A Systematic Review on the Effects of Plant-Feeding by Omnivorous Arthropods: Time to Catch-Up With the Mirid-Tomato Bias?

Abstract

Zoophytophagous (omnivorous) predators provide valuable pest control services, and offer an advantage over strict carnivores as plant-feeding enables survival during prey shortage. This putative advantage can potentially be their downside, as plant-feeding may entail damage that negatively affects plant growth/yield (i.e., the cost arising from of omnivore plant-feeding). Yet, benefits conferred by predatory services are usually thought to counterbalance any impact of plant damage. In this systematic review, our goal was to determine how often levels of omnivore damage and its consequences for plants (costs) are considered or quantified. We provide a synthesis of publication trends and findings on omnivore plant-feeding levels, plant injury variables, actual (if quantified) and potential effects on growth/yield, the type of study (lab, greenhouse) and the plants/omnivores most often examined. Our search revealed that measures of omnivore plant-feeding are occasionally reported, but seldom are the direct consequences of such damage also considered. Omnivore plant-feeding were reported in 57% of studies (53 of 93 full-text examined); within these, the majority (>80%) indicated moderate to high levels of plant-feeding. However, only 22% of reports (15 of 69) quantified the effects of omnivore-inflicted damage on plant performance. Of these 15 reports, a greater number found negative consequences for plants compared to those showing no effect (8 vs. 4; 3 with both), with consequences for yield relative to growth being more often evaluated (6 vs. 2). Overall, fruit/leaf injuries relative to stem/flower-feeding were most often examined, and lab/greenhouse experiments predominated. Tomatoes (Solanum lycopersicum) and the mirid Nesidiocoris tenuis were the most common species studied (34 and 14 reports, respectively). Our results indicate that costs to plants of omnivore-inflicted damage are often neglected. We argue that predatory benefits need to be simultaneously considered with plant-feeding effects to appropriately evaluate pest control services. Publication trends suggest that more studies are evaluating costs to plants, but a paradigm shift is still needed. Furthermore, we found that our understanding of plant-feeding and its effects is disproportionally based on studies examining tomato plants and its omnivorous biocontrol agents. To confirm the generality of findings thus far, other plant omnivore systems should be further considered.

Jekyll or Hyde? The genome (and more) of Nesidiocoris tenuis, a zoophytophagous predatory bug that is both a biological control agent and a pest

“…In recent years, the controversial success of N. tenuis has encouraged the scientific community to study this predatory mirid (Puentes et al ., 2018; Pérez‐Hedo et al ., 2020). However, some issues remain to be addressed, such as the genetic variation in commercial stocks of similar biological control agents when compared to wild populations, with the former often diminished in comparison to the latter as seen in other biological control agents (Streito et al ., 2017; Rasmussen et al ., 2018; Paspati et al ., 2019; Pérez‐Hedo et al ., 2020).…”

“…Furthermore, the taxonomic issues that lie within both Miridae and Hemiptera could better be resolved using protein and transcriptome‐based analysis, but there is a noted lack of data in this regard as well (Panfilio and Angelini, 2018). While there is a relatively large amount of research into mirids and their use in biological control compared to other predators (Puentes et al ., 2018), sequencing projects, if any, often focus on pest species and not on biological control agents (Panfilio and Angelini, 2018). For more advanced molecular methods such as RNAi and CRISPR‐based genome editing strategies, it is necessary to have access to genomic and transcriptomic resources of the target species, and so these methods are currently out of reach for N. tenuis researchers.…”

Know your enemy : Genomes of biological control agents

“…The complete dataset of search returns at this point are available in the supplementary materials (Supplementary to the present-day, likely attributed to both the well-documented increase in scientific publishing (Larsen and von Ins, 2010) and a general increase in biological control studies. Similar results occurred in a recent review on zoophytophagous predators (Puentes, Stephan, and Björkman, 2018). The majority of returns are from the CAB Abstracts database (1304), which was chosen as the preferred database for the search and deduplication, followed by Biological Abstracts (969), and Agricola (654).…”

“…The damage ranges from necrotic rings and leaf wilt to spontaneous flower abortion (eventual fruit loss), all in addition to facilitating the spread of plant pathogens due to this damage (Pérez-Hedo and Urbaneja, 2016). This tomato-Nesidiocoris problem is well-documented, making up the largest proportion of research on the damage caused by omnivorous arthropods (Puentes et al, 2018). In determining whether there is a possibility to select for N. tenuis that switch to phytophagy at a lower prey density, knowing more about the genome and genes in particular can help any selective adaptation programs.…”

Tomato Inoculation With a Non-pathogenic Strain of Fusarium oxysporum Enhances Pest Control by Changing the Feeding Preference of an Omnivorous Predator

“…Plant feeding by mirid predators can not only induce plant defenses, but in some cases also cause considerable plant damage (Casta et al, 2011;Puentes et al, 2018). Although M. pygmaeus is in general considered as a safe predator, it can cause serious plant damage at high predator levels and low prey densities .…”