Behavioral Ecology Advance Access first published online on February 13, 2008
This version published online on May 6, 2008
Behavioral Ecology, doi:10.1093/beheco/arm157
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Grouping increases visual detection risk by specialist parasitoids
Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106, USA
Address correspondence to C. Low. E-mail: c_low{at}lifesci.ucsb.edu.
Received 17 April 2007; revised 18 December 2007; accepted 20 December 2007.
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ABSTRACT |
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The benefits of prey grouping may be offset by increased detectability. With a focus on visual detectability, I investigated the potential costs of 2 traits, mine size and group size (number of mines per leaf), of a leaf-mining species, Antispila nysaefoliella (Lepidoptera: Heliozelidae), on the risk of visual detection by parasitoids and the ability to evade attack and capture after detection. Through field experimentation using artificial leaves and mines coated with a nontoxic adhesive spray for trapping insects, I found that the visual cues from groups of mines caused a significant increase in the number of parasitoids captured on experimental leaves (with artificial mines) relative to control leaves (without artificial mines). However, mine size did not. The observational evidence not only supports these patterns but also shows that the per capita risk of parasitism declines with large groups. These results provide evidence of a trade-off between avoiding visual detection and escaping attack after detection.
Key words: aggregation, conspicuousness, dilution effect, host-parasitoid, prey defense, vision.
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INTRODUCTION |
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Prey species display an amazing array of patterns, colors, and forms that protect them against their predators (Cott 1940
; Edmunds 1974; Endler 1986b; Vermeij 1987; Ruxton et al. 2004). For instance, cryptic coloration is important for evading visual predators (Cott 1940; Endler 1991) and noxiousness is important for defending against predators that are averse to those toxins (Lindström et al. 2001c; Brodie et al. 2002). However, such demonstrations of a match between the defenses of prey and the sensory abilities of the predator neglect that there are multiple pathways for defenses to evolve, even when there is only one predator species involved. The predation process involves a sequence of events where a predator must detect, identify, approach, subjugate, and consume its prey (Endler 1986a). Hence, prey can defend at any one of these stages and have multiple and sequential opportunities to do so. But can there be conflict between stages?
Conflicts can arise from limitations in defense efficiency, and the degree of specialization to any individual stage will depend ultimately on the relative importance of that stage, its costs, and its interactions with other stages. However, avoiding detection should be the primary line of defense taken by any prey species because the earlier that predation is interrupted, the less likely that they will have to pay the potential costs of direct confrontation with a predator (Endler 1986a; Stamp and Wilkens 1993; Ruxton et al. 2004). In probabilistic terms, as long as postdetection defense is imperfect, the risk of predation will always be greater after detection (Cooper and Vitt 1991). On the other hand, in some circumstances, the need to hide and to be cryptic can pose costs of its own. For example, maintaining crypsis can reduce the opportunities for finding food or mates, and conversely, the drive to meet these demands can reduce the efficiency of a cryptic strategy (Ruxton et al. 2004). Thus, when crypsis is sufficiently costly or likely to fail, then selection should favor secondary, or postdetection, defenses.
Evolving repertoires of multiple forms of defense may often ameliorate trade-offs in defense efficiency, especially where predators use various tactics to capture their prey (Endler 1986a; Pearson 1989; Gross 1993). As a result, any potential costs of increased detectability, or failed crypsis, can be offset by postdetection "active" defenses such as escape or startle behaviors, noxiousness, encapsulation (with parasitism), or postdetection "passive" defenses such as dilution or confusion effects. In the latter cases, the benefits are the result of the mere presence of more group members (Taylor 1979; Turner and Pitcher 1986; Wrona and Dixon 1991; Riipi et al. 2001; Jackson et al. 2005). However, in all these examples, the expectation is that there are net benefits despite costs of being detected. But what exactly are these costs and how much do they contribute to (or diminish) net benefits? Many published studies have identified the potential costs or benefits of prey grouping. However, most of these reports have been theoretical (Vine 1971; Taylor 1979; Turner and Pitcher 1986; Wrona and Dixon 1991), observational (Foster and Treherne 1981; Cresswell 1994), or experimental studies conducted in controlled and unnatural settings (Watt and Chapman 1998; Riipi et al. 2001a; Jackson et al. 2005).
In this study, I experimentally quantify the potential costs of increased detectability and the degree to which these costs can offset the benefits of postdetection defenses in the field using a natural population of a leaf-mining moth, Antispila nysaefoliella Clemens (Lepidoptera: Heliozelidae). Leaf-mining larvae feed by excavating the leaf mesophyll, creating a "mine," and as larvae feed, crypsis is expected to become more difficult to achieve because their mines grow inevitably larger and more visible (Hering 1951). Hence, a mine can serve as a highly reliable cue for natural enemies to find hosts (e.g., Heinrich and Collins 1983). However, despite the potentially high risks of the leaf-mining habit, this feeding form persists—which suggests that selection for postdetection defense must be intense if indeed visual detectability and the inability to flee are substantial liabilities for leafminers (see discussions in Cornell 1990; Djemai et al. 2000). This paper investigates, more generally, the selective balance between avoiding detection and escaping attack in a host or prey species.
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METHODS |
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Study system
Antispila nysaefoliella specializes on black gum, Nyssa sylvatica Marsh (Nyssaceae). The study site is located within a deciduous forest in the northern Shenandoah Valley, Virginia. Mines begin to appear in early fall, and larvae feed for approximately 3–4 weeks (Low 2007
). The mines of A. nysaefoliella are blotch shaped and tend to expand radially and often become more oblong shaped at later instars. At the final instar, when feeding ceases, a larva will position itself at the mine periphery and tie the inner surfaces together with silk into an oval-shaped double-sided shield (
5 mm, major diameter length). While sandwiched inside, the larva cuts the shield away from the leaf and then descends into the leaf litter for pupation (while remaining inside the enclosed shield). At this point, the leaf is left with an empty mine and a very distinctive "punch hole" shaped by the shield that was once there. By the time of shielding, an individual larva will have consumed up to an average of 2.48 ± 0.56 cm2 of leaf tissue, weighs 0.472 ± 0.22 mg (dry mass), and measures 3.18 ± 0.07 mm in length (mean ± 1 standard deviation [SD], n = 30).
Two traits of A. nysaefoliella, mine size and group size, were chosen for this study because of their hypothesized effects on both visual detection risk and the ability to escape after detection. Mine size is measured in units of area and major diameter length, and group size is the total number of larvae that occur on a single leaf. Increases in values of both traits were expected to increase the visual cue available to parasitoids and, thus, should increase the probability that an individual is detected both within its mine and within its patch (e.g., Riipi et al. 2001a; Jackson et al. 2005). On the other hand, the opposite pattern can also be expected if behavioral escape from within the mine is more likely with larger mines because larger mines provide greater escape space from within the mine allowing a leafminer to "wriggle" away from a probing ovipositor (Connor and Cargain 1994; Djemai et al. 2000); or if in larger groups, the per capita probability of being attacked decreases through a dilution effect (Turner and Pitcher 1986; Wrona and Dixon 1991), confusion effect from multiple mines (Tosh et al. 2006), group behavioral defenses (Cocroft 1996; Low 2007), or other possible mechanisms (Hamilton 1971; reviewed by Krause and Ruxton 2002).
Natural patterns of parasitism
To estimate natural parasitism rates of A. nysaefoliella, I sampled the population both destructively and nondestructively. Because parasitism is often difficult to confirm in the field, especially in minute mines by minute species (both <1 mm diameter), I collected a random sample of leaves from 10 trees (4 branches each) on approximately the 10th day of the season, 29 August 2004, and stored them at 4 °C for 2 weeks in plastic storage bags lined with moist paper towels to allow for parasitoid eggs, larvae, and pupae to develop. Then, I inspected all mines and larvae (from a total of 361 leaves with group sizes 1–43) for any signs of parasitism (e.g., parasitoid eggs, larvae, pupae, and emergence holes) using a 100x magnification dissecting microscope.
Because this method provides only information about parasitism at a single point in time and excludes past and future parasitism events, I also monitored individual leaves and mines in the field in an attempt to capture parasitism as it occurred throughout the leaf-mining stage of an entire group of larvae. In this nondestructive method, I photographed individual leaf mines (from a total of 63 leaves with group sizes 1–44) every 3–5 days from the time of mine initiation until all larvae on a leaf were determined to have 1) survived to the shielding stage, 2) become parasitized, 3) been preyed upon, or 4) ceased development (from unknown causes). The major diameter length and the total area of mines were measured using image analysis software and were calibrated against a metric scale that was placed in every image. Identifications of individual leaves were kept with white labeling tape folded across the petioles bearing an identification number.
Artificial leaf experiment
To test directly the effect of mine size and group size on visual detection risk, I conducted a field experiment using sticky artificial leaves with artificial mines to capture parasitic wasps and other flying insects. In contrast to typical assays of parasitism or predation that measure the final outcomes after the completion of all stages of predation, this experiment provides a much better approximation of detection risk because parasitoids and other potential natural enemies cannot leave after landing. This experiment was designed as a 2-way factorial experiment testing 4 mine sizes (diameter: 1.6, 3.2, 6.4, and 12.7 mm) and 4 group sizes (1, 3, 5, and 10). However, the treatment level of mine size 12.7 mm by group size 10 was omitted because of leaf size limitations and the associated difficulty with affixing the artificial (vellum) mines to very little surface area.
I created the experimental leaf set by, first, selectively pruning very realistic looking leaves from artificial "Ficus" trees. These leaves were made of a pliable lightweight fabric with a light gloss coating. The selected leaves fell within the range of natural leaves in size (artificial: 29.6 cm2, natural: 44.5 ± 19 cm2), length (artificial: 9.2 cm, natural: 11.2 ± 2.5 cm), and perimeter (artificial: 25.4 cm, natural: 30.4 ± 6.8 cm) (n = 132; mean ± 1 SD). These also matched the general shape of N. sylvatica leaves, which included the tapered leaf tip (Figure 1a).
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Next, I created artificial mines by punching holes in the artificial leaves with different-sized hole punchers according to the treatment levels mentioned above. The purpose of this was to allow the translucence of natural mines to be recreated when mines cut out from a semitransparent vellum paper (30# Earth Brown, Marco's Printed Products Company, Dayton, OH) were applied. To create these mines, discs were punched or cut from the vellum paper in sizes slightly larger than the punch holes and were affixed to the leaf undersides using a colorless nontoxic glue, covering the holes entirely.
I confirmed that the color of the artificial leaves and mines fell within the range of natural N. sylvatica leaves and A. nysaefoliella mines by measuring their spectral properties with an Ocean Optics USB2000 spectroradiometer and a Xenon flash light source. Using a 3-mm-diameter probe, I took reflectance scans of 15 natural leaves, 13 natural mines, an artificial leaf, and the vellum paper used for the artificial mines. The reflectance scans were taken at 0.40-nm intervals across the visible light spectrum, 300–700 nm. Because the color of an object depends on the light that illuminates it, the ambient light in the 2 most common light environments, forest shade and sun fleck, was measured using a cosine-corrected sensor. The ambient light was measured as the total irradiance summed over all wavelengths from 300 to 700 nm. Then, to estimate the radiance of leaves and mines in sun flecks and forest shade, the reflectance spectrum of each leaf and mine was multiplied by the irradiance of each light habitat to produce the final spectra that characterized their appearance (Figure 1b). These methods are described in more detail by Endler (1990, 1993) and have been applied similarly in Uy and Endler (2004). (Many trials with different materials and methods, including the uptake of glycerin into natural leaves, produced this final suitable and functional combination of materials for this experiment.)
To capture insects landing on the artificial leaves, I sprayed the upper leaf surfaces with a colorless, odorless, and pesticide-free insect adhesive coating (TanglefootTM). I then placed these leaves within natural leaf clusters by tying their (brown) plastic petioles with green floral wire to branches and stems. Each experimental leaf was paired with a sticky artificial leaf without mines to control for location-specific differences. I attached each leaf pair (1 experimental and 1 control) on the same stem next to one another either in the same or opposite orientation (example in Figure 1a). Each treatment set (15 pairs) was replicated 5 times within a tree across 10 trees (total of 50 replicates per treatment level; n = 750 pairs). Each replicate set was distributed within a different area of each tree. Leaves were set out on 19–21 August 2004 and removed on 18–20 September 2004. This period spanned the peak of leaf-mining activity. At the end of the experiment, I collected and sealed each leaf individually in plastic snack bags and stored them at 4 °C for later processing. The trees used for this experiment are the same as those used for the observational data in the previous section.
To process leaves for data, I visually scanned the artificial leaves for all hymenopteran parasitoids using a dissecting microscope. I removed all specimens from the sticky leaf surfaces using a citrus solvent (Goo GoneTM) and identified them to family level, which is sufficient for sorting between parasitoids that attack leafminers and those that do not (Grissell and Schauff 1990; Gates et al. 2002).
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RESULTS |
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Observational
Of the total larvae sampled both destructively and nondestructively (n = 712), approximately 38.1% (271) survived to the shielding stage and the rest died from parasitism (25.1%, 179), predation (2.1%, 15), or unknown causes (34.7%, 247). The average size (diameter) of mines for each fate was 4.8 ± 3.7 mm (unknown), 6.53 ± 2.9 mm (parasitism), 7.4 ± 3.4 mm (predation), and 15.7 ± 2.3 mm (shield) (mean ± 1 SD). Figure 2 describes the distribution of final mine sizes for each fate and illustrates, most importantly, that the occurrence of parasitism and other sources of mortality is rarely found among the largest mine sizes. Mine sizes differed significantly by fate according to analysis of variance (ANOVA) (degrees of freedom [df] = 3,711, F = 636.7, P < 0.001), and post hoc comparison tests (Tamhane's T2 in SPSS 11.5) determined that parasitism and unknown and parasitism and shield were significantly different (P < 0.001) but predation and parasitism (P = 0.928) and predation and unknown (P = 0.065) were not.
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Logistic regression analyses of both nondestructive and destructive data sets revealed that the probability of parasitism occurring on a leaf increases with group size (Wald = 32.87, df = 1; P < 0.001; Figure 3a). However, despite the greater frequency of parasitism across leaves with larger group sizes, the per capita rate of parasitism (y), calculated as the proportion of parasitized larvae on each leaf given that parasitism had occurred, decreased significantly with group size in both the destructive sample (model: y = 0.78 – 0.26 x log [group size]; R2 = 0.75, df = 99, F = 300.1, P < 0.001) and the nondestructive sample (model: y = 0.83 – 0.22 x log [group size]; R2 = 0.62, df = 34, F = 57.9, P < 0.001) (Figure 3b).
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From the samples of collected leaves, I collected and identified 3 families of hymenopteran parasitoids that are candidates for parasitoids of leaf-mining lepidoptera: Eulophidae (Chalcidoidea), Ceraphronidae (Ceraphronoidea), and Platygastridae (Platygastroidea). These families had also been reared in previous seasons, and their sole inclusion as parasitoids of A. nysaefoliella is so far confirmed by the analysis of 44 mtDNA (COI) sequences screened from more than 300 genomic samples of A. nysaefoliella larvae from a full range of mine sizes (Low C, unpublished data). These taxa are known to attack other lepidopteran leaf-mining larvae (Grissell and Schauff 1990
; Gates et al. 2002).
Experimental
A total of 1175 parasitic wasps were captured on the artificial leaves. Of these, 445 (38%) were parasitoids of lepidopteran leafminers and 730 (62%) were parasitoids of other types of hosts (Table 1). Because every experimental leaf was paired with its own control leaf (no mines), I used a repeated measures ANOVA to test for differences in each of these categories of wasps due to the experimental treatments. I considered each pair of leaves as a subject (or sample unit) and entered the experimental treatment (with mines or without mines) as a within-subjects factor. The mean density of leafminers for each tree was entered as a covariate. The results reported below are from a full factorial Type I sums-of-squares model using SPSS 11.5.
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Leafminer parasitoids
The repeated measures ANOVA detected a significant treatment effect and a significant interaction of the experimental treatment with group size (Table 2). Tests of between-subjects effects revealed no significant main effects of mine size or group size or their interaction on the abundance of leafminer parasitoids that landed among experimental pairs (Table 2). The density of A. nysaefoliella among trees was a significant covariate of the number of leafminer parasitoids captured but not with other parasitic wasps (Table 2).
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The number of leafminer parasitoids was, on average, greater on experimental leaves for all group sizes >1. The effect magnitudes for each group size (1, 3, 5, and 10) were 0%, 100%, 24.5%, and 103.7%, respectively. These results were not correlated with the total number of parasitoids (np) captured within each group size (np = 106, 138, 119, and 82, respectively). A post hoc analysis using paired t-tests detected significant differences for group sizes of 3 and 10 only (Figure 4a). Using the average number of parasitoids per mine (y) as a proxy for per capita risk, the potential risk of parasitism for an individual was found to decrease significantly with group size according to the function y = 0.26 – 0.1 x log (group size) (using treatment leaves only; R2 = 0.623, df = 31, P < 0.001; Figure 4b).
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The effect of mine size in the experiment was not statistically significant. However, the 2 largest mine sizes showed the greatest effect magnitudes (1.6 mm: 34.9%; 13.2 mm: 6.2%; 6.4 mm: 61.4%; and 2.7 mm: 115.4%) (Supplementary Appendix A). Similar to the results with group size, this pattern was not correlated with the total number of parasitoids captured within each mine size category (np = 101, 113, 149, and 82, respectively).
Other parasitic wasps
The abundance of other types of parasitic wasps was significantly greater on experimental leaves than control leaves for all treatment combinations, but there was no significant association with mine size, group size, or their interaction (Table 2, Supplementary Appendix A).
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DISCUSSION |
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The results of this study indicate that the visual aspects of leaf mines and especially groups of leaf mines can increase the rate of detection by parasitic wasps that specialize on leafminers. Both observational and experimental data sets reveal that when a mine occurs singly, the risk of being detected is no different from when a leaf has no mines (or when parasitoids are landing at random). A close look of the observational data (in Figure 3a) reveals that it is at 3 mines or more that the risk of detection begins to increase, with the risk of at least one parasitism event for groups of 30 or more. Although the experiment did not cover the entire range of naturally occurring group sizes, it did capture the point at which detection risk appears to increase for A. nysaefoliella and clearly demonstrated a significant increase in visual detection risk in groups of 3 mines or more.
So why do mines occur in groups of as many as 50 per leaf? My observational results reveal that, despite increased detectability with larger group size, group size has a positive association with per capita survival. This suggests that the potential costs of increased detectability are likely offset by postdetection escape mechanisms, such as dilution or confusion effects, and the net survival benefits will drive selection for larger aggregations. That is, the potential costs of increased visual detectability are ameliorated by the benefits of escape at later stages of the predation sequence by living in groups.
Evolution and the predation sequence
The predation sequence outlined by Endler (1986a) serves as a general conceptual framework for understanding how prey should evolve defenses against predators. Throughout this paper, I treated the predation sequence as consisting of 2 parts: a detection stage and an all-encompassing postdetection stage. However, a closer look at A. nysaefoliella and other leaf-mining systems reveals that there are distinct traits or defenses involved specifically with each stage of predation. For example, although they cannot escape from their mines, some species have been found to have the ability to escape subjugation and capture from within their mines by either wriggling away or creating vibrations that disrupt the parasitoid's search for the host beneath the leaf surface (Gross 1993; Connor and Cargain 1994; Bacher et al. 1996). Antispila nysaefoliella has a unique vibrational behavior that is observed only in the larvae, which is deliberate and produces intense, fully audible, airborne vibrations (Low 2007). Perhaps, larger mines or concerted vibrational behavior allow larvae to produce vibrations that are more intense or confusing and, possibly, more effective at evading a parasitoid that is probing or searching from the leaf surface via vibrational sounding and antennation (Fischer et al. 2001). This could explain why the risk of parasitism is reduced in large groups and rarely occurs among the largest mine sizes (Figure 2).
Moreover, even when leafminers (and other insects) have completely failed to evade attack at all previous stages, the cellular immune response of encapsulating a parasite egg that is already within the host's body provides the host one final chance at surviving parasitism by avoiding the stage of consumption (Fellowes et al. 1999). A similar examination of other prey or host systems might also reveal repertoires of defenses suited for multiple, if not all, stages of predation. Thus, it may be essential to estimate the contribution of a trait to risk at each stage of the predation process in order to fully understand the general advantage of a particular prey (or host) trait and to predict the direction of evolution. The importance of decomposing the predation sequence has been implied or directly suggested by several theoretical studies (Taylor 1979; Sillén-Tullberg and Bryant 1983; Turner and Pitcher 1986; Cooper and Vitt 1991; Ruxton et al. 2004).
The saturating function
The results of this study are consistent with the results of Riipi et al. (2001) and Jackson et al. (2005) where detectability risk was also found to be higher for individuals in groups than when solitary. In both studies, detection risk quickly saturated beyond a single individual. In Riipi et al. (2001), birds in an aviary selected from among artificial prey groups (crosses and squares on white sheets of paper), and in Jackson et al. (2005), human subjects searched for computerized prey which were mottled squares set against colored backgrounds. My study supports these laboratory findings but is the first to provide direct experimental evidence and a quantification of visual detection risk in the field. My results clearly demonstrate a saturating function between group size and visual detectability—which is a prerequisite for the mechanisms of safety from group living, such as a simple numerical dilution effect, to operate. In addition, it has been commonly observed that the parasitoids of leafminers and many other types of predators attack only a few hosts per leaf (Casas 1989; Connor and Taverner 1997), which is the ideal context for the evolution of group formation. However, in contrast to these previous studies, my results suggest that the expected net benefits of increased per capita survival due to grouping could diminish if an increase in the frequency of visitations and attacks is a consequence of greater visual detectability, which is especially problematic when group numbers are essentially fixed and individuals cannot reorganize. Therefore, the temporal and additive effects of increased detectability should be explicitly considered in future models.
Implications for leafminer evolution
Researchers have often speculated about the adaptive significance of leaf mining because of the apparent disadvantages of living inside a leaf, creating unavoidable visual cues through feeding, and being physically constrained within a small space where the only protection from predators is a thin leaf epidermis (Kato 1985; Connor and Taverner 1997; Salvo and Valladares 2004). However, until now, the detectability costs of leaf mining have been largely assumed and is perhaps the reason why a great deal of attention has been devoted to understanding postdetection escape tactics (Meyhöfer et al. 1997), the behavioral decisions of the attacking parasitoid (Casas 1989; Djemai et al. 2000, 2004), or alternate advantages of the leaf-mining habit such as protection from environmental factors and other mortality agents (Connor and Taverner 1997).
Although the size of a mine was not associated with an increase in visual detectability, mine size could play an important role in facilitating discrimination and specialization among parasitoid species. The ability for parasitoids to differentiate among hosts based on mine morphology, such as shape, size, color, or contrast, is likely to be important and adaptive (Wäckers and Lewis 1999; Salvo and Valladares 2004). If the parasitic wasps of nonleaf-mining hosts are not specialized for searching for leafminers, then they may be responding to the general visual aspects of herbivory damage rather than to cues that are specific to leaf-mining hosts—which might explain why they showed an overall positive response to the experimental treatment (i.e., presence of the mines), but not with respect to mine size or group size.
In conclusion, the results reported here suggest that group size contributes to increased visual detectability, but the potential costs of increased detectability are likely offset by postdetection advantages of group living. I would expect that for leafminers, this balance would be highly sensitive to environmental and physiological conditions where the pressure to reduce detectability may be relaxed when parasitism risk is low—which would allow for slower feeding rates, greater consumption (larger mines), and solitary feeding. In contrast, under conditions of high parasitism risk, it may become more important to feed more quickly to reach a less vulnerable state (i.e., larger mine size), occur in larger, but safer, groups or develop on high-quality resources so that nutritional requirements can be satisfied with lower consumption (to produce smaller, less conspicuous mines). All this, however, is highly dependent on the search and attack behaviors of the predator or parasitoid. Finding the evolutionary optima, understanding the conditions that shift these optima, and evaluating their effects on population stability would be important lines of research for future studies.
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SUPPLEMENTARY MATERIAL |
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Supplementary Appendix A can be found at http://www.beheco.oxfordjournals.org/.
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FUNDING |
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The Blandy Graduate Research Fellowship to C.L. and National Science Foundation Field Stations Grant (BIR-9512202) to Blandy Experimental Farm.
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ACKNOWLEDGEMENTS |
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Many special thanks go to J. Endler, R. Nisbet, E. Connor, A. Uy, and M. Gates for their advice, expertise, and overall support. Also, S. Pitnick, T. Roulsten, and T. Starmer provided logistical support, and W.R. Rice provided comments on statistics and the manuscript. Red Gate Farms graciously provided permission to conduct this study on their property.
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FOOTNOTES |
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Figure 1 and the funding paragraph have been updated.
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REFERENCES |
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