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Behav Ecol. 2011 Jul-Aug; 22(4): 730–737.
Published online Apr 29, 2011. doi:  10.1093/beheco/arr042
PMCID: PMC3117901
Resource quality or competition: why increase resource acceptance in the presence of conspecifics?
Jeremy M. Davis,corresponding authorab César R. Nufio,acd and Daniel R. Papaja
aCenter for Insect Science, University of Arizona, 1007 E. Lowell Street, P.O. Box 210106, Tucson, AZ 85721, USA
bDepartment of Biology, Vassar College, 124 Raymond Avenue, Poughkeepsie, NY 12604, USA
cUniversity of Colorado Museum of Natural History, 1030 Broadway Street, Boulder, CO 80309, USA
dDepartment of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA
corresponding authorCorresponding author.
Address correspondence to J.M. Davis. E-mail: jedavis/at/vassar.edu.
Received June 28, 2010; Revised January 17, 2011; Accepted March 4, 2011.
Some animal species increase resource acceptance rates in the presence of conspecifics. Such responses may be adaptive if the presence of conspecifics is a reliable indicator of resource quality. Similarly, these responses could represent an adaptive reduction in choosiness under high levels of scramble competition. Although high resource quality and high levels of scramble competition should both favor increased resource acceptance, the contexts in which the increase occurs should differ. In this paper, we tested the effect of social environment on egg-laying and aggressive behavior in the walnut fly, Rhagoletis juglandis, in multiple contexts to determine whether increased resource acceptance in the presence of conspecifics was better viewed as a response to increased host quality or increased competition. We found that grouped females oviposit more readily than isolated females when provided small (low-quality) artificial hosts but not when provided large (high-quality) artificial hosts, indicating that conspecific presence reduces choosiness. Increased resource acceptance was observed even when exposure to conspecifics was temporally or spatially separate from exposure to the resource. Finally, we found that individuals showed reduced aggression after being housed in groups, as expected under high levels of scramble competition. These results indicate that the pattern of resource acceptance in the presence of conspecifics may be better viewed as a response to increased scramble competition rather than as a response to public information about resource quality.
Keywords: conspecific attraction, experience, host choice, Rhagoletis, social facilitation, social information
Simple models of resource selection, such as ideal-free distribution (Fretwell and Lucas 1969), predict that animals should be less likely to use resources that are being used by potential competitors such as conspecifics. However, in many species, the presence of conspecifics increases an animal's propensity to use a resource (Clayton 1978; Muller et al. 1997; Onyabe and Roitberg 1997; Prokopy and Roitberg 2001; Otis et al. 2006). One explanation for this pattern is that animals use conspecifics as sources of information about the quality of resources (Stamps 1987; Prokopy et al. 2000; Dall et al. 2005). If individuals are attracted to or arrested by high-quality resources, for example, the presence of conspecifics can indicate the presence of a high-quality resource.
Although conspecifics may be a moderately reliable indicator of resource quality, they should be an even better indicator of competition. The presence of competitors on a particular resource will typically reduce the fitness of individuals using that resource. However, for animals conducting a sequential search, the presence of individuals on one resource can also indicate high levels of scramble competition for all resources in the local environment. Such high levels of local competition will favor individuals that are less selective and accept a wider range of resource quality more readily as the risk of resource depletion increases (Mitchell 1990; Van Alphen and Visser 1990; Visser 1991; Amita et al. 2010). For example, Plowright and Landry (2000) demonstrated that solitary pigeons prefer large seeds to small ones but that they more readily accept small seeds in the presence of a potential competitor. Therefore, another possibility—less often considered—is that increased response to resources in the presence of conspecifics reflects an adaptive response to perceived competition in the local environment.
Although the use of conspecifics to assess resource quality or competition can cause superficially similar responses in behavior (increased acceptance of resources), in certain contexts, the responses to the assessment of resource quality or competition should differ greatly. Therefore, by testing animals in different contexts, we can determine whether behavioral responses are better viewed as a response to information about competition or as a response to information about resource quality.
First, no-choice tests to measure the acceptance of low- and high-quality resources in the presence or absence of conspecifics are sensitive to changes in an animal's perception of resource quality, as well as its choosiness or selectivity (Singer et al. 1992; Davis 2008). Decreased choosiness in response to perceived competition should result in increased acceptance of low-quality resources, but little change in acceptance of higher quality resources. Alternatively, if conspecifics indicate increased resource quality, any resource associated with conspecifics should, regardless of intrinsic quality, be perceived as higher quality than it would without conspecifics and, barring a ceiling effect on maximum acceptance rate, be accepted more readily.
Furthermore, the location or timing of experience with conspecifics differentially affects the reliability of information about resource quality and competition. Conspecifics observed near a particular resource provide reliable information about that particular resource but less reliable information about the quality of other resources. Therefore, if individuals are primarily using conspecifics as indicators of resource quality, their response to the presence of conspecifics should be primarily restricted to resources directly associated with conspecifics. Alternatively, when conspecifics are used as indicators of local competition, then increased propensity to use resources should be seen at sites away from conspecifics and due to recent previous encounters with conspecifics.
Finally, aggressive behavior should be affected differently by information about resource quality and competition, so the effect of conspecifics on aggression can also be used to determine what type of information animals get from conspecifics. Animals should be more willing to invest in any territorial behavior required to monopolize resources of particularly high quality (Reichert 1998) but less willing if levels of scramble competition are very high (and the resource will be visited by multiple potential competitors; Dubois et al. 2003). Therefore, previous experience with conspecifics should increase aggressive behavior if those conspecifics indicate resource quality or high levels of interference competition but decrease aggressive behavior if those conspecifics indicate high levels of scramble competition.
In this paper, we test the context-dependent effects of conspecifics on oviposition decisions in the tephritid fruit fly, Rhagoletis juglandis, a species in which this phenomenon has not previously been studied. Tephritid fruit flies are a useful system to study the relative importance of conspecifics as potential competitors and as indicators of resource quality. Many species in this family lay their eggs in ripening fruit, providing a situation in which the presence of flies on a fruit might indicate the quality of that fruit and/or the risk of host depletion in a tree. In several species, females have been shown to lay eggs more readily when housed in groups (e.g., Prokopy and Bush 1973a; Robertson et al. 1995; Rull et al. 2003), but experiments on these species have not attempted to determine what type of information conspecifics provide. Using R. juglandis, we tested for the effect of conspecifics on resource acceptance and aggressive behavior in various contexts (i.e., on different quality hosts, and when conspecifics are spatially or temporally separated from hosts) to determine whether context-dependent patterns of the effect are better viewed as a response to information about competition or about quality.
Natural history
In southern Arizona, R. juglandis uses Arizona walnut, Juglans major, as its host. There is a single generation per year. Adult flies emerge between July and September, depending on elevation, from puparia in the soil beneath their natal tree. Females begin ovipositing in fruit 1 or 2 weeks after emergence. After oviposition, females deposit a host-marking pheromone (HMP) that deters oviposition (Nufio and Papaj 2004a). Nonetheless, females show a strong propensity to lay eggs within previously established oviposition cavities (Papaj 1993, 1994; Lalonde and Mangel 1994). Eggs hatch within 4 days, and larvae develop over the course of 2 weeks. Survival is higher and final size larger when larvae develop in larger walnuts (Nufio and Papaj 2001). Development is usually completed after the fruit fall to the ground, with larvae then leaving the fruit to form puparia in the soil beneath the natal tree. Puparia enter an obligate diapause until the following year.
General methods
All flies were collected as larvae inhabiting fruit that had fallen from J. major trees in southern Arizona. After pupation, flies were kept at 4 °C for at least 9 months and warmed to room temperature 4–6 weeks prior to each experiment. As adult flies began to emerge, pupae were transferred to 3.8 l plastic containers (emergence containers), held at 28 °C on a 14:10 light:dark cycle, and provided sugar cubes, powdered hydrolyzed yeast, and distilled water (delivered through a cotton wick) ad libitum. No hosts were provided at this time.
Experiments 1, 2, and 4 were conducted in 473-ml clear plastic cups (SOLO brand) topped with 10 cm petri dishes (experimental cups). Flies in all experimental cups were provided with water and a strip of paper dipped in a solution of hydrolyzed yeast and sugar. All cups were surrounded by white cardboard barriers to minimize extraneous visual stimuli. Mortality was relatively low (<10%) and not obviously biased toward particular treatments or collection locations.
Oviposition behavior was assayed in experiments 1 through 3 using 25 and 37 mm diameter artificial hosts wrapped in Parafilm as artificial walnut hosts. Spheres were prepared using a ratio by weight of 1:2:40 agar to sucrose to water. Two drops of yellow and 1 drop of green food coloring (Kroger brand) were added for every 200 ml of water. The solution was heated until boiling and poured into silicone molds (Chicago School of Mold-Making, Chicago, IL). Spheres were hardened at 4 °C and wrapped individually in Parafilm (2.5 or 4.0 cm2 pieces stretched over each sphere and twisted into a “stem”).
Experiment 1: do conspecifics affect oviposition decisions?
Flies used in this experiment were collected from the town square of Patagonia, AZ (lat 31°32′24″N, 110°45′14″ W). Female flies that had emerged 2–3 weeks earlier were removed from emergence cages and placed into experimental cups in one of 2 treatments: 1) held individually or 2) held in groups of 3. Flies were allowed to acclimate for 24 h, after which 25 mm diameter artificial hosts were suspended from the top of each cup. Artificial hosts and flies were removed after 48 h. Flies were frozen at −10 °C. The number of clutches and eggs laid in each artificial host were counted (eggs within clutches laid at the same site occurred in distinct groups, entering the sphere at different angles).
Flies were dissected under stereoscopy and digital images of the wings and dissected ovaries were captured with a Canon EOS 20D camera. We counted all fully yolked and chorionated oocytes (Stage E of egg maturation in Lachmann and Papaj 2001). Furthermore, because body size and oocyte number are known to be positively correlated, we used ImageJ (National Institutes of Health) software to measure the length of the discal medial cell of the wing. This wing measure was used as an estimate of female size because previous laboratory investigations demonstrated that it was strongly correlated with other indicators of female size such as thorax and head width and femur length (Alonso-Pimentel H, unpublished data).
This experiment was performed in 3 blocks (72-h periods) across several weeks. No block or block × treatment effects were found, so data were pooled across blocks. Binomial tests (see RESULTS) were conducted on the presence or absence of eggs in each artificial host. For those cases where eggs were present, the number of eggs or clutches was analyzed with an analysis of variance (Type III ANOVA). Egg load data were also analyzed with an ANOVA. All egg data required square root transformation to fit variance and normality assumptions (tested with Levene's and Shapiro–Wilk tests, respectively). All statistical tests were conducted with SPSS (v. 17.0 for Windows, SPSS Inc., Chicago, IL). All continuous data are reported with standard errors of the mean.
Experiment 2: does the effect of conspecifics depend on host quality?
To test for changes in choosiness in response to the presence of conspecifics, we conducted a pair of no-choice tests. Flies used in this experiment were collected from the town square of Patagonia, AZ. The experiment was set up similarly to experiment 1 but with a crossed design in which both host size and social condition were manipulated. Flies were housed alone or in groups of 3. Half of the cups in each social treatment received artificial hosts (25 mm diameter) identical to those in experiment 1 and half received larger artificial hosts (37 mm diameter). This experiment was performed in 3 blocks across several weeks. No block or block × treatment effects were seen, so data were pooled across blocks. Statistical analysis was conducted as described for experiment 1.
Experiment 3: is the effect of conspecifics restricted to the resource item on which conspecifics reside?
This experiment was designed to determine whether the presence of conspecifics resulted in a general increase in the propensity to oviposit as predicted by our competition hypothesis or whether increased oviposition was specifically directed at fruit near conspecifics, as predicted if females are responding to information about fruit quality. All females used in the experiment were collected from Canelo Hills Cienega Reserve (lat 31°33′40″N, long 110°31′46″W). Fly behavior was tested in 3.8 l plastic arenas. On either side of the arena, we placed a 297-ml clear plastic beverage cup (SOLO brand), which would hold test stimuli to which a focal female released into each arena could respond. A vial of water and a yeast/sugar strip were placed in the middle of the arena and in each cup. A pair of 25 mm artificial hosts attached with gardening wire was placed over the edge of each cup, such that one host was outside of cup and the other was inside the cup. The top of each cup was covered with square of cloth mesh to allow olfactory cues to escape into the arena (Figure 1a).
Figure 1
Figure 1
Design and results of experiment on spatial scale of conspecific effects. (a) Set up for all arenas in part 2 of experiment 3; 3.8-l box containing two 297-ml cups, one containing 12 female flies and each with 2 model walnuts, 1 inside the cup and 1 outside. (more ...)
During the first trial of this experiment, in half of the replicate arenas neither cup received females (n = 10), whereas in the other half of the arenas, 12 female flies were placed in one of the 2 cups (n = 10). In the second trial, conducted in 2 blocks, one of the 2 cups contained 12 females in all arenas (n = 40). To control for position effects, in each block, an equal number of arenas were set up with fly-containing cups placed on either side of the arena. Focal flies that had eclosed 2–3 weeks prior to the experiment were held singly outside of the arenas in 473-ml cups for 48 h prior to being introduced to arenas at 1100 on the first day of each trial. Arenas were scanned hourly from 1100 to 1800 for 2 days (number of scans per arena = 15). During these scans, we noted the side of the arena on which females were located and whether or not they were on one of the walnut models. Seventy-two hours after focal females were placed in the arena, walnut models were removed and the eggs laid in each model were counted.
Experiment 4: does previous experience with conspecifics increase oviposition response?
In this experiment, we used a crossed design to determine the roles of previous and current experience with conspecifics on the propensity of a female to oviposit. Flies used in this experiment were collected from a variety of sites in southern Arizona. We placed females within 2 days of eclosion into experimental cups. Half of the females were placed alone in a cup, the other half were held 10 to a cup (single- vs. group-rearing treatment). Flies were tested for their propensity to oviposit when they were 12–21 days old.
A test began by suspending a ripe J. major fruit by wire from the ceiling of a 17.2 × 17.2 × 17.2 cm plexiglass-frame screen cage. Fruit was 26–38 mm in diameter and had been previously punctured once with a 00 insect pin. Females are attracted to these pinpricks and oviposit in them, as they typically do with naturally formed oviposition punctures (Papaj 1994).
In half of the tests, we next placed a “resident female” gently on the test fruit; in the other half, the fruit was left unoccupied (resident vs. no resident treatment). The resident was a female of the same or similar population origin as the focal female. When placed on the fruit, the resident almost always began ovipositing into the artificial puncture. If the resident attempted to oviposit in other areas of the fruit, she was gently nudged toward the artificial puncture with a probe. Residents that did not oviposit within 5 min were removed.
A focal female from either the isolated or the grouped treatment was placed gently on a test fruit. If a resident was present, we placed the focal female on the fruit out of sight from the resident. We noted any oviposition attempts made by the focal female, as well as successful egg deposition. An oviposition attempt is a conspicuous behavior in which a female turns the tip of her abdomen down toward the fruit surface, extending her needle-like ovipositor, and bores into the fruit with the ovipositor. Oviposition, or egg deposition, begins when the ovipositor-boring female becomes virtually motionless. If a resident was present on the fruit, we also noted the occurrence and form of any aggressive interactions by the focal female. Aggressive interactions included lunges, chases, head butting, and foreleg kicking.
An observation ended when either the focal female had initiated oviposition or the focal female had left the fruit for at least 5 min. As soon as the observation ended, the focal female was frozen at −10 °C and measurements of body size and egg load were made under stereoscopy. Oviposition behavior was analyzed with a logit loglinear model. The improvement in model fit provided by each factor was assessed with chi-square tests.
Experiment 1: do conspecifics affect oviposition decisions?
Group housing increased the probability that flies oviposited in small artificial hosts. When held alone, 7 of 39 females laid eggs in the artificial host provided to them. Given this percentage of oviposition in isolation (=18%), if there were no effect of social treatment, eggs should have been laid in only 45% of the cups holding 3 females (1 − probability that none of 3 females in a cup lay eggs = (1 − [1 − 0.18]3 = 0.45)). In fact, eggs were laid in 81% (29 of 36) of the cups holding 3 females (exact binomial probability < 0.0001|expected = 45%).
Using the percentage of groups in which no female laid eggs (=19%), the probability (f) that a given female laid eggs when in the presence of 2 other females is: f = P (1 grouped female lays eggs) = An external file that holds a picture, illustration, etc.
Object name is behecoarr042fx1_ht.jpg. Thus, we estimate that the probability that a female lays any eggs in a small artificial host increases from 0.18 to 0.42 when she is housed with conspecifics.
Although social environment affected the probability of ovipositing, it did not affect the number or size of clutches laid per female. We estimated an average 1.56 females oviposited in grouped treatments where eggs were found (see APPENDIX). Given this estimate, each ovipositing female in grouped treatments (N = 29 cups) laid an average of 15.69 (±1.80) eggs and an average of 4.1 (±0.50) clutches. Isolated females that laid eggs (N = 7) laid an average of 11.00 (±3.22) eggs and an average of 2.86 (±0.86) clutches. These differences between ovipositing isolated and grouped females were not statistically significant (tsqrt(eggs) = 1.39, degrees of freedom [df] = 34, P = 0.17; tsqrt(clutches)=1.20, df = 34, P = 0.24). Furthermore, the size of individual clutches did not differ between treatments (grouped: 5.85 ± 0.50 eggs per clutch; isolated: 4.28 ± 0.79 eggs per clutch; teggs = 1.42, df = 34, P = 0.16).
Posttest dissections revealed that females housed in groups and females housed in isolation had similar egg loads at the end of the assay (isolated: average no. of mature oocytes = 24.7 ± 2.4.; grouped: average no. of mature oocytes per female: 24.6 ± 1.3; ANOVA: F1,69 < 0.01, P = 0.89). This indicates that egg load is unlikely to have been a mechanism driving differences in the probability of laying eggs. Because egg load was not affected by treatment, and 95% of all females contained eggs, we did not conduct dissections of females in experiments 2 and 3.
Experiment 2: does the effect of conspecifics depend on host quality?
The effect of social treatment was detected when small agar spheres were offered to females but not when they were offered large agar spheres. Controlling for social treatment, large spheres were more likely to contain eggs (85% contained eggs) than small spheres (52% contained eggs) (Mantel–Haenszel χ2 = 26.2, df = 1, P < 0.0001). As in experiment 1, only a small proportion of females held alone laid eggs in small spheres (11 of 45 = 0.24); the proportion of cups of grouped females in which eggs were laid into small spheres was greater than expected, based on oviposition by isolated females (expected proportion of spheres with eggs = 1 − [1 − 0.24]3 = 0.56; observed: 0.81 [33 of 41]; (exact binomial probability = 0.0009|expected = 56%)). As in experiment 1, females housed in groups with small spheres laid eggs with an estimated probability of An external file that holds a picture, illustration, etc.
Object name is behecoarr042fx2_ht.jpg .
When females were held in isolation with large spheres, a majority of females laid eggs (32 of 44 = 0.73). Given this high rate of acceptance, almost all large agar spheres housed with 3 females would be expected to contain eggs (expected prob.= 1 − [1 − 0.73]3 = 0.98) regardless of any effect of conspecifics. This expectation was met (observed: 98% (41 of 42); binomial test P = 0.8). Females housed in groups with large spheres laid eggs with an estimated probability An external file that holds a picture, illustration, etc.
Object name is behecoarr042fx3_ht.jpg.
We estimated that in cups of grouped females where eggs were laid, an average of 1.56 and 2.19 females per cup laid eggs in small and large spheres, respectively. The number of eggs laid per ovipositing female (square root transformed) was influenced by a marginally significant interaction between the size of the sphere and the social treatment (F(size)1,113 = 4.87, P = 0.03, F(social)1,113 = 4.20, P = 0.04, F(social × size)1,113 = 3.50, P = 0.06). Grouped females laid significantly more eggs in small spheres per ovipositing female than isolated females (t = 2.07, df = 42, P = 0.04), whereas grouped and isolated females laid a similar number of eggs in large agar spheres (t = 0.18, df = 71, P = 0.86; Figure 2a). We found no significant effects of sphere size or social treatment on the number of clutches laid per ovipositing female (F(size)1,113 = 0.88, P = 0.35, F(social)1,113 = 2.91, P = 0.09, F(social × size)1,113 = 2.04, P = 0.16; Figure 2b). Clutch size was not affected by sphere size or social treatment (F(size)1,113 = 2.17, P = 0.14, F(social)1,113 = 0.02, P = 0.89, F(social × size)1,118 = 0.08, P = 0.78; Figure 2c).
Figure 2
Figure 2
The effect of social environment and host size on oviposition behavior (experiment 2). Number of ovipositing females estimated as described in text. (a) Mean (+standard error of the mean [SEM]) number of eggs per ovipositing female. Shared letters indicate (more ...)
In summary, the effect of conspecifics on oviposition was not independent of sphere size; the effect was only detectable when flies were provided with small spheres. This result may indicate that the presence of conspecifics decreased choosiness, but we are faced with the possibility that the lack of an observed effect in the large sphere treatment was due to a ceiling effect. However, if grouped females were more likely to lay eggs than isolated females in the large sphere treatment (i.e., f > 0.73), then our estimate of the number of females ovipositing per cup (2.19) would be an underestimate. We would expect in turn that our estimate for the number of eggs per ovipositing female would be higher in groups than for isolated flies. This was not the case. In fact, our estimates of eggs laid per ovipositing female were nearly identical in isolated and grouped females with large spheres and for grouped females with small spheres (Figure 2a). If the probability of laying eggs in large spheres was any greater when flies were in groups, this would mean that grouped females laid fewer eggs per capita in large spheres than in small spheres. Therefore, it seems unlikely that the lack of an observed effect of social treatment on propensity to oviposit was due to a ceiling effect on the number of eggs each fly could lay.
Experiment 3: is the effect of conspecifics restricted to the resource item on which conspecifics reside?
The results of experiment 3 indicated the facilitating effect of conspecifics was not restricted to artificial hosts near those conspecifics. The first trial of this experiment indicated that the presence of females in one cup influenced the oviposition behavior of focal females in the arena. Only 2 of 10 females in arenas without conspecifics present laid any eggs. In contrast, 6 of 10 females in arenas with conspecifics present laid eggs. The difference is marginally significant (Fisher's Exact test, P = 0.08). The presence of females in one of the cups resulted in an increase in the percentage of scans during which the focal female was seen on either sphere (with flies: 2.37 (± 0.74) of scans; without flies: 0.97 (±0.31) scans; Mann–Whitney U test: U = 22, N1 = N2 = 10, P < 0.02). Given that only 2 isolated females laid eggs, we cannot statistically compare the clutch number or size, however, there was a trend for females in arenas with conspecifics to lay more and larger clutches (mean no. of clutchesisolated = 3.5; mean no. of clutcheswith conspecifics = 8.17; mean clutch sizeisolated = 1.8, mean clutch sizewith conspecifics = 3.4). Among the 10 pairs of cups that contained flies in one of the cups, no strong bias was observed toward or away from the cup containing the female cues. Data from these 10 pairs of cups were analyzed along with data from the 2 blocks of the second trial of this experiment to increase our statistical power to detect any bias toward or away from cup-containing conspecifics.
Fifty females across 3 blocks were tested for a tendency to spend time and/or lay their eggs near conspecifics. Females were observed more often on the sphere set away from conspecifics (t = 2.309, df = 49, P = 0.025). However, in general, focal females demonstrated no strong bias toward or away from conspecifics (Figure 1b). Females did not spend more or less time on the side of the cage with containing conspecifics (t = 0.122, df = 49, P > 0.91). Similarly, there was no difference in the number of clutches laid in either sphere (t = .379, df = 49, P = 0.76) or in the size of clutches laid on either side (t = 0.715, df = 12, P = 0.49; Figure 1b).
Experiment 4: does previous experience with conspecifics increase oviposition response?
Rearing flies in groups increased their propensity to lay eggs and decreased their level of aggressive behaviors. The probability that females attempted oviposition was higher for those reared with other females (χ2 =5.28, df = 1, P < 0.025). Similarly, the presence of a resident female on the host during testing, increased the probability that a female attempted oviposition (χ2 = 5.28, df = 1, P < 0.025) (Figure 3). There were marginally significant trends in same direction when analyzing the proportion of females that successfully oviposited (rearing treatment: χ2 = 3.52, df = 1, P < 0.06; resident presence: χ2 = 3.52, df = 1, P < 0.06) (Figure 3). There was no significant interaction between treatment factors on either attempted or successful ovipositions. Although nearly all the successful ovipositions were in the puncture provided (20 of 21 ovipositions when no conspecific was present; 31 of 33 when conspecific was present), oviposition attempts were not more frequent on the side of the fruit containing the puncture (pooled across treatments, proportion of attempts on puncture side = 0.51, tone-sample = 0.373, df = 80, P = 0.78).
Figure 3
Figure 3
Effect of previous and current social environment on egg-laying decisions (experiment 4). Bars represent proportion of flies in each rearing treatment that attempted to oviposit when presented with a fruit with or without a resident female. Lines represent (more ...)
When residents were present, the frequency of attacks by a focal female on a resident, measured in terms of lunges, head butts and foreleg kicks, depended on social history treatment, as well as whether or not females attempted oviposition (Figure 4). In both rearing treatments, females that attempted oviposition engaged in more attacks than females that did not attempt oviposition (reared alone: Mann–Whitney U = 172.0, Nattempt = 22, Nno attempt = 31, P = 0.001; reared socially: Mann–Whitney U = 279.0, Nattempt = 32, Nno attempt = 24, P = 0.042). Among females that attempted oviposition, those reared alone engaged in a markedly greater number of attacks on the residents than females reared in groups (Mann–Whitney U = 240.0, Nsocial = 32, Nisolated = 24, P = 0.038) (Figure 4).
Figure 4
Figure 4
Mean (+standard error of the mean) number of aggressive encounters (lunges, head butts, and foreleg kicks) in flies differing in social-rearing condition. Shared letters indicate nonsignificant differences (Mann–Whitney U test, α = 0.05). (more ...)
The effect of social history on egg laying and aggression was not due to an effect of rearing conditions on egg maturation. Among individuals used in the analysis (i.e., individuals with egg load >0), females held alone carried 27.62 (±1.57) mature oocytes on average (N = 75), whereas females held in groups carried 25.19 (±1.49) mature oocytes on average (N = 83). As in experiment 1, the difference in egg load is not statistically significant (t156 = 1.12, P = 0.26). Females from different social history treatments also did not differ significantly either in age or in wing vein length, a proxy for body size (t-tests, P > 0.26).
Our experiments demonstrate that the presence of conspecific females increases the probability that individual R. juglandis will lay eggs. Several species in the family Tephritidae show the same basic pattern, indicating that the social environment plays an important facilitating role in the oviposition decisions of this group (Prokopy and Bush 1973b; Robertson et al. 1995; Prokopy and Duan 1998; Prokopy et al. 1999; Díaz-Fleischer and Aluja 2003; Rull et al. 2003). This is particularly interesting because larval density has a negative effect on both size and survivorship in tephritid flies (Nufio and Papaj 2004b; Burrack et al. 2009), and many species, including R. juglandis, use HMPs after oviposition that inhibit superparasitism by conspecifics (Nufio and Papaj 2001).
In experiment 2, oviposition in large spheres (which represent superior resources; Nufio and Papaj 2004a) did not appear to be influenced by social treatment, whereas oviposition in small spheres was seen more often in group housed females. This quality-dependent response to conspecifics may reflect a reduction in choosiness in flies held in groups relative to flies held alone, a predicted response to higher levels of scramble competition (host depletion or larval competition). Alternatively, the lack of social effect seen when flies were held with large models may have been due to a ceiling effect. Although it is unlikely such a ceiling effect was due to a limitation in the number of eggs available for laying (see RESULTS), if the large models were perceived to be of extremely high quality, additional indications of quality (i.e., conspecifics) may not have affected how flies perceived them. However, it is unclear if model walnuts, which are only rough approximations of the flies' natural host, could possibly be perceived to be of such high quality.
The pattern of female aggressive encounters observed in experiment 4 also supports the hypothesis that females use the presence of conspecifics as an indicator of high competitor density. Females were more aggressive toward another female on a fruit when they attempted oviposition. The association between oviposition and aggression suggests that aggression functions to monopolize resources for a female's offspring (see also Papaj and Messing 1998). However, when flies were reared at high densities they were much less likely to engage in such aggressive behaviors. At high densities, fighting with the resident may have relatively little value because the fruit will likely be visited later and exploited often by other females (Nufio and Papaj 2004b). In fact, fighting with the resident under these conditions may incur an opportunity cost related to finding and utilizing other fruit. On the other hand, at low to intermediate competitor densities there is a relatively high payoff to a female that fights with a resident female, if such fighting expels the resident from the fruit before her clutch is completed (Dubois et al. 2003).
The patterns of oviposition observed in experiments 3 and 4 do not support the hypothesis that females use the presence of females as indicators of the quality of particular fruit. In experiment 3, when given a choice between hosts near or away from conspecifics, females did not oviposit more near conspecifics and in fact alighted more often away from conspecifics (Figure 1b). A similar pattern has been observed in Anastrepha ludens (Díaz-Fleischer and Aluja 2003). Similarly, in experiment 4, the resident female could have provided inadvertent social information about the location of an area on the fruit that was especially appropriate for oviposition. However, females did not appear to use such information as they did not obviously position their oviposition attempts near the resident females. Finally, in experiment 4, previous encounters with conspecifics, which should have provided little information about the quality of the resource provided during the test, affected both aggression and oviposition efforts (Figure 3).
In summary, the pattern of social stimulation of oviposition (and concurrent inhibition of aggression) observed in R. juglandis seems best viewed as a response to increased competition in the local environment. Thus, social stimulation of oviposition in tephritid flies may represent a case in which animals increase acceptance of a resource in the presence of conspecifics, even if conspecifics provide no information about the quality of that resource.
Theory predicts that the information value of a cue such as the presence of conspecifics depends on how reliably that cue is associated with the environmental factor of interest and how uncertain that factor is when the cue is unavailable (Stephens 1989; McLinn and Stephens 2006; Hall and Kramer 2008). As such, it is unsurprising that walnut flies behave as though conspecifics provide them information about competition that is more valuable than information they provide about the quality of resources. First, it is reasonable to assume that the presence of conspecifics is reliably correlated with level of competition present in the environment because conspecifics are the source of that competition. Any correlation between conspecific presence and resource quality is probably weaker than the correlation between conspecific presence and the level of competition because it relies on the conspecifics ability to identify high-quality larval resources. Furthermore, it seems likely that in the absence of conspecific cues, individuals will not be able to estimate the level of competition they will encounter. Conversely, individuals can use size and perhaps chemical cues to determine the quality of walnuts.
Recently, the idea that conspecifics provide “public information” about resource quality has gained increasing attention (Danchin et al. 2004; Dall et al. 2005). Discussion of the use of public information often implicitly assumes animals are choosing among several available resources (using a “best-of-n” search strategy), where the relative fitness gain of accepting one of the sampled resources is the major factor in adaptive choice. When this is the case, if 2 resources are of equal intrinsic quality then individuals are expected to choose the resource where competition will be lower (typically, the resource without conspecifics). Therefore, in those cases where animals choose resources that contain conspecifics, it is concluded that the conspecifics must be providing information about intrinsic resource quality.
Although there seems little doubt that animals use the presence and behavior of conspecifics as indicators of resource quality, when considering animals that sequentially search for resources it is important to consider that adaptive decision making is based not only on the quality of a given resource but also on the distribution of quality in the local environment. Individuals using sequential search can use the presence of conspecifics on a resource not only as an indicator of quality and the level of competition for that resource but also of the quality and level of competition in the local environment. Our results indicate that using conspecifics as indicators of local levels of competition can affect decision making in ways that are superficially similar to using conspecifics as sources of information about resource quality.
FUNDING
Natural Resource Institute (9702562 to R.J.P.); National Institutes of Health (GM00708) to the Center for Insect Science, University of Arizona.
Supplementary Material
Lay Summary
Acknowledgments
We acknowledge R.J. Prokopy for helpful discussions on experimental design S. Duffy, J. Hoyos, and K. Hobaica for technical assistance and 2 anonymous reviewers for assistance improving the manuscript.
APPENDIX
We estimated the number of females that were responsible for the eggs found in spheres in order to obtain a “per ovipositing female” estimate of clutch number in cups containing 3 females. The mean number of females laying eggs in spheres where eggs were found (x) was estimated as:
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where f is the probability of ovipositing and q = (1 − f). In experiment 1, given each group-housed female has a probability, f = 0.42, of laying eggs, an estimated mean x = 1.56 females held in groups contributed to the total number of eggs laid by the group.
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