Introduction

The interest in organic foods grows permanently worldwide, as does the area devoted to this type of agriculture. Organic agriculture land has quadrupled since 1990, reaching a total area of 43.7 million hectares in 2014 ( Willer & Lernoud, 2016 ).

Nuts are among the main permanent organic crops in the world, surpassed only by coffee and olives. In 2014 the worldwide area for organic nuts was 286,109 ha ( Willer & Lernoud, 2016 ) and an important portion of this (94,646 ha) corresponded to Spain where the main organic nut crop is almond (85,241 ha) ( MAGRAMA, 2015 ).

Monosteira unicostata (Mulsant & Rey) (Hemiptera: Tingidae), commonly known as false tiger or poplar lace bug, is one of the most serious pests of organic almond orchards in Spain ( García Marí & Ferragut, 2002 ; Almacellas & Marín, 2011 ; Marcotegui et al., 2015 ). This insect is frequently found damaging almond crops in other Mediterranean countries ( Talhouk, 1977 ; Moleas, 1987 ; Liotta & Maniglia, 1994 ; Russo et al., 1994 ; Bolu, 2007 ) and it has been cited in North America recently ( Scudder, 2012 ). Adults and nymphs of this species suck the cellular content of leaves and can cause significant defoliation of trees thus resulting in a yield decrease ( Liotta & Maniglia, 1994 ; García Marí & Ferragut, 2002 ). These damages are particularly serious in organic almond orchards, where chemical insecticides, commonly used to control this pest, are not authorized.

The production of certified organic food requires practices authorized by organic production standards ( IFOAM, 2014 ; EC, 2015 ; USDA, 2016 ). Crop protection in organic agriculture is based on preventive strategies (well adapted varieties, balanced fertility, rotations, companion planting, green manures, functional biodiversity, habitat management, beneficial organisms) and insecticide application is restricted to products of mineral or vegetable origin included in the standards that are used as a last option when prevention has failed ( Zehnder et al., 2007 ). Some studies have been conducted recently to search for products allowed in organic production that would be effective for controlling M. unicostata in almond crops. Sánchez-Ramos et al. (2014) found out, in laboratory tests, that kaolin sprayed on almond leaves reduced oviposition plus adult and nymphal feeding, while potassium salts of fatty acids combined with thyme essential oil caused high mortality of nymphs. The effect of these products against this pest was also tested in field trials ( Marcotegui et al., 2015 ). In this case, both products reduced abundance of M. unicostata and the damage on leaves, being kaolin the most effective.

To conserve or improve biodiversity is a general objective of organic cropping and enhancing abundance and efficacy of the natural enemies existing community is a priority for this production system ( Zehnder et al., 2007 ; IFOAM, 2014 ). Therefore, the potential impact of any insecticide application on natural enemies arthropod fauna must be previously investigated. Natural biological control of M. unicostata has not been deeply studied. Although different groups of predators (like Araneae, Forficulidae, Chrysopidae, Miridae, Anthocoridae, Coccinelidae, Carabidae, and predatory Thysanoptera, Hymenoptera and Diptera) and parasitoids (like Mymaridae) have been reported as possible natural enemies of M. unicostata ( Vessia, 1961 ; Moleas, 1987 ) only Araneae and Anthocoridae have shown an obvious predatory activity against this pest in the field ( Moleas, 1987 ).

Kaolin affects the recognition and attractiveness of host plants by arthropods and has proved to be an effective barrier to prevent damage by phytophagous arthropods in many crops ( Showler, 2002 ; Glenn & Puterka, 2005 ). Laboratory studies have also reported negative biological and behavioral effects of kaolin particle film on entomophagous arthropods ( Ulmer et al., 2006 ; Porcel et al., 2011 ; Bengochea et al., 2013 , 2014a , b ; Benhadi-Marín et al., 2016 ). In addition, although some field trials did not find negative effects of kaolin on certain natural enemies ( Karagounis et al., 2006 ; Sackett et al., 2007 ; Porcel et al., 2011 ) in other studies, populations of different taxa of parasitoid and predatory arthropods were reduced after kaolin applications ( Knight et al., 2001 ; Showler & Sétamou, 2004 ; Lombardini et al., 2005 ; Jaastad et al., 2006 ; Markó et al., 2006 , 2008 , 2010 ; Stelinski et al., 2006 ; Sackett et al., 2007 ; Pascual et al., 2010 ; Scalercio et al., 2010 ).

Insecticidal soaps and plant oils are commonly used for pests control in organic farming ( Zehnder et al., 2007 ) but few data are available on the selectivity of these “organic treatments” to beneficials. No negative effect of insecticidal soaps on natural enemies have been reported in many studies ( Natarajan, 1990 ; Bigler & Waldburger, 1994 ; Jacas Miret & García-Marí, 2001 ; Karagounis et al., 2006 ; Jansen et al., 2010 ). However, in others, negative effects of soaps applications were found on some groups of natural enemies ( Oetting & Latimer, 1995 ; Smith & Krischik, 2000 ; Stansly et al., 2002 ; Kraiss & Cullen, 2008 ; Raudonis et al., 2010 ; Hall & Richardson, 2013 ; Smaili et al., 2014 ). In the case of essential oils, again some studies reported no negative effect on natural enemies ( Echegaray & Cloyd, 2012 ; González et al., 2013 ), but some detrimental effects have been also reported ( Momen & Amer, 1999 ; Amer & Momen, 2002 ; Choi et al., 2004 ; Bostanian et al., 2005 ; Huignard et al., 2008 ; Cloyd et al., 2009 ).

In the present work, the effects of these organic-farming-compatible pests control products on non-target arthropods of almond tree canopy were evaluated, under real field conditions, paying special attention to the community of natural enemies of pests.

Material and methods

Results

Discussion

One of the most important issues in integrated pest management strategies is the proper use of all the available methods to control pests, taking into account environmental concerns, like the possible negative effects of these methods on non-target fauna ( Barzman et al., 2015 ). In this respect, it is necessary to assess the influence of control strategies on those beneficial organisms that contribute to maintain populations of damaging arthropods under economic thresholds. This is especially important in organic production systems, because the availability of allowed products for pest control is more reduced than in conventional production.

There is few information about the composition of the natural enemies’ community of almond orchards. Regarding predators, our results reasonably agree with those reported by Benhadi-Marín et al. (2011) , who pointed out Araneae as the most abundant group, followed by Coleoptera (mainly from Family Coccinellidae), Formicidae, Neuroptera, Hemiptera and Dermaptera. Other authors also report the occurrence of predators belonging to these groups in almond trees ( Bolu, 2007 ; Eilers & Klein, 2009 ; Yanik et al., 2011 ; Santos et al., 2012 ). However, in none of these works the occurrence of predatory Acari, Thysanoptera or Diptera is reported, but Hoy et al. (1979) collected phytoseiid mites and predatory thrips in almond orchards, as well as Neuroptera and predatory Coleoptera. Of the families of spiders collected by Benhadi-Marín et al. (2011) , Philodromidae, Salticidae, Theridiidae, Thomisidae, Araneidae, Oxyopidae and Gnaphosidae were also present in our orchards. Concerning parasitoids, in the work by Eilers & Klein (2009) the families Bethylidae and Encyrtidae comprised the majority of parasitoids collected, with only seven morphospecies captured, whereas we have collected up to 16 families of hymenopteran parasitoids. Regarding the possible natural enemies of M. unicostata, most of the groups reported by different authors ( Vessia, 1961 ; Moleas, 1987 ) have been collected in our assays, and those that have been proved to feed on this lace bug in the field (Araneae and Anthocoridae) ( Moleas, 1987 ) are well represented in both years of study.

In the search of more environmentally friendly strategies to control almond pests in organic production, some compounds like the aluminosilicate mineral kaolin, the insecticidal soaps based on potassium salts of fatty acids and plant essential oils have shown relatively good results in laboratory and field assays ( Braham et al., 2014 ; Sánchez-Ramos et al., 2014 ; Marcotegui et al., 2015 ). However, although these products are considered to have safe environmental profiles ( Weinzierl & Henn, 1991 ; Glenn et al., 1999 ; Isman, 2006 ; Markó et al., 2008 ; Regnault-Roger et al., 2012 ), they cannot be considered as selective pesticides and their impact on non-target arthropod fauna should be evaluated.

In this work, we have observed some detrimental effects of kaolin and a combination of potassium salts of fatty acids and thyme essential oil on non-target arthropod fauna. Kaolin produced the most negative effects, since this product reduced the abundance of beneficials and other arthropods, and arthropod diversity and species richness in both years of the study. PSTEO only produced a slight decrease in abundance of natural enemies in the second year. Curiously, abundance of natural enemies in 2009 was significantly higher in control plots than in PSTEO plots before treatment application. This could be considered a random effect, since plots were assigned randomly to each treatment. In addition, no significant differences were observed after treatments.

Negative effects of kaolin on non-target arthropod fauna have been reported before in many crops, including olive, apple, plum, blueberry, pecan or cotton ( Knight et al., 2001 ; Showler & Sétamou, 2004 ; Lombardini et al., 2005 ; Jaastad et al., 2006 ; Markó et al., 2006 , 2008 , 2010 ; Stelinski et al., 2006 ; Sackett et al., 2007 ; Pascual et al., 2010 ; Scalercio et al., 2010 ). These detrimental effects were independent of the number of applications made, because in these studies they ranged from one to more than ten. The affected taxa are very diverse and include a high number of families of Araneae (Salticidae, Philodromidae, Theridiidae), Acari (Phytoseiidae, Trombidiidae, Tydeidae), Coleoptera (Coccinellidae), Heteroptera (Anthocoridae, Miridae, Reduviidae), Dermaptera (Forficulidae), Neuroptera (Chrysopidae) or Hymenoptera (Formicidae and different families of parasitoids like Scelionidae, Pteromalidae, Aphelinidae, Braconidae, Ichneumonidae). In addition, different functional groups are affected, from predaceous and parasitoids to arthropods with other food habits. Laboratory studies have also shown some negative effects of kaolin on different beneficial arthropods like predatory Heteroptera (Anthocoridae), parasitoid Hymenoptera (Braconidae, Pteromalidae), Neuroptera (Chrysopidae) or Araneae (Bengochea et al., 2013 , 2014a , b ; Benhadi-Marín et al., 2016 ).

Regarding insecticidal soaps, some detrimental effects of different formulations have also been registered both in field and laboratory conditions on beneficial non-target arthropods belonging to Acari (Phytoseiidae), Coleoptera (Coccinellidae), Neuroptera (Chrysopidae) and Hymenoptera (Eulophidae, Braconidae) ( Oetting & Latimer, 1995 ; Smith & Krischik, 2000 ; Kraiss & Cullen, 2008 ; Raudonis et al., 2010 ; Hall & Richardson, 2013 ; Smaili et al., 2014 ). In addition, negative effects on predators and parasitoids have been reported for plant essential oils. Thus, predators belonging to Acari (Phytoseiidae), Coleoptera (Staphylinidae) and Heteroptera (Anthocoridae), and parasitoids belonging to Hymenoptera (Braconidae, Pteromalidae) showed some negative effects when treated with different essential oils from citronella, basil, soybean, rosemary, peppermint or Chenopodium ( Momen & Amer, 1999 ; Amer & Momen, 2002 ; Choi et al., 2004 ; Bostanian et al., 2005 ; Huignard et al., 2008 ; Cloyd et al., 2009 ). However, the degree of magnitude of these effects can be considered much lower compared with the effect of kaolin, similarly to what has been obtained in our field assay with the combination of insecticidal soap and thyme essential oil.

With the aim of determining the most affected taxa after the treatment applications, PRC analyses were performed. However, the differences observed regarding abundance and diversity were not fully reflected in the PRC results, because significant effects were only detected in two analyses in 2010. This contrasts with former studies that indicated that PRC analyses were more sensitive than methods based on comparison of means ( Pascual et al., 2010 ).

As stated in our previous work, the intention was to evaluate the efficacy of the treatments with a reduced number of applications to establish cost-effective control strategies ( Marcotegui et al., 2015 ). These applications produced a moderate effect on almond tree pests and, though M. unicostata is one of the most affected taxa, a higher number of applications might be necessary to reduce damage effectively. However, we have found negative effects, especially with kaolin, on non-target arthropod fauna even with such low number of applications. Therefore, the increase in the frequency of applications would surely exert much higher disruption on the community of beneficial and other non-target arthropods.

In conclusion, despite the fact that the products assayed in the present work are claimed to be environmentally safer than those used in conventional agriculture, they still have detrimental effects on non-target arthropod fauna because of their reduced selectivity. This is especially relevant in the case of kaolin, because a continuous coverage of the plants throughout the season is essential for the effectiveness of this product, what might lead to long-term effects on the community of beneficial arthropods. Thus, a rational use of this type of products should be implemented, for example by alternating them with other strategies with less negative effects or by taking into account the best timing for its application according to the phenology of pests.

Acknowledgements

We thank Javier Melgares de Aguilar and David González (Oficinas Comarcales Agrarias de la Región de Murcia) for their collaboration in field assays.