Pino, F.G., Heng, J., Hunt, D.J., Kozodoy, E., Mracek, Z., Nguyen, K.B., Reid, A.P., Spiridonov, S., Stock, P., Sturhan, D., Waturu, C., Yoshida, M., 1997. Biosystematics of entomopathogenic nematodes: current status, protocols and definitions. J. Helminthol. 71, 271–298. Ireson, J.E., Miller, L.A., 1983. Susceptibility of the collembolan Sminthurus viridis to the insect parasitic nematodes Neoaplectana bibionis and Heterorhabditis heliothidis. Entomol. Exp. Appl. 34, 342–343. Islas-López, M.A., Sanjuan-Galindo, R., Rodríguez-Hernández, A.I., ChavarríaHernández, N., 2005. Monoxenic production of the entomopathogenic nematode Steinernema carpocapsae using culture media containing agave juice (aguamiel) from Mexican maguey-pulquero (Agave spp.). Effects of the content of nitrogen, carbohydrates and fat on infective juveniles. Appl. Microbiol. Biotechnol. 68, 91–97. Jaffee, B.A., Strong, D.R., 2005. Strong bottom-up and weak top-down effects in soil: nematode-parasitized insects and nematode-trapping fungi. Soil Biol. Biochem. 37, 1011–1021. Jagdale, G.B., Gordon, R., 1997. Effect of temperature on the composition of fatty acids in total lipids and phospholipids of entomopathogenic nematodes. J. Therm. Biol. 22, 245–251. Jagdale, G.B., Grewal, P.S., 2003. Acclimation of entomopathogenic nematodes to novel temperatures: trehalose accumulation and the acquisition of thermotolerance. Int. J. Parasitol. 33, 145–152. Jagdale, G.B., Grewal, P.S., 2008. Influence of the entomopathogenic nematode Steinernema carpocapsae infected host cadavers or their extracts on the foliar nematode Aphelenchoides fragariae on Hosta in the greenhouse and laboratory. Biol. Control 44, 13–23. Jagdale, G.B., Grewal, P.S., Salminen, S.O., 2005. Both heat-shock and cold-shock influence trehalose metabolism in an entomopathogenic nematode. J. Parasitol. 91, 988–994. Jagdale, G.B., Kamoun, S., Grewal, P.S., 2009. Entomopathogenic nematodes induce components of systemic resistance in plants: biochemical and molecular evidence. Biol. Control 51, 102–109. Jansson, R.K., Lecrone, S.H., 1994. Application methods for entomopathogenic nematodes (Rhabditida: Heterorhabditidae): aqueous suspensions versus infected cadavers. Florida Entomol. 77, 281–284. Jansson, R.K., Lecrone, S.H., Gaugler, R., 1993. Field efficacy and persistence of entomopathogenic nematodes (Rhabditida: Steinernematidae, Heterorhabditidae) for control of sweetpotato weevil (Coleoptera: Apionidae) in southern Florida. J. Econ. Entomol. 86, 1055–1063. Jaworska, M., Gorczyca, A., Sepiol, J., Szeliga, E., Tomasik, P., 1997. Metal–metal interactions in biological systems. Water Air Soil Pollut. 93, 213–223. Jaworska, M., Ropek, D., 1994. Influence of host-plant on the susceptibility of Sitona lineatus L. (Col., Curculionidae) to Steinernema carpocapsae Weiser. J. Invertebr. Pathol. 64, 96–99. Jaworska, M., Sepiol, J., Tomasik, P., 1996. Effect of metal ions under laboratory conditions on the entomopathogenic Steinernema carpocapsae (Rhabditida: Steinernematidae). Water Air Soil Pollut. 88, 331–341. Jaworska, M., Tomasik, P., 1999. Metal–metal interactions in biological systems. Part VI. Effect of some metal ions on mortality, pathogenicity and reproductivity of Steinernema carpocapsae and Heterorhabditis bacteriophora entomopathogenic nematodes under laboratory conditions. Water Air Soil Pollut. 110, 181–194. Jess, S., Bingham, J.F.W., 2004. Biological control of sciarid and phorid pests of mushroom with predatory mites from the genus Hypoaspis (Acari: Hypoaspidae) and the entomopathogenic nematode Steinernema feltiae. Bull. Entomol. Res. 94, 159–167. Jin, Y.-L., Han, R.-C., Cong, B., 2004. Effects of application parameters and adjuvants on the foliar survival and persistence of entomopathogenic nematode Steinernema carpocapsae ALL strain on cabbages. Insect Sci. 11, 99–112. Jing, Y., Toubarro, D., Hao, Y., Simões, N., 2010. Cloning, characterisation and heterologous expression of an astacin metalloprotease, Sc-AST, from the entomoparasitic nematode Steinernema carpocapsae. Mol. Biochem. Parasitol. 174, 101–108. Kain, D.P., Agnello, A.M., 1999. Pest status of American plum borer (Lepidoptera: Pyralidae) and fruit tree borer control with synthetic insecticides and entomopathogenic nematodes in New York State. J. Econ. Entomol. 92, 193– 200. Kakouli-Duarte, T., Hague, N.G.M., Otto, A.A., 1993. Evaluation of the entomopathogenic nematode Steinernema carpocapsae against the black vine weevil Otiorhynchus sulcatus. Ann. Appl. Biol. 122, 190–192. Kakouli-Duarte, T., Labuschagne, L., Hague, N.G.M., 1997. Biological control of black vine weevil, Otiorhynchus sulcatus (Coleoptera: Curculionidae) with

E. San-Blas / Biological Control 66 (2013) 102–124 entomopathogenic nematodes (Nematoda: Rhabditida). Ann. Appl. Biol. 131, 11–27. Kanagy, J.M.N., Kaya, H.K., 1996. The possible role of marigold root and a-terthienyl in mediating host-finding by steinernematid nematodes. Nematologica 42, 220–231. Kaya, H.K., 1984. Effect of the entomogenous nematode Neoaplectana carpocapsae on the tachinid parasite Compsilura concinnata (Diptera: Tachinidae). J. Nematol. 16, 9–13. Kaya, H.K., Aguillera, M.M., Alumai, A., Choo, H.Y., De La Torre, M., Fodor, A., Ganguly, S., Haz, S., Lakatos, T., Pye, V., Wilson, M., Yamanaka, S., Yang, H., Ehlers, R.-U., 2006. Status of entomopathogenic nematodes and their symbiotic bacteria from selected countries or regions of the world. Biol. Control 38, 134– 155. Kaya, H.K., Burlando, T.M., 1989. Infectivity of Steinernema feltiae in fenamiphostreated sand. J. Nematol. 21, 434–436. Kaya, H.K., Burlando, T.M., Choo, H.Y., Thurston, G.S., 1995. Integration of entomopathogenic nematodes with Bacillus thuringiensis or pesticidal soap for control of insect pests. Biol. Control 5, 432–441. Kaya, H.K., Gaugler, R., 1993. Entomopathogenic nematodes. Annu. Rev. Entomol. 38, 181–206. Kaya, H.K., Klein, M.G., Burlando, T.M., 1993. Impact of Bacillus popilliae, Rickettsiella popilliae and entomopathogenic nematodes on a population of the scarabaeid, Cyclocephala hirta. Biocontrol Sci. Tech. 3, 443–453. Kaya, H.K., Mannion, C.M., Burlando, T.M., Nelsen, C.E., 1987. Escape of Steinernema feltiae from alginate capsules containing tomato seeds. J. Nematol. 19, 287–291. Kaya, H.K., Nelsen, C.E., 1985. Encapsulation of steinernematid and heterorhabditid nematodes with calcium alginate: a new approach for insect control and other applications. Environ. Entomol. 14, 572–574. Kermarrec, A., Mauleon, H., 1985. Potential noxiousness of the entomogenous nematode Neoaplectana carpocapsae Weiser to the Antilan toad Bufo marinus L. Mededelingen van de Faculteit Landbouwwetenschappen Rijksuniversiteit 50, 831–838. Klingler, J., 1988. Investigations on the parasitism of Otiorhynchus salicicola and O. sulcatus [Col.: Curculionidae] by Heterorhabditis sp. [Nematoda]. Entomophaga 33, 325–333. Kocan, K.M., Pidherney, M.S., Blouin, E.F., Claypool, P.L., Samish, M., Glazer, I., 1998. Interaction of entomopathogenic nematodes (Steinernematidae) with selected species of ixodid ticks (Acari: Ixodidae). J. Med. Entomol. 35, 514–520. Koppenhöfer, A.M., Baur, M.E., Stock, S.P., Choo, H.Y., Chinnasri, B., Kaya, H.K., 1997. Survival of entomopathogenic nematodes within host cadavers in dry soil. Appl. Soil Ecol. 6, 231–240. Koppenhöfer, A.M., Brown, I.M., Gaugler, R., Grewal, P.S., Kaya, H.K., Klein, M.G., 2010. Synergism of entomopathogenic nematodes and imidacloprid against white grubs: greenhouse and field evaluation. Biol. Control 19, 245–251. Koppenhöfer, A.M., Choo, H.Y., Kaya, H.K., Lee, D.W., Gelernter, W.D., 1999. Increased field and greenhouse efficacy against scarab grub with a combination of an entomopathogenic nematode and Bacillus thuringiensis. Biol. Control 14, 37–44. Koppenhöfer, A.M., Fuzy, E.M., 2003. Effects of turfgrass endophytes (Clavicipitaceae: Ascomycetes) on white grub (Coleoptera: Scarabaeidae) control by the entomopathogenic nematode Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae). Environ. Entomol. 32, 392–396. Koppenhöfer, A.M., Fuzy, E.M., 2008. Early timing and new combinations to increase the efficacy of neonicotinoid–entomopathogenic nematode (Rhabditida: Heterorhabditidae) combinations against white grubs (Coleoptera: Scarabaeidae). Pest Manag. Sci. 64, 725–735. Koppenhöfer, A.M., Ganguly, S., Kaya, H.K., 2000a. Ecological characterization of Steinernema monticolum, a cold-adapted entomopathogenic nematode from Korea. Nematology 2, 407–416. Koppenhöfer, A.M., Grewal, P.S., Kaya, H.K., 2000b. Synergism of imidacloprid and entomopathogenic nematodes against white grubs: the mechanism. Entomol. Exp. Appl. 94, 283–293. Koppenhöfer, A.M., Jaffe, B.A., Muldoon, A.E., Strong, D.R., Kaya, H.K., 1996. Effect of nematode-trapping fungi on an entomopathogenic nematode originating from the same field site in California. J. Invertebr. Pathol. 68, 246–252. Koppenhöfer, A.M., Kaya, H.K., 1997. Additive and synergistic interaction between entomopathogenic nematodes and Bacillus thuringiensis for scarab grub control. Biol. Control 8, 131–137. Koppenhöfer, A.M., Kaya, H.K., 1998. Synergism of imidacloprid and an entomopathogenic nematode: a novel approach to white grub (Coleoptera: Scarabaeidae) control in turfgrass. J. Econ. Entomol. 91, 618–623. Kung, S., Gaugler, R., Kaya, H.K., 1990. Influence of soil pH and oxygen on persistence of Steinernema spp. J. Nematol. 22, 440–445. Kunkel, B.A., Grewal, P.S., 2003. Endophyte infection in perennial ryegrass reduces the susceptibility of black cutworm to an entomopathogenic nematode. Entomol. Exp. Appl. 107, 95–104. Kushida, T., Mamiya, Y., Mitsuhashi, J., 1987. Pathogenicity of the newly detected Steinernema sp. (Nematoda) to scarabaeid larvae injurious to tree seedlings. Jpn. J. Appl. Entomol. Zool. 31, 144–149 [Abstr.]. Lacey, L.A., Unruh, T.R., Headrick, H.L., 2003. Interactions of two idiobiont parasitoids (Hymenoptera: Ichneumonidae) of codling moth (Lepidoptera: Tortricidae) with the entomopathogenic nematode Steinernema carpocapsae (Rhabditida: Steinernematidae). J. Invertebr. Pathol. 83, 230–239. Łaczynski, A., Dierickx, W., De Moor, A., 2007. The effect of agitation system, temperature of the spray liquid, nematode concentration, and air injection on the viability of Heterorhabditis bacteriophora. Biocontrol Sci. Tech. 17, 841–851.

121

Lamondia, J.A., Cowles, R.S., 2002. Effect of entomogenic nematodes and Trichoderma harzianum on the strawberry black root rot pathogens Pratylenchus penetrans and Rhizoctonia fragariae. J. Nematol. 34, 351–357. Lara, J.C., Dolinski, C., De Sousa, E.F., Daher, R.F., 2008. Effect of mini-sprinkler irrigation system on Heterorhabditis baujardi LPP7 (Nematoda: Heterorhabditidae) infective juvenile. Sci. Agric. 65, 433–437. Leger, C., Riga, E., 2009. Evaluation of marigolds and entomopathogenic nematodes for control of the cabbage maggot Delia radicum. J. Sustain. Agric. 33, 128–141. Leppla, N.C., Frank, J.H., Adjei, M.B., Vicente, N.E., 2007. Management of pest mole crickets in Florida and Puerto Rico with a nematode and parasitic wasp. Florida Entomol. 90, 229–233. Lewis, E.E., Campbell, J., Griffin, C., Kaya, H., Peters, A., 2006. Behavioral ecology of entomopathogenic nematodes. Biol. Control 38, 66–79. Lewis, E.E., Gaugler, R., 1994. Entomopathogenic nematode (Rhabditida: Steinernematidae) sex ratio relates to foraging strategy. J. Invertebr. Pathol. 64, 238–242. Lewis, E.E., Gaugler, R., Harrison, A., 1992. Entomopathogenic nematode hostfinding: response to contact cues by cruise and ambush foragers. Parasitology 105, 309–315. Lewis, E.E., Gaugler, R., Harrison, R., 1993. Response of cruiser and ambusher entomopathogenic nematodes (Steinernematidae) to host volatile cues. Can. J. Zool. 71, 765–769. Lewis, E.E., Shapiro-Ilan, D.I., 2002. Host cadavers protect entomopathogenic nematodes during freezing. J. Invertebr. Pathol. 81, 25–32. Liu, N.X., Zhang, Z.Y., 1982. Entomopathogenic nematodes in the soil. Nat. Enemies Insects 4, 50–54. Lola-Luz, T., Downes, M., 2007. Biological control of black vine weevil Otiorhynchus sulcatus in Ireland using Heterorhabditis megidis. Biol. Control 40, 314–319. Lopez-Robles, J., Hague, N.G.M., 2003. Evaluation of entomopathogenic nematodes against the stem nematode Ditylenchus dipsaci in garlic. Tests Agrochem. Cultiv. 24, 24–25. Loya, L.J., Hower Jr., A.A., 2002. Population dynamics, persistence, and efficacy of the entomopathogenic nematode Heterorhabditis bacteriophora (Oswego strain) in association with the clover root Curculio (Coleoptera: Curculionidae) in Pennsylvania. Environ. Entomol. 31, 1240–1250. Lunau, S., Stoessel, S., Schmidt-Peisker, A.J., Ehlers, R.-U., 1993. Establishment of monoxenic inocula for scaling up in vitro cultures of the entomopathogenic nematodes Steinernema spp. and Heterorhabditis spp. Nematologica 39, 385– 399. Lynch, L.A., Thomas, M.B., 2000. Nontarget effects in the biocontrol of insects with insects, nematodes, and microbial agents: the evidence. Biocontrol 21, 117N– 130N. Madikhanov, M., 1982. Embryogenesis of the entomopathogenic nematode Neoaplectana agriotos. Zoologicheskii Zhurnal 61, 500–506. Mahmoud, M.F., 2007. Combining the botanical insecticides NSK extract, NeemAzal T 5%, Neemix 4.5% and the entomopathogenic nematode Steinernema feltiae Cross N 33 to control the peach fruit fly, Bactrocera zonata (Saunders). Plant Prot. Sci. 43, 19–25. Mamiya, Y., 1988. Steinernema kushidai n. sp. (Nematoda: Steinernematidae) associated with scarabaeid beetle larva from Shizuoka Japan. Appl. Entomol. Zool. 23, 313–320. Mason, J.M., Matthews, G.A., Wright, D.J., 1998a. Appraisal of spinning disc technology for the application of entomopathogenic nematodes. Crop Protect. 17, 453–461. Mason, J.M., Matthews, G.A., Wright, D.J., 1998b. Screening and selection of adjuvants for the spray application of entomopathogenic nematodes against a foliar pest. Crop Protect. 17, 463–470. Matha, V., Mráceˇk, Z., 1984. Changes in haemocyte counts in Galleria mellonella (L.) (Lepidoptera: Galleriidae) larvae infected with Steinernema sp. (Nematoda: Steinernematidae). Nematologica 30, 86–89. Mauleon, H., Barré, N., Panoma, S., 1993. Pathogenicity of 17 isolates of entomophagous nematodes (Steinernematidae and Heterorhabditidae) for the ticks Amblyomma variegatum (Fabricius), Boophilus microplus (Canestrini) and Boophilus annulatus (Say). Exp. Appl. Acarol. 17, 831–838. Mbata, G.N., Shapiro-Ilan, D.I., 2010. Compatibility of Heterorhabditis indica (Rhabditida: Heterorhabditidae) and Habrobracon hebetor (Hymenoptera: Braconidae) for biological control of Plodia interpunctella (Lepidoptera: Pyralidae). Biol. Control 54, 75–82. McCoy, C.W., Stuart, R.J., Duncan, L.W., Nguyen, K., 2002. Field efficacy of two commercial preparations of entomopathogenic nematodes against larvae of Diaprepes abbreviatus (Coleoptera: Curculionidae) in alfisol type soil. Florida Entomol. 85, 537–544. Molina-Acevedo, J.P., Samuels, R.I., Ribeiro-Machado, I., Dolinski, C., 2007. Interactions between isolates of the entomopathogenic fungus Metarhizium anisopliae and the entomopathogenic nematode Heterorhabditis bacteriophora JPM4 during infection of the sugar cane borer Diatraea saccharalis (Lepidoptera: Pyralidae). J. Invertebr. Pathol. 96, 187–192. Molina, J.P., Dolinski, C., Souza, R.M., Lewis, E.E., 2007. Effect of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) on Meloidogyne mayaguensis Rammah and Hirschmann (Tylenchida: Meloidoginidae) infection in tomato plants. J. Nematol. 39, 338–342. Molina-Ochoa, J., Nguyen, K.B., González-Ramírez, M., Quintana-Moreno, M.G., Lezama-Gutiérrez, R., Foster, J.E., 2009. Steinernema diaprepesi (Nematoda: Steinernematidae): its occurrence in western Mexico and susceptibility of engorded cattle ticks Boophilus microplus (Acari: Ixodidae). Florida Entomol. 92, 661–663.

122

E. San-Blas / Biological Control 66 (2013) 102–124

Molyneux, A.S., 1985. Survival of infective juveniles of Heterorhabditis spp., and Steinernema spp. (Nematoda: Rhabitida) at various temperatures and their subsequent infectivity for insects. Rev. Nématol. 8, 165–170. Morales-Rodriguez, A., Peck, D.C., 2009. Synergies between biological and neonicotinoid insecticides for the curative control of the white grubs Amphimallon majale and Popillia japonica. Biol. Control 5, 169–180. Moureaux, N., Karjalainen, T., Givaudan, A., Bourlioux, P., Boemare, N., 1995. Biochemical characterization and agglutinating properties of Xenorhabdus nematophilus F1 fimbriae. Appl. Environ. Microbiol. 61, 2707–2712. Moyle, P.L., Kaya, H.K., 1981. Dispersal and infectivity of the entomogenous nematode, Neoaplectana carpocapsae Weiser (Rhabditida: Steinernematidae), in sand. J. Nematol. 13, 295–300. Mrácˇek, Z., 1977. Steinernema kraussei, a parasite of the body cavity of the sawfly, Cephaleia abietis, in Czechosiovakia. J. Invertebr. Pathol. 30, 87–94. Mrácˇek, Z., Becˇvárˇ, S., Kindlmann, P., Jersáková, J., 2005. Habitat preference for entomopathogenic nematodes, their insect hosts and new faunistic records for the Czech Republic. Biol. Control 34, 27–37. Mrácˇek, Z., Spitzer, K., 1983. Interaction of the predators and parasitoids of the sawfly, Cephalcia abietis (Pamphilidae: Hymenoptera) with its nematode Steinernema kraussei. J. Invertebr. Pathol. 42, 397–399. Mrácˇek, Z., Weiser, J., Arteaga, E., 1984. Scanning electron microscope study of Heterorhabditis heliothidis (Nematoda: Heterorhabditidae). Nematologica 30, 112–114. National Research Council, 1993. Pesticides in the diets of infants and children. National Academy Press, USA, pp. 408. Navon, A., Keren, S., Salame, L.A., Glazer, I., 1998. An edible-to-insects calcium alginate gel as a carrier for entomopathogenic nematodes. Biocontrol Sci. Technol. 8, 429–437. Newman, M.E.J., 2004. Coauthorship networks and patterns of scientific collaboration. Proc. Nat. Acad. Sci. 101, 5200–5205. Nickle, W.R., Shapiro, M., 1992. Use of a stilbene brightener, Tinopal LPW, as a radiation protectant for Steinernema carpocapsae. J. Nematol. 24, 371–373. Nickle, W.R., Shapiro, M., 1994. Effects of eight brighteners as solar radiation protectants for Steinernema carpocapsae, AII strain. Suppl. J. Nematol. 26 (4S), 782–784. Nielsen, O., Philipsen, H., 2004. Recycling of entomopathogenic nematodes in Delia radicum and in other insects from cruciferous crop. Biocontrol 49, 285– 294. Nishimatsu, T., Jackson, J.J., 1998. Interaction of insecticides, entomopathogenic nematodes, and larvae of the western corn root worm (Coleoptera: Chrysomelidae). J. Econ. Entomol. 91, 410–418. Nguyen, K.B., Smart, G.C., 1990. Vertical dispersal of Steinernema scaptericsi. J. Nematol. 22, 574–578. Oestergaard, J., Belau, C., Strauch, O., Ester, A., Van Rozen, K., Ehlers, R.-U., 2006. Biological control of Tipula paludosa (Diptera: Nematocera) using entomopathogenic nematodes (Steinernema spp.) and Bacillus thuringiensis subsp. Israelensis. Biol. Control 39, 525–531. Ogura, N., Haraguchi, N., 1994. Artificial media for xenic culture of Steinernema kushidai (Nematoda: Steinernematidae). Nematologica 40, 613–616. Patel, M.N., Perry, R.N., Wright, D.J., 1997a. Desiccation survival and water contents of entomopathogenic nematodes, Steinernema spp. (Rhabditida: Steinernematidae). Int. J. Parasitol. 27, 61–70. Patel, M.N., Stolinski, M., Wright, D.J., 1997b. Neutral lipids and the assessment of infectivity in entomopathogenic nematodes: observations on four Steinernema species. Parasitology 114, 489–496. Patel, M.N., Wright, D.J., 1997a. Fatty acid composition of neutral lipid energy reserves in infective juveniles of entomopathogenic nematodes. Comp. Biochem. Physiol. Part B 118, 341–348. Patel, M.N., Wright, D.J., 1997b. Glycogen: its importance in the infectivity of aged juveniles of Steinernema carpocapsae. Parasitology 114, 591–596. Patel, M.N., Wright, D.J., 1997c. Phospholipids and their fatty acids in infective juveniles of entomopathogenic steinernematid nematodes. Comp. Biochem. Physiol. Part B 118, 649–657. Pereault, R.J., Whalon, M.E., Alston, D.G., 2009. Field efficacy of entomopathogenic fungi and nematodes targeting caged last-Instar plum curculio (Coleoptera: Curculionidae) in Michigan cherry and apple orchards. Environ. Entomol. 38, 1126–1134. Pérez, E.E., Lewis, E.E., 2002. Use of entomopathogenic nematodes to suppress Meloidogyne incognita on greenhouse tomatoes. J. Nematol. 34, 171–174. Pérez, E.E., Lewis, E.E., 2004. Suppression of Meloidogyne incognita and Meloidogyne hapla with entomopathogenic nematodes on greenhouse peanuts and tomatoes. Biol. Control 30, 336–341. Pérez, E.E., Lewis, E.E., Shapiro-Ilan, D.I., 2003. Impact of the host cadaver on survival and infectivity of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) under desiccating conditions. J. Invertebr. Pathol. 82, 111–118. Perry, R.N., Hominick, W.M., Beane, J., Briscoe, B., 1997. Effect of the entomopathogenic nematodes, Steinernema feltiae and S. carpocapsae, on the potato cyst nematode, Globodera rostochiensis, in pot trials. Biocontrol Sci. Tech. 8, 175–180. Pizano, M.A., Aguillera, M.M., Monteiro, A.R., Ferraz, L.C.C.B., 1985. Incidence of Neoaplectana glaseri Steiner, 1929 (Nematoda: Steinernematidae) parasitizing Migdolus fryanus (Westwood, 1863) (Col.: Cerambycidae). Entomol. Newsletter 17, 9–10. Poinar Jr., G.O., 1972. Nematodes as facultative parasites of insects. Annu. Rev. Entomol. 17, 103–122.

Poinar Jr., G.O., 1989. Non-insect hosts for the entomogenous rhabditoid nematodes Neoaplectana (Steinernematidae) and Heterorhabditis (Heterorhabditidae). Rev. Nématol. 12, 423–428. Poinar Jr., G.O., 1985. Spermatogenesis in the insect-parasite nematode, Heterorhabditis bacteriophora Poinar (Heterorhabditidae: Rhabditida). Rev. Nématol. 8, 357–367. Poinar Jr., G.O., Hom, A., 1986. Survival and horizontal movement of infective stage Neoaplectana carpocapsae in the field. J. Nematol. 18, 34–36. Poinar Jr., G.O., Jansson, H., 1986a. Infection of Neoaplectana and Heterorhabditis (Rhabditida: Nematoda) with the predatory fungus, Monacrosporium ellipsosporumI and Arthrobotrys oligospora (Moniliales: Deuteromycetes). Rev. Nématol. 9, 241–244. Poinar Jr., G.O., Jansson, H., 1986b. Susceptibility of Neaoplectana spp. and Heterorhabditis heliothidis to the endoparasitic fungus Drechmeria coniospora. J. Nematol. 18, 225–230. Poinar Jr., G.O., Karunakar, G.K., David, H., 1992. Heterorhabditis indicus n. sp. (Rhabditida: Nematoda) from India: separation of Heterorhabditis spp. by infective juveniles. Fund. Appl. Nematol. 15, 467–472. Poinar Jr., G.O., Leutenegger, R., 1968. Anatomy of the infective juveniles of Neoaplectana carpocapsae Weiser (Steinernematidae: Nematoda). J. Parasitol. 54, 340–350. Poinar Jr., G.O., Linhartdt, K., 1971. The re-isolation of Neoaplectana bibionis Bovien (Nematoda) from Danish bibionids (Diptera) and their possible use as biological control agents. Entomologia Scandinavica 2, 301–303. Poinar Jr., G.O., Mrácˇek, Z., Doucet, M.M.A., 1988. A re-examiation of Neoaplectana rara Doucet, 1986. (Steinernematidae: Rhabditida). Rev. Nématol. 11, 447–449. Poinar Jr., G.O., Paff, M., 1985. Laboratory infection of terrestrial isopods (Crustacea: Isopoda) with neoaplectanid and heterorhabditid nematodes (Rhabditida: Nematoda). J. Invertebr. Pathol. 45, 24–27. Poinar Jr., G.O., Thomas, G.M., 1985. Laboratory infection of spiders and harvestmen (Arachnida: Araneae and Opiliones) with Neoaplectana and Heterorhabditis nematodes (Rhabditoidea). J. Arachnol. 13, 297–302. Poinar Jr., G.O., Thomas, G.M., Lighthart, B., 1990. Bioassay to determine the effect of commercial preparations of Bacillus thuringiensis on entomogenous rhabditoid nematodes. Agric. Ecosyst. Environ. 30, 195–202. Poinar Jr., G.O., Thomas, G.M., Lin, K.C., Mookerjee, P., 1985. Feasibility of embedding parasitic nematodes in hydrogels for insect control. IRCS Med. Sci. 13, 754–755. Polavarapu, S., Koppenhöfer, A.M., Barry, J.D., Holdcraft, R.J., Fuzy, E.M., 2007. Entomopathogenic nematodes and neonicotinoids for remedial control of oriental beetle, Anomala orientalis (Coleoptera: Scarabaeidae), in highbush blueberry. Crop Protect. 26, 1266–1271. Popiel, I., Grove, D.L., Friedman, M.J., 1989. Infective juvenile formation in the insect parasitic nematode Steinernema feltiae. Parasitology 99, 77–81. Preisser, E.L., Dugaw, C.J., Dennis, B., Strong, D.R., 2005. Long-term survival of the entomopathogenic nematode Heterorhabditis marelatus. Environ. Entomol. 34, 1501–1506. Premachandra, W.T.S.D., Borgemeister, C., Berndt, O., Ehlers, R.-U., Poehling, H.-M., 2003. Combined releases of entomopathogenic nematodes and the predatory mite Hypoaspis aculeifer to control soil-dwelling stages of western flower thrips Frankliniella occidentalis. Biocontrol 48, 529–541. Pu˚zˇa, V., Mrácˇek, Z., 2007. Natural population dynamics of entomopathogenic nematode Steinernema affine (Steinernematidae) under dry conditions: possible nematode persistence within host cadavers? J. Invertebr. Pathol. 96, 89–92. Qiu, L., Bedding, R., 2000. Energy metabolism and its relation to survival and infectivity of infective juveniles of Steinernema carpocapsae under aerobic conditions. Nematology 2, 551–559. Ram, K., Preisser, E.L., Gruner, D.S., Strong, D.R., 2008. Metapopulation dynamics override local limits on long-term parasite persistence. Ecology 89, 3290–3297. Ramírez, R.A., Henderson, D.R., Riga, E., Lacey, L.A., Snyder, W.E., 2009. Harmful effects of mustard bio-fumigants on entomopathogenic nematodes. Biol. Control 48, 147–154. Rasmann, S., Köllner, T.G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzon, J., Turlings, T.C.J., 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732–737. Reed, D.K., Reed, G.L., Creighton, C.S., 1986. Introduction of entomogenous nematodes into trickle irrigation systems to control striped cucumber beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 79, 1330–1333. Richmond, D.S., Kunkel, B.A., Somasekhar, N., Grewal, P., 2004. Top–down and bottom–up regulation of herbivores: Spodoptera frugiperda turn tables on endophyte-mediated plant defence and virulence of an entomopathogenic nematode. Ecol. Entomol. 29, 353–360. Román, J., Beavers, J.B., 1983. A survey of Puerto Rican soils for entomogenous nematodes which attack Diaprepes abbreviatus (L.) (Coleoptera: Curculionidae). J. Agric. Univ. Puerto Rico 67, 311–316. Rovesti, L., Deseö, K.V., 1989. Effect of neem kernel extract on Steinernematid and Heterorhabditid nematodes. Nematologica 35, 493–496. Rovesti, L., Deseö, K.V., 1990. Compatibility of chemical pesticide with the entomopathogenic nematodes, Steinernema carpocapsae Weiser and S. feltiae Filipjev (Nematoda: Steinernematidae). Nematologica 36, 237–245. Rovesti, L., Heinzpeter, E.W., Tagliente, F., Deseö, K.V., 1988. Compatibility of pesticides with the entomopathogenic nematode, Heterorhabditis bacteriophora Poinar (Nematoda: Heterorhabditidae). Nematologica 34, 462–476. Salam, K.A.A., Ghally, S.E., Kamel, E.G., Mohamed, S.A., 1995. Effect of gammairradiated entomopathogenic nematode Steinernema carpocapsae (Fil.) on the larvae of the potato tuber moth, Phthorimaea operculella (Zell.). J. Pest. Sci. 68, 51–54.

E. San-Blas / Biological Control 66 (2013) 102–124 Salame, L., Glazer, I., Miqaia, N., Chkhubianishvili, T., 2010. Characterization of populations of entomopathogenic nematodes isolated at diverse sites across Israel. Phytoparasitica 38, 39–52. Samish, M., Alekseev, E., Glazer, I., 1999. Interaction between ticks (Acari: Ixodidae) and pathogenic nematodes (Nematoda): Susceptibility of tick species at various developmental stages. J. Med. Entomol. 36, 733–740. Samish, M., Alekseev, E., Glazer, I., 2000a. Biocontrol of ticks by entomopathogenic nematodes. Ann. NY Acad. Sci. 916, 589–594. Samish, M., Alekseev, E., Glazer, I., 2000b. Mortality rate of adult ticks due to infection by entomopathogenic nematodes. J. Parasitol. 86, 679–684. Samish, M., Ginsberg, H., Glazer, I., 2004. Biological control of ticks. Parasitology 129, 389–403. Samish, M., Glazer, I., 1991. Killing ticks with parasitic nematodes of insects. J. Invertebr. Pathol. 58, 281–282. Samish, M., Glazer, I., 1992. Infectivity of entomopathogenic nematodes (Steinemematidae and Heterorhabditidae) to female ticks of Boophilus annulatus (Arachnida: Ixodidae). J. Med. Entomol. 29, 614–618. Samish, M., Glazer, I., 1993. Suitability of Boophilus annulatus replete female ticks as host of the nematode Steinernema carpocapsae. J. Invertebr. Pathol. 61, 220–222. Samish, M., Glazer, I., 2001. Entomopathogenic nematodes for the biocontrol of ticks. Trends Parasitol. 17, 368–371. San-Blas, E., Gowen, S.R., 2008. Facultative scavenging as a survival strategy of entomopathogenic nematodes. Int. J. Parasitol. 38, 85–91. Schroeder, W.J., 1990a. Supression of Diaprepes abbreviatus (Coleptera: Curculionidae) adult emergence with soil application of entomopathogenic nematodes (Nematoda: Rhabditida). Florida Entomol. 73, 680–683. Schroeder, W.J., 1990b. Water-absorbent starch polymer: survival aid to nematodes for control of Diaprepes abbreviatus (Coleoptera: Curculionidae) in citrus. Florida Entomol. 73, 129–132. Schroeder, W.J., Beavers, J.B., 1987. Movement of the entomogenous nematodes of the families Heterohabditidae and Steinernematidae in soil. J. Nematol. 19, 257–259. Schroeder, W.J., Sieburth, P.J., 1997. Impact of surfactants on control of the root weevil Diaprepes abbreviatus larvae with Steinernema riobravis. J. Nematol. 29, 216–219. Schroer, S., Sulistyanto, D., Ehlers, R.-U., 2005a. Control of Plutella xylostella using polymer-formulated Steinernema carpocapsae and Bacillus thuringiensis in cabbage fields. J. Appl. Entomol. 129, 198–204. Schroer, S., Yi, X., Ehlers, R.-U., 2005b. Evaluation of adjuvants for foliar application of Steinernema carpocapsae against larvae of the diamondback moth (Plutella xylostella). Nematology 7, 37–44. Schulte, M.J., Martin, K., Büchseb, A., Sauerborna, J., 2009. Entomopathogens (Beauveria bassiana and Steinernema carpocapsae) for biological control of bark-feeding moth Indarbela dea on field-infested litchi trees. Pest Manag. Sci. 65, 105–112. Selvan, S., Gaugler, R., Lewis, E.E., 1993. Biochemical energy reserves of entomopathogenic nematodes. J. Parasitol. 79, 167–172. Selvan, S., Grewal, P.S., Leustek, T., Gaugler, R., 1996. Heat shock enhances thermotolerance of infective juvenile insect-parasitic nematodes Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae). Experientia 52, 727–730. Shapiro-Ilan, D.I., Berry, E.C., Lewis, L.C., 1993. Interactions between nematodes and earthworms: enhanced dispersal of Steinernema carpocapsae. J. Nematol. 25, 189–192. Shapiro-Ilan, D.I., Gaugler, R., Tedders, W.L., Brown, I., Lewis, E.E., 2002a. Optimization of inoculation for in vivo production of entomopathogenic nematodes. J. Nematol. 34, 343–350. Shapiro-Ilan, D., Glazer, I., 1996. Comparison of entomopathogenic nematode dispersal from infected hosts versus aqueous suspension. Environ. Entomol. 25, 1455–1461. Shapiro-Ilan, D.I., Gouge, D.H., Koppenhöfer, A.M., 2002b. Factors affecting commercial success: case studies in cotton, turf and citrus. In: Gaugler, R. (Ed.), Entomopathogenic Nematology. CAB International, Wallingford, UK, pp. 333–355. Shapiro-Ilan, D., Lewis, E.E., 1999. Comparison of entomopathogenic nematode infectivity from infect hosts versus aqueous suspension. Environ. Entomol. 28, 907–911. Shapiro-Ilan, D.I., Lewis, E.E., Behle, R.W., McGuire, M.R., 2001. Formulation of entomopathogenic nematode-infected cadavers. J. Invertebr. Pathol. 78, 17–23. Shapiro-Ilan, D.I., Lewis, L.C., Obrycki, J.J., Abbas, M., 1999. Effects of fertilizers on suppression of black cutworm (Agrotis ipsilon) damage with Steinernema carpocapsae. Suppl. J. Nematol. 31 (4S), 690–693. Shapiro-Ilan, D., McCoy, C., 2000a. Effect of culture method and formulation on the virulence of Steinernema riobrave (Rhabditida: Steinernematidae) to Diaprepes abbreviatus (Coleoptera: Curculionidae). J. Nematol. 32, 281–288. Shapiro-Ilan, D., McCoy, C., 2000b. Susceptibility of Diaprepes abbreviatus (Coleoptera: Curculionidae) larvae to different rates of entomopathogenic nematodes in the greenhouse. Florida Entomol. 83, 1–9. Shapiro-Ilan, D., McCoy, C., 2000c. Virulence of entomopathogenic nematodes to Diaprepes abbreviatus (Coleoptera: Curculionidae) in the laboratory. J. Econ. Entomol. 93, 1090–1095. Shapiro-Ilan, D., Tylka, G.L., Lewis, L.C., 1996. Effects of fertilizers on virulence of Steinernema carpocapsae. Appl. Soil Ecol. 3, 27–34. Sher, R.B., Parrella, M.P., Kaya, H.K., 2000. Biological control of the leafminer Liriomyza trifolii (Burgess): implications for intraguild predation between

123

Diglyphus begini Ashmead and Steinernema carpocapsae (Weiser). Biol. Control 17, 155–163. Sicard, M., Hinsinger, J., Boemare, N., Moulia, C., 2005a. Co-evolutionary process in the symbiotic interaction between the nematode Steinernema carpocapsae and the enterobacterium Xenorhabdus nematophila. Bulletin de la Societe Zoologique de France 130, 193–204. Sicard, M., Ramone, H., Le Brun, N., Pagès, S., Moulia, C., 2005b. Specialization of the entomopathogenic nematode Steinernema scapterisci with its mutualistic Xenorhabdus symbiont. Naturwissenschaften 92, 472–476. Smigielski, A.J., Akhurst, R.J., Boemare, N.E., 1994. Phase variation in Xenorhabdus nematophilus and Photorhabdus luminiscens: differences in respiratory activity and membrane energization. Appl. Environ. Microbiol. 60, 120–125. Somasekhar, N., Grewal, P.S., De Nardo, E.A.B., Stinner, B.R., 2002a. Non-target effects of entomopathogenic nematodes on the soil nematode community. J. Appl. Ecol. 39, 735–744. Somasekhar, N., Grewal, P.S., Klein, M.G., 2002b. Genetic variability in stress tolerance and fitness among natural populations of Steinernema carpocapsae. Biol. Control 23, 303–310. Somvanshi, V.S., Koltai, H., Glazer, I., 2008. Expression of different desiccationtolerance related genes in various species of entomopathogenic nematodes. Mol. Biochem. Parasitol. 158, 65–71. Spaull, V.W., 1992. On the use of a methylcellulose polymer to increase the effectiveness of a Heterorhabditis species against the sugar cane stalk borer, Eldana saccharina. Fund. Appl. Nematol. 15, 457–461. Stack, C.M., Easwaramoorthy, S.G., Metha, U.K., Downes, M.J., Griffin, C.T., Burnell, A.M., 2000. Molecular characterisation of Heterorhabditis indica isolates from India, Kenya, Indonesia and Cuba. Nematology 2, 477–487. Stanuszek, S., 1970. Neoaplectana feltiae (Filipjev, 1934) – a facultative parasite of the caterpillars of Agrotinae in Poland. In: Proceedings of the 9th International Symposium of the European Society of Nematology, August 1967, Warsaw, pp. 355–358. Stark, J.D., 1996. Entomopathogenic nematodes (Rhabditida: Steinernematidae): toxicity of neem. J. Econ. Entomol. 89, 68–73. Steiner, G., 1923. Aplectana kraussei n. sp. Eine in der blattwespe Lyda sp. parasitiderende nematodenform, nebst bemerkungen uber das steiteorgan der parasitsichen nematoden. Zentralblatt für bakteriologie Zweite Abteilung 59, 14–18. Steiner, G., 1929. Neoaplectana glaseri n.g. n.sp. (Oxyuridae) a new nemic parasite of the Japanese beetle. J. Wash. Acad. Sci. 19, 436–440. Stock, S.P., 2005. Insect-parasitic nematodes: from lab curiosities to model organisms. J. Invertebr. Pathol. 89, 57–66. Stoll, N.R., 1953. Axenic cultivation of the parasitic nematode, Neoaplectana glaseri, in a fluid medium containing raw liver extract. J. Parasitol. 39, 422–444. Strauch, O., Niemann, I., Neumann, A., Shmidt, A.J., Peters, A., Ehlers, R.-U., 2000. Storage and formulation of the entomopathogenic nematodes Heterorhabditis indica and H. bacteriophora. Biocontrol 45, 483–500. Strauch, O., Stoessel, S., Ehlers, R.-U., 1994. Culture conditions define automictic or amphimictic reproduction in entomopathogenic rhabditid nematodes of the genus Heterorhabditis. Fund. Appl. Nematol. 17, 575–582. Stuart, R.J., El-Borai, F.E., Duncan, L.W., 2008. From augmentation to conservation of entomopathogenic nematodes: trophic cascades, habitat manipulation and enhanced biological control of Diaprepes abbreviatus root weevils in Florida citrus groves. J. Nematol. 40, 73–84. Stuart, R.J., Hatab, M.A., Gaugler, R., 1998. Sex ratio and the infection process in entomopathogenic nematodes: are males the colonizing sex? J. Invertebr. Pathol. 72, 288–295. Sunderababu, R., Menon, P.P.V., Vadivelu, S., 1985. Effect of temperature on DD-136 in storage. Indian J. Nematol. 15, 109–110. Surrey, M.R., Davies, R.J., 1996. Pilot-scale liquid culture and harvesting of an entomopathogenic nematode, Heterorhabditis bacteriophora. J. Invertebr. Pathol. 67, 92–99. Surrey, M.R., Wharton, D.A., 1995. Desiccation survival of the infective larvae of the insect parasitic nematode, Heterorhabditis zealandica Poinar. Int. J. Parasitol. 25, 749–752. Susurluk, A., Dix, I., Stackebrandt, E., Strauch, O., Wyss, U., Ehlers, R.-U., 2001. Identification and ecological characterization of three entomopathogenic nematode–bacterium complexes from Turkey. Nematology 3, 833–841. Timper, P., Kaya, H.K., Jaffee, B.A., 1991. Survival of entomogenous nematodes in soil infested with the nematode-parasitic fungus Hirsutella rhossiliensis (Deuteromycotina: Hyphomycetes). Biol. Control 1, 42–50. Thomas, G.M., Poinar, G.O., 1979. Xenorhabdus gen. nov., a genus of entomopathogenic, nematophilic, bacteria of the family Enterobactericeae. Int. J. Syst. Bacteriol. 29, 352–360. Thurston, G.S., Ni, Y., Kaya, H.K., 1994. Influence of salinity on survival and infectivity of entomopathogenic nematodes. J. Nematol. 26, 345–351. Toubarro, D., Lucena-Robles, M., Nascimento, G., Costa, G., Montiel, R., Coelho, A.V., Simões, N., 2009. An apoptosis-inducing serine protease secreted by the entomopathogenic nematode Steinernema carpocapsae. Int. J. Parasitol. 39, 1319–1330. Toubarro, D., Lucena-Robles, M., Nascimento, G., Santos, R., Montiel, R., Veríssimo, P., Pires, E., Faro, C., Coelho, A.V., Simões, N., 2010. Serine protease-mediated host invasion by the parasitic nematode Steinernema carpocapsae. J. Biol. Chem. 285, 30666–30675. Tyson, T., Reardon, W., Browne, J.A., Burnell, A.M., 2007. Gene induction by desiccation stress in the entomopathogenic nematode Steinernema carpocapsae

124

E. San-Blas / Biological Control 66 (2013) 102–124

reveals parallels with drought tolerance mechanisms in plants. Int. J. Parasitol. 37, 763–776. Unlu, I.O., Ehler, R.-U., Susurluk, A., 2007. Additional data and first record of the entomopathogenic nematode Steinernema weiseri from Turkey. Nematology 9, 739–741. Van Sloun, P., Nicolay, R., Lohmann, U., Sikora, R.A., 1990. Susceptibility of entomopathogenic nematodes to nematode-trapping and endoparasitic fungi. J. Phytopathol. 129, 217–227 [Abst.]. Vänninen, I., Hokkanen, H., 1997. Efficacy of entomopathogenic fungi and nematodes against Argyresthia conjugella (Lep. Yponomeutidae). Entomophaga 42, 377–385. Vänninen, I., Koskula, H., 2003. Biological control of the shore fly (Scatella tenuicosta) with steinernematid nematodes and Bacillus thuringiensis var. thuringiensis in peat and rockwool. Biocontrol Sci. Tech. 13, 47–63. van Tol, R.W.H.M., van der Sommen, A.T.C., Boff, M.I.C., van Bezooijen, J., Sabelis, M.W., Smits, P.H., 2001. Plants protect their roots by alerting the enemies of grubs. Ecol. Lett. 4, 292–294. Wang, J.X., Li, L.Y., 1987. Entomogenous nematode research in China. Rev. Nématol. 10, 483–489. Wang, Y., Crocker, R.L., Wilson, L.T., Smart, G., Wei, X., Nailon Jr., W.T., Cobb, P.P., 2001. Effect of nematode and fungal treatments on nontarget turfgrassinhabiting arthropod and nematode populations. Environ. Entomol. 30, 196– 203. Wang, Y., Gaugler, R., 1999. Steinernema glaseri surface coat protein suppresses the immune response of Popillia japonica (Coleoptera: Scarabaeidae) larvae. Biol. Control 14, 45–50. Weiser, J., 1955. Neoaplectana carpocapsae n. sp. (Angullulinata: Steinernematidae), novy, cizopasnic housenik obalece jableeneho, Carpocapsa pomonella L. Westnik Ceskoslovenske Zoologicke Spolecnosti 19, 44–52. Welch, H.E., Briand, L.J., 1960. Field experiment on the use of a nematode for control of vegetable crop insects. Proc. Entomol. Soc. Ontario 91, 197–202 [Abstr.]. Westerman, P.R., 1992. The influence of time of storage on performance of the insect parasitic nematode, Heterorhabditis sp. Fund. Appl. Nematol. 15, 407– 412.

Wennemann, L., Cone, W.W., Wright, L.C., Pérez, J., Conant, M.M., 2003. Distribution patterns of entomopathogenic nematodes applied through drip irrigation systems. J. Econ. Entomol. 96, 287–291. Wharton, D.A., Surrey, M.R., 1994. Cold tolerance mechanisms of the infective larvae of the insect parasitic nematode, Heterorhabditis zealandica Poinar. Cryo-Letters 15, 353–360. Whitehorn, P.R., O’Connor, S., Wackers, F.L., Goulson, D., 2012. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336, 351–352. Wilson, M., Ivanova, E., 2004. Neutral density liquid formulations for nematodebased biopesticides. Biotechnol. Lett. 26, 1167–1171. World Wide Fund for Nature, 1993. Pesticide reduction programmes in Denmark, the Netherlands and Sweden. A WWF International Research Report, p. 48. Wouts, W.M., 1979. The biology and life cycle of a New Zealand population of Heterorhabditis heliothidis (Heterorhabditidae). Nematologica 25, 191–202. Wouts, W.M., 1981. Mass production of the entomogenous nematode Heterorhabditis heliothidis (Nematoda: Heterorhabditidae) on artificial media. J. Nematol. 1, 467–469. Wright, R.J., Witowski, J.F., Echtenkamp, G., Georgis, R., 1993. Efficacy and persistence of Steinernema carpocapsae (Rhabditida: Steinemematidae) applied through a center-pivot irrigation system against larval corn rootworms (Coleoptera: Chrysomelidae). J. Econ. Entomol. 86, 1348–1354. Yang, H., Jian, H., Zhang, S., Zhang, G., 1997. Quality of the entomopathogenic nematode Steinernema carpocapsae produced in different media. Biol. Control 10, 193–198. Young, J.M., Dunnill, P., Pearce, J.D., 2002. Separation characteristics of liquid nematode cultures and the design of recovery operations. Biotechnol. Prog. 18, 29–35. Zaki, F.N., Awadallah, K.T., Gesraha, M.A., 1997. Competitive interaction between the braconid parasitoid, Meteorus rubens Nees and the entomogenous nematode, Steinernema carpocapsae (Weiser) on larvae of Agrotis ipsilon Hufn. (Lep., Noctuidae). J. Appl. Entomol. 121, 151–153. Zoltowska, K., Lipinski, Z., Lopienska, E., 2003. Beneficial nematodes: a potential threat to honey bees? Bee World 84, 125–129.