Influence of extraguild prey density on intraguild predation by heteropteran predators: A review of the evidence and a case study

Heteropteran predators constitute an important component of predatory guilds in terrestrial and aquatic ecosystems. Most heteropteran species have generalist diets, and intraguild predation has been documented in most heteropteran families. Zoophytophagous species also frequently engage in intraguild interactions. An increase in extraguild prey density is often predicted to reduce intraguild predation between guild members by providing abundant alternate prey. However, an increase of extraguild prey density may also be associated with an increase in the density of intraguild predators, which could instead strengthen intraguild predation. Evaluating the combined effect of these potentially opposing influences on intraguild predation is difficult. Most studies have been carried out in the laboratory, using artificially simplified communities of predators and prey and employing spatial and temporal scales that may not reflect field conditions. We review experimental studies examining how extraguild prey density influences the intensity of intraguild predation and then report an observational case study examining the influence of extraguild prey density on the intensity of intraguild predation at larger spatial and temporal scales in unmanipulated cotton fields. Fields with more abundant extraguild prey (aphids, mites) were not associated with elevated densities of intraguild predators, and were strongly associated with increased survival of intraguild prey (lacewing larvae). In this system, the ability of extraguild prey to relax the intensity of intraguild predation, as previously documented in small-scale field experiments, also extends to the larger spatial and temporal scales of commercial agriculture. 2011 Elsevier Inc. All rights reserved. 1. Intraguild predation in the Heteroptera The present paper deals with intraguild predation (predation on a competitor, Polis et al., 1989) involving the true bugs (Hemiptera: Heteroptera) as intraguild predators, focusing mainly on terrestrial species. The Heteroptera suborder includes terrestrial predators in the infraorder Cimicomorpha (mainly Reduviidae, Miridae, Nabidae, and Anthocoridae) and the infraorder Pentatomorpha (Pentatomidae, Geocoridae, . . .), aquatic predators in the Nepomorpha (Belostomatidae, Nepidae, Corixidae, Notonectidae, . . .) and finally surface dwelling predators in the Gerromorpha (Gerridae, Veliidae, . . .) (Triplehorn and Johnson, 2004). There is an array of different heteropteran species with different habitats, morphologies, sizes, mobility, and feeding habits. Among these, many species may be involved as predators in an intraspecific (cannibalism), intraguild, or extraguild (classical predation) predation event. Intraguild predation (henceforth ‘‘IGP’’) by heteropteran predators is widespread (Rosenheim et al., 1995; Schmidt et al., 1998; Arim and Marquet, 2004). Among predatory species, numerous ll rights reserved. studies have reported IGP and cannibalistic events involving terrestrial (Rosenheim et al., 1993; Wheeler, 2001), surface (Spence and Carcamo, 1991) and aquatic organisms (Miller, 1971; Dolling, 1991). Most aquatic heteropterans are generalist predators and select their prey more according to their size than to the guild to which they belong (see Hall et al., 1970); as a consequence, they may frequently be involved in IGP. In terrestrial systems, the Heteroptera includes a great number of generalist predators, which by definition constitute potential (and suspected) intraguild predators. Finally, some extremely generalist heteropteran predators, called zoophytophagous consumers (or true omnivores), may even exploit and develop on both plant and animal tissues. Formally, when these predators consume an herbivore they are engaging in IGP, since both the pest and the predator exploit the plant as a shared resource (However, this definition is not used in the present document). These predators may also compete with their extraguild prey for high-quality sites on the plant (Coll and Izraylevich, 1997). Their broad diet often includes some intraguild prey (i.e., their competitors; Lucas and Alomar, 2001, 2002a,b; McGregor and Gillespie, 2005; Provost et al., 2006; Fréchette et al., 2007). Finally, according to the tremendous variability (in size, development stage, andmobility) of the different insect species belonging to 62 É. Lucas, J.A. Rosenheim / Biological Control 59 (2011) 61–67 the same predator guilds as heteropteran predators, IGP opportunities may be common. Eggs, younger (and smaller) instars, andmolting individuals are especially susceptible to predation. In terrestrial food webs, heteropteran predators may consume a diverse array of intraguild prey, including other predators (coccinellids, syrphids, neuropteran and dipteran predators, other heteropteran predators, . . .), parasitoids (especially when consuming herbivores harboring developing parasitoid immatures), pathogens (when consuming infected hosts), and ants (Rosenheim et al., 1995; Kester and Jackson, 1996; Schmidt et al., 1998). IGP by heteropterans has been reported involving species in the families Geocoridae (Guillebeau and All, 1989, 1990; Wheeler, 2001; Rosenheim, 2005), Anthocoridae (Fauvel et al., 1975; Gillespie and Quiring, 1992; Cloutier and Johnson, 1993; Coll and Izraylevich, 1997; Erbilgin et al., 2004), Berytidae (Kester and Jackson, 1996), Miridae (Wheeler, 2001; Fréchette et al., 2007; Lucas et al., 2009), Nabidae (Whitcomb and Bell, 1964; Atim and Graham, 1984; Rosenheim et al., 1993, 1999), Reduviidae (Miller, 1971; Rosenheim et al., 1993, 1999) and Pentatomidae (Mallampalli et al., 2002; De Clercq et al., 2003; Herrick et al., 2008). In aquatic-surface food webs, heteropteran intraguild predators include at least members of the families Nepidae, Notonectidae, (Dolling, 1991), and Gerridae (Spence and Carcamo, 1991). 2. Theoretical effects of an increase of extraguild prey density on IGP One of the key factors influencing the direction, symmetry and magnitude of IGP is the quantity and quality of extraguild prey that are available. At first sight, an increase in the density of extraguild prey might be expected to decrease the magnitude of IGP, simply by increasing the satiation of the predators. In this case, the extraguild prey essentially dilutes the effect of the IG predator on the IG prey. Of course, the situation in nature may be more complex, and may involve species other than just the three species that make up the intraguild predation community module (the extraguild prey, intraguild prey, and intraguild predator). Any change of population density within the trophic web may generate an array of direct and indirect effects on different members of the web, including either vertical effects (top-down or bottom-up) or more complex effects. The whole system typically includes (1) the first trophic level, (2) the extraguild prey – the second trophic level, (3) both the intraguild predator and prey – the third trophic level, and (4) higher order natural enemies, the fourth trophic level (Rosenheim, 1998). Considering a classical terrestrial arthropod food web, the first trophic level is the plant. When extraguild prey density increases, more herbivores (extraguild prey, the second trophic level) attack the plant, which may elicit the expression of induced defences. The production of defensive compounds can have detrimental effects on the extraguild prey, and, when sequestered by herbivores, detrimental effects may also be extended to higher trophic levels (Rogers and Sullivan, 1986). Detrimental effects may reduce the nutritional value of the extraguild prey, and could theoretically increase their vulnerability to predators. On the other hand, sequestration of defensive compounds may reduce the susceptibility of herbivores to predators. Furthermore, zoophytophagous heteropteran IG predators involved in direct consumption of plant material could be affected by plant defensive mechanisms. Any reduction in host plant quality or availability of suitable feeding sites due to herbivory could increase competition (and IGP) between herbivores and omnivorous IG predators. Also, the integrity of the plant substrate may influence the oviposition decisions of those heteropterans that lay their eggs directly in plant tissues. An increase in the density of herbivores (extraguild prey) may generate an increase of intraspecific and interspecific competition, and possibly cannibalism. Consequently, extraguild prey may also modify their behavior by exploiting the plant differently, for example by colonizing less productive plants or less productive microsites on the plant. The distribution of the extraguild prey may change from a contagious pattern to a regular pattern. Extraguild prey will also, most of the time, increase the efficiency of their colonial defences (dilution, encounter, and selfish herd effects) (Turchin and Kareiva, 1989; Lucas and Brodeur, 2001). These changes could affect the foraging efficiency of predators and consequently the magnitude of IGP. Regarding the third trophic level, an increase in extraguild prey density may affect both the behavior and population density of the intraguild predators and the intraguild prey, with implications for overall guild structure and dynamics. For any particular predator, an increase of the shared resource could generate three types of responses: a numerical response, a functional response, or a developmental response. Predator density could increase both by increasing oviposition (reproductive numerical response) and by increasing the recruitment of individuals from other sites (aggregative numerical response). As a consequence, intraguild prey and intraguild predator densities can often be expected to increase. The ratio between both intra and extraguild prey typesmay shape the prey preferences of the intraguild predator, if preference increases for the most common prey (Chow et al., 2008). Also, as the shared resource becomes more common, predation efficiency may improve due to a decrease in handling and searching times (functional response). The intraguild predatormay also bemore likely to become satiated. As a consequence of the functional response, thedevelopment of thepredators may accelerate (developmental response), and for the intraguild prey this may reduce the window of susceptibility to the intraguild predator. As the food required to reach a specific developmental stagemayvarygreatly among thedifferent families of predators, and among species within a same family, the occurrence and duration of the predatory window (as intraguild predator) or prey window (as intraguild prey) will also change. In some cases, the intraguild preymay also benefit from the improvement of the extraguild prey’s defensive traits. This may be especially likely for furtive predators (Lucas and Brodeur, 2001; Fréchette et al., 2008) and parasitoids (Chacón et al., 2008). The composition of the predator guild may also respond to changes in extraguild prey availability. Guild composition and diversity may change according to the threshold density of extraguild prey required for particular predators to exploit extraguild prey populations. For example, some predators may only oviposit if herbivore densities exceed some density threshold (see for example Obrycki et al., 1998; Evans, 2004). In contrast, some predators may avoid sites already colonized by competitors (Janssen et al., 1997; Ruzicka, 1998) or emigrate from these sites (Briggs and Borer, 2005). These changes could be extremely important for a given intraguild prey species, since the arrival of a new intraguild predator may increase its susceptibility to IGP. Alternatively, a given intraguild prey could benefit from a release of IGP pressure if the new intraguild predator has a negative impact on another intraguild predator species that is an important predator of the intraguild prey. The latter hypothesis has been proposed for ladybirds: the arrival of a (second) invasive intraguild predator Harmonia axyridis Pallas in North America may have released some indigenous intraguild prey (smaller ladybirds) from predation by a previous invader Coccinella septempunctata L. (Brown, 2003). Extraguild prey density changes can also have an impact on guild dynamics (time of establishment, voltinism, and life-cycle duration of guild members) and thus on the probability of IGP occurrences (Lucas, 2005). In conclusion, an increase in extraguild prey density may lead to (1) an increase intraguild prey density, with individuals developing more rapidly and spending less time moving about, and (2) a