Age-related changes in characteristics and prey capture of seasonal cohorts of Sarracenia alata pitchers.
|Abstract:||The characteristics associated with prey attraction and capture in pitcher plants are not well understood. Because of physiological constraints due to growth patterns and resource availability, pitcher characteristics should vary among seasonal cohorts and with pitcher age. We measured age-related changes in characteristics (funnel diameter, extrafloral nectar guides, extrafloral nectar concentration) and in prey capture of early- and mid-season cohorts of Sarracenia alata pitchers. Pitchers achieved their mature height before opening, and pitchers of the mid-season cohort were smaller than those produced early in the growing season. In both cohorts, extrafloral nectar concentration on the lip of the pitcher and the number of "secondary nectar guides" (an indication of hood coloration) were highest approximately 3 wk after pitchers opened. The rate of insect capture in both cohorts was highest approximately 3 wk after pitchers opened, corresponding with the peak in nectar concentration and the maximal number of secondary nectar guides observed. The mean intact insect capture from the four main collections (the three sampling periods for Cohort A and the single period for Cohort B) was significantly positively related to mean nectar concentrations for those collections. When pitchers were capturing at their maximal rate (3 wk after opening), prey capture per unit size per unit time was higher in the mid-season cohort even though nectar concentration was not significantly different than that in the early-season cohort. Furthermore, ants comprised a significantly greater proportion of intact insects captured by the mid-season cohort. The results of this study show that characteristics of pitchers and their effect on prey capture vary between seasonal cohorts and with pitcher age. Nectar appears to be an important attractant, and foraging insects may be attracted by nectar, coloration, or most likely by some combination of these and other characteristics. The physiological constraints and evolutionary pressures leading to these differences need to be examined.|
Predation (Biology) (Research)
Horner, John D.
Steele, Julie Cross
Underwood, Christopher A.
|Publication:||Name: The American Midland Naturalist Publisher: University of Notre Dame, Department of Biological Sciences Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Earth sciences Copyright: COPYRIGHT 2012 University of Notre Dame, Department of Biological Sciences ISSN: 0003-0031|
|Issue:||Date: Jan, 2012 Source Volume: 167 Source Issue: 1|
|Topic:||Event Code: 310 Science & research|
|Geographic:||Geographic Scope: United States Geographic Code: 1USA United States|
Carnivorous plants typically inhabit sunny, wet, nutrient-poor habitats (Schnell, 2002; Givnish et al., 1984; Givnish, 1989; Juniper et al., 1989). They have evolved a number of mechanisms by which they capture animal (usually insect) prey, which supplements the nutrients acquired from the soil (reviews in Schnell, 2002; Givnish, 1989; Juniper et al., 1989). Prey capture has been shown to increase fitness (survival, growth, and/or reproduction) of carnivorous plants (e.g., Karlsson and Pate, 1992; Thum, 1988, 1989; Zamora et al., 1997). Because of their impact on the fitness of carnivorous plants, it is important to understand the traits that affect prey capture and the factors that may cause changes in these traits.
A number of traits of pitcher plants have been implicated as attractants (reviewed in Juniper et al., 1989; Schnell, 2002), including extrafloral nectar (e.g., Cresswell, 1993; Merbach et al., 2001; Bennett and Ellison, 2009), color (e.g., Joel, 1986; Cresswell, 1993; Schaefer and Ruxton, 2008), patterns of reflectance and absorbance of ultraviolet radiation (Joel et al., 1985; Joel, 1986; Moran, 1996), and odors (e.g., Jaffe et al., 1995; Moran, 1996; Bauer et al., 2009; Jurgens et al., 2009). Pitcher size has also been demonstrated to be important in prey capture in pitcher plants (Cresswell, 1993; Heard, 1998; Green and Horner, 2007; Bhattarai and Horner, 2009), and this may be due to the relationship between pitcher size and/or number and the total quantity of attractants produced (Bhattarai and Horner, 2009).
The characteristics of pitchers are not static, but instead they change as pitchers age. For example, both color (e.g., Fish and Hall, 1978) and nectar production (e.g., Cipollini et al., 1994) have been shown to vary with pitcher age in Sarracenia purpurea. If prey capture is affected by pitcher traits, and if pitcher traits vary temporally, then prey capture may differ among pitchers of different age. For example, prey capture in S. purpurea has been shown to vary with pitcher age, ostensibly because of changes in attractants (e.g., Fish and Hall, 1978; Wolfe, 1981). Similarly, both pitcher characteristics and prey capture have been shown to vary temporally in Nepenthes (Bauer et al., 2009).
However, phenological changes in pitcher characteristics are not the only way in which pitcher plants may exhibit dynamic variation and adaptation. In North American pitcher plants, cohorts of pitchers are produced throughout the growing season, so populations are composed of pitchers of various ages. Just as the characteristics of pitchers can be expected to change as they age, physiological constraints and evolutionary pressures may lead to differences in traits of pitchers produced at various times during the growing season. For example, the allocation of resources to storage and to the production of new pitchers varies over time (Butler and Ellison, 2007), and this should lead to differences in characteristics of pitchers produced at different times during the growing season. If cohorts of pitchers do, in fact, differ in characteristics that affect prey attraction, then prey capture should vary among cohorts. However, relatively little attention has been directed at examining the differences in characteristics and prey capture among cohorts of pitchers (but see Heard, 1998).
Sarracenia alata is a rhizomatous, perennial herb that inhabits bogs along the Gulf coast from Texas to Alabama (Schnell, 2002). In S. alata, the pitchers are erect, relatively slender, and taper to a very narrow base. The tip of the leaf forms a flap, or "hood," that extends over the pitcher opening approximately perpendicular to the axis of the pitcher. However, the hood does not occlude the opening. As they mature and age, the hood and the upper portion of the pitcher usually produce red-colored veins that contrast with the photosynthetic green tissue. We refer to these red veins as "nectar guides," since extrafloral nectaries are located along these lines in at least some species (Joel, 1986), and they may act as an attractant (Joel, 1986; Juniper et al., 1989). Surrounding most of the opening of the pitcher is a swollen portion of tissue called the peristome or "lip." Nectar is commonly found on the lip and other surfaces of the pitcher (Schnell, 2002).
The pitcher-shaped leaves are both photosynthetic and serve as pitfall traps for insects. (For a detailed description of the trapping mechanism, see Juniper et al., 1989.) In S. alata as in other species of Sarracenia, prey are ostensibly attracted by pitcher color, odor, and/or nectar (Green and Horner, 2007; Bhattarai and Horner, 2009). While extrafloral nectaries have been observed over the entire pitcher, they are concentrated around the lip or peristome and immediately inside the mouth of the pitcher. If potential prey lose their foothold, they fall into the pitcher, and egress from the pitcher is minimized by downward-pointing hairs. Prey includes insects from more than ten orders of insects, but the majority of the mass consists of ants (Green and Homer, 2007; Bhattarai and Horner, 2009). Once prey items have been captured, they are digested by a combination of enzymes secreted from the cells of the pitcher wall and the activity of commensal organisms, such as larvae of sarcophagid flies and the mosquito genus Wyeomyia (Schnell, 2002; Juniper et al., 1989). Mineral nutrients are then absorbed by the plant (e.g., Plummer and Kethley, 1964; Chandler and Anderson, 1976; Christensen, 1976; reviewed in Juniper et al., 1989; Adamec, 1997), which has been shown to enhance reproduction and other aspects of fitness in some carnivorous plant species (e.g., Karlsson and Pate, 1992; Thum, 1988, 1989; Zamora et al., 1997).
Sampling prey capture in Sarracenia alata is complicated by pitcher shape. Although numerous attempts have been made to develop a methodology that allows repeated sampling of prey from the same pitcher, the long, slender structure of S. alata pitchers renders it difficult or impossible to remove prey without damaging the pitcher. Therefore, we could not repeatedly sample prey capture in the same individual pitchers as can be done in some species of pitcher plants. Instead, we measured age- and season-related differences in pitcher characteristics and prey capture among individuals of cohorts (i.e., groups of individual pitchers of similar physiological age).
We established 10, 10-m transects separated by at least 1 m on 14-15 Apr. in a natural hillside seepage bog in Kisatchie National Forest, near Natchitoches, LA, USA (31[degrees]30'N, 93[degrees]4'W). Newly opened pitchers closest to every 30-cm, 60-cm, and 1-m mark (30 pitchers per transect, 300 pitchers total) were tagged prior to any prey capture and designated "Cohort A." In order to allow comparison of characteristics and prey capture of the early-season cohort of pitchers produced in Apr. to those of a mid-season cohorts of pitchers, 100 additional newly opened pitchers (10 pitchers per transect) were tagged on 4-5Jun. (prior to any prey capture) and designated as "Cohort B." The sampling regime was as follows (summarized in Table 1).
For each age and cohort of pitchers sampled, prey capture was measured over a 3 wk period. This period was chosen to allow sufficient time for measureable prey capture to occur but to minimize the loss of insect mass by decomposition. To serve as a marker indicating the beginning of the 3 wk period of prey capture ("time zero") for each sample of pitchers, a small piece of cotton was gently pushed into the base of each of 100 tagged pitchers (10 per transect) separated by at least one meter 3 wk prior to sampling for prey capture. The pitchers were then allowed to trap insects for approximately 3 wk. The cotton marker allowed us to distinguish the prey captured over the 3 wk period from that captured previously.
Prey capture in Cohort A was measured oi1 three dates following pitcher opening (12-13 May, 4-5 Jun., and 24-25 Jun.). Thus, on 14-15 Apr. (when pitchers had just opened and there had not yet been any insect capture), cotton markers were inserted into 100 pitchers, which would be collected on 12-13 May. On 12-13 May, cotton markers were inserted into 100 pitchers, which would be collected on 4-5Jun. Finally, on 4-5Jun., cotton markers were inserted into the pitchers to be collected on 24-25 Jun. Prey capture in Cohort B was measured on one date following pitcher opening. On 4-5 Jun. (the day that Cohort B was established), cotton markers were inserted into newly opened pitchers (prior to any prey capture) to be collected on 24-25 Jun. Thus, the sampling of prey capture for Cohort B corresponded with the last sampling of prey capture for Cohort A. On the collection dates, pitcher characteristics (see below) were measured, and each undamaged pitcher was cut at the base and placed together with its contents in a snap-cap vial and placed on ice. Upon returning to the lab, the vials containing pitchers and their contents were filled with 70% aqueous ethanol for preservation.
We measured pitcher characteristics of 50 randomly selected pitchers of each cohort on the dates that the cohorts were established and tagged (prior to any prey capture). Pitcher characteristics were also measured on capturing pitchers immediately prior to collection for determination of prey capture (see above). The height of the pitcher (from the substrate to the lip along the rib), funnel diameter, and hood height and width were measured to the nearest mm. We then took samples of nectar from the peristome ("lip") by the method of McKenna and Thomson (1988) as modified by Green and Horner (2007). Using forceps, we dampened a 1-cm2 piece of filter paper with deionized water and placed it on the lip for five seconds. The nectar sample from each pitcher was placed in a separate screw-cap vial on ice for transport to the laboratory. All nectar samples were collected in the morning in order to standardize for any potential diel variation in nectar content (Deppe et al., 2000). We also determined an index of the area of the hood covered with nectar guides. Nectar guides on the hood originate near or slightly below the level of the peristome. Each of these was termed a "primary nectar guide." The first-order branches from the primary nectar guides were termed "secondary nectar guides." We counted the number of secondary nectar guides as an estimate of the proportion of the underside (abaxial side) of the hood covered by nectar guides.
Analysis of prey capture.--The contents of pitchers above the cotton markers were sorted under a dissecting microscope into intact, identifiable insects and unidentifiable mass (principally composed of partially digested insect exoskeletons, hereafter called "detritus"). Thus, detritus was the decomposed remains of insects captured earlier in the 3 wk capture period. In contrast, intact insects represent those that were captured closer to the time of sampling (or possibly those with relatively hard exoskeletons that resist decomposition). Commensal insect larvae (primarily larvae of sarcophagid flies and pitcher plant mosquitoes) and commensal arachnids (mites and spiders) were excluded from the samples. Intact insects were identified to order (using Borror and DeLong, 1971) and were transferred to new Petri dishes. Then the insects and detritus were dried at 60 C to a constant mass (for a minimum of 3 d). Dry mass (to the nearest 0.1 rag) was determined for each order and the detritus. A value of 0.01 mg was assigned for negligible mass. The total mass of prey capture was determined for each pitcher as the sum of the mass of intact insects and of detritus. Since the number of capture days varied slightly among sampling dates, all capture data were expressed as mass per day.
Analysis of nectar samples.--Nectar samples on wicks were stored in individual vials on ice in the field. Immediately upon return from the field, the nectar samples were dried in an oven at 60 C for 3 d, then sealed in their screw-cap vials, and stored at room temperature. For analysis, 3 ml deionized (DI) water were added to the screw-cap vial containing the wick to re-dissolve the sample. The vial was agitated on a vortex mixer, and the wick remained in contact with the water for 10 min before centrifugation (to precipitate potentially interfering cellulose fibers from the filter). A sample (1.5 ml) of the nectar solution was analyzed using the anthrone colorimetric technique (Cresswell, 1993; as modified by Green and Horner, 2007). Because this technique is based on comparison to a sucrose standard curve, the units are reported in [micro]g sucrose equivalents per ml ([micro]g SEq/ml) for each of the nectar samples.
Statistical analysis.--Differences in plant characteristics among sampling dates and cohorts were examined by incompletely cross-classified two-factor analyses of variance (ANOVA). Since characteristics related to pitcher size are strongly correlated (Green and Horner, 2007; Bhattarai and Horner, 2009), funnel diameter was the only metric of size used in the analyses. The dependent variables were funnel diameter, number of secondary nectar guides, and nectar concentration. The independent variables were cohort (2 levels, A and B) and sampling date (4 levels for cohort A, 2 levels for cohort B), both of which were treated as fixed factors. When significant differences were indicated by the overall analysis, differences among cohorts and sampling dates were further assessed by Tukey's multiple range tests.
Differences in prey capture among sampling dates and between cohorts were examined using similar analyses, except that there were only three levels for sampling date for cohort A and one level for sampling date for cohort B. The dependent variables were detritus mass/day, mass of ants/day, mass of insects other than ants/day, total mass of insects/day, and total mass of insects + detritus/day. When indicated by significant differences in the overall model, differences among cohorts and sampling dates were further assessed by Tukey's multiple range tests.
In order to determine whether early- and mid-season cohorts capture qualitatively different prey, we compared the proportion of the total prey consisting of ants in physiologically similar-aged pitchers (3 wk after pitcher opening) of the two cohorts. The proportion of total insects captured that consisted of ants was arcsine- transformed before analysis by t-test.
Plant characteristics related to prey capture were analyzed by forward stepwise regression. The dependent variables for prey capture that were assessed were the same as above, and the independent variables were funnel diameter, number of nectar guides, and sugar concentration in nectar. The criteria for entering the regression were that the variable had to improve the coefficient of determination by at least 0.05 and the overall equation had to be significant.
In all analyses, a significance level of 0.05 was used. All statistics were performed with SPSS Version 17.0, SPSS Inc. Headquarters, Chicago, IL) and in Microsoft Excel 2007.
Funnel diameter was significantly affected by cohort but not by date or the date cohort interaction (Table 2). The second cohort of plants had significantly smaller funnel diameters than did the early-season cohort (Fig. 1A). Within a cohort, there were no significant changes in funnel diameter over time. These trends were true for pitcher height as well. [Since size variables were strongly correlated (Table 3), only data for funnel diameter are shown.]
The number of secondary nectar guides was affected by date, cohort, and their interaction (Table 2). For both cohorts, pitchers from the first sampling date had fewer secondary nectar guides than those from subsequent sampling dates (Fig. 1B). In the first cohort, the number of secondary nectar guides was highest during the second sampling and then decreased in the two later dates, possibly due to the obscuring of individual guides by a general increase in red pigmentation (see below). The number of secondary nectar guides in the second sampling of the first cohort was significantly higher than that in the second sampling of the second cohort even though the developmental or physiological age of the pitchers was similar (i.e., 3 wk after pitcher opening).
Nectar concentration was significantly affected by date and the date x cohort interaction but not by cohort (Table 2). The nectar concentration was lowest on the first sampling and highest on the second sampling in both cohorts (Fig. 1C). In the first cohort, the nectar concentration decreased in subsequent samplings. Nectar concentration was significantly correlated with the number of secondary nectar guides (Pearson's partial coefficient = 0.334, n = 183; P < 0.001).
Prey included ants, coleopterans, dipterans, hemipterans, homopterans, collembolans, lepidopterans, and thysanopterans. (Counts and mass of orders of insects captured are available upon request from the corresponding author.) The mass of detritus represented the greatest mass captured and was several times that of intact prey.
There were no significant effects of either date or cohort on the mass of ants captured or the mass of intact insects other than ants captured. However, there was significantly more intact insect mass captured on the first sampling date for prey capture than on subsequent sampling dates (Table 4, Fig. 2A). There was a significant effect of cohort but not of date on the mass of detritus (Table 4). There was significantly more detritus in the sole sampling of the second cohort than in any single date in the first cohort (Fig. 2B). As with detritus, the total mass (intact insects + detritus) captured was significantly affected by cohort but not by date (Table 4). Since detritus mass was several times the mass of intact captured insects, detritus mass was the major determinant of the mass of total prey capture. Again, the total mass captured by the second cohort was greater than that captured on any sampling date by the first cohort (Fig. 2C).
[FIGURE 1 OMITTED]
When prey capture was regressed against pitcher characteristics, we found that both detritus mass and mass of total capture (detritus + intact insects) significantly increased as a function of pitcher size (funnel diameter). However, the coefficients of determination were low when cohorts were combined for the analysis [detritus mass = 0.31 (funnel diameter) 0.93, FI,234 = 25.482, P < 0.001, adjusted [r.sup.2] = 0.094; total mass of prey capture = 0.32 (funnel diameter) - 0.99, [F.sub.1,234] = 26.44, P < 0.001, adjusted [r.sup.2] = 0.098; respectively]. Because pitchers in the mid-season cohort were smaller than those in the early- season cohort and because several measures of prey capture differed between cohorts, we examined the relationship between prey capture and size for pitchers of similar physiological ages (3 wk after opening) from the two cohorts separately. When cohorts were analyzed separately, there was no statistically significant relationship between total mass of prey capture and funnel diameter in the early-season cohort. In contrast, funnel diameter explained 52% of the variation in total mass of prey capture in the mid-season cohort (Fig. 3). The proportion of the total intact insects captured that consisted of ants was significantly greater in the mid-season cohort (0.41 [+ or -] 0.47, mean [+ or - ] SD) than in the early-season cohort [0.23 [+ or -] 0.38; t = -2.04; df = 95; P = 0.022]).
The mass of total insects captured was significantly related to nectar concentration, but again the coefficient of determination was low [mass of total insects = 0.13x + 0.052, [F.sub.1,234] = 4.20, adjusted [r.sup.2] = 0.013). There were no other statistically significant relationships between numbers or mass of prey capture and plant characteristics for individual plants.
Mean intact insect capture from the four main collections (the three sampling periods for Cohort A and the single period for Cohort B) was significantly related to mean nectar concentrations for those collections (P < 0.046; Fig. 4). No other relationships between insect capture and plant characteristics at the population level were statistically significant.
Carnivorous plants capture and digest animal (usually insect) prey in order to supplement the nutrients they can acquire from the nutrient-poor soils that they inhabit. The purpose of this study was to examine how some traits purportedly associated with prey capture change over time, whether these traits differ between cohorts of pitchers, and how the differences in these characteristics are related to prey capture. We found that the quantity of nectar and nectar guides changed as pitchers aged, and that cohorts of pitchers differed in size, in the relationship between size and rate of prey capture, and in the types of prey captured. We also found that prey capture was positively correlated with nectar concentration at the population level.
[FIGURE 2 OMITTED]
[FIGURE 3 OMITTED]
CHANGES IN PITCHER CHARACTERISTICS WITH AGE
Pitchers in both cohorts had achieved their maximum size by the time pitchers opened, as indicated by the fact that there were no significant effects of sample date or the sample date x cohort interaction on pitcher height or funnel diameter. Other Sarracenia species have been reported to attain their maximum height by the time pitchers open (Juniper et al., 1989).
In contrast to the static size of pitchers after opening, both nectar concentration and the number of secondary nectar guides varied with pitcher age after opening. For both cohorts, the nectar concentration was higher on pitchers approximately 3 wk after opening than it was on newly opened pitchers. In the early-season cohort (for which we had subsequent samples at approximately 6 and 9 wk after opening), nectar concentration decreased after the peak at 3 wk. This is similar to observations by Cipollini et al. (1994), who observed higher nectar concentrations in pitchers of Sarracenia purpurea that had recently reached maturity than in older pitchers. Interestingly, we found that the number of secondary nectar guides exhibited a pattern similar to that observed for nectar and was in fact significantly correlated with nectar concentration. Thus, insects foraging for nectar (i.e., potential prey) could utilize nectar guides on the hood as an indication of the presence of nectar. Fish and Hall (1978) also observed changes in pitcher coloration with pitcher age in S. purpurea, and Cresswell (1993) found that nectar concentration and striping on the hood of S. purpurea were positively correlated at the time of his sampling. Joel (1986) observed that nectaries are associated with nectar guides (pigmented veins) in Sarracenia, calling them "nectariferous lines." This could explain the correlation between nectar concentration and the number of secondary nectar guides. Although there are not nectar guides on the lip (peristome), extrafloral nectaries over the entire pitcher surface may mature at approximately the same time. Red pigmentation in the pitchers generally increased over the growing season, and the apparent decrease in number of secondary guides in later samplings was probably due to individual guides being obscured by this general darkening (i.e., increase in red pigmentation) of the hoods. Therefore, as pitchers age, the relationship between nectar guides and nectar concentration may weaken. Rather than counting nectar guides, we strongly recommend using another method for recording changes in hood coloration, such as making a photographic record or scanning the pitcher hoods (e.g., Green and Horner, 2007; Bhattarai and Horner, 2009).
[FIGURE 4 OMITTED]
DIFFERENCES BETWEEN COHORTS IN PITCHER CHARACTERISTICS
The mid-season cohort of pitchers (Cohort B) was significantly smaller than the early-season cohort in both height and funnel diameter. This is consistent with observations in Sarracenia leucophylla (Juniper et al., 1989) and in S. purpurea (Butler and Ellison, 2007). Differences in pitcher size between cohorts may be the result of physiological constraints, selection pressures, or both. The first cohort of pitchers is initiated from reserves stored in rhizomes during the previous growing season(s) (Butler and Ellison, 2007). Since pitchers produced early in the growing season potentially have a longer functional life span (growing season) than pitchers produced later in the growing season, the total seasonal resource acquisition through photosynthesis and/or insect capture is potentially greater in the former than in the latter. Therefore, natural selection might favor the production of larger pitchers early in the growing season. In contrast, pitchers produced later in the growing season are likely produced from a combination of stored reserves and resources recently acquired by the first cohort of pitchers (Butler and Ellison, 2007). However, as the growing season progresses, a greater proportion of acquired resources is probably allocated to storage (Butler and Ellison, 2007). Therefore, the size of pitchers produced later in the growing season is probably physiologically constrained by the fact that recently captured resources are being divided between new pitcher production and storage. Furthermore, natural selection may have favored this allocation strategy if greater availability of insects (potential prey) late in the growing season allows for a greater quantity of prey capture by smaller pitchers. (See below.)
In contrast to differences in pitcher size, there were no significant differences between cohorts in nectar concentration on pitchers of a similar developmental or physiological age. That is, the nectar concentrations on pitchers of Cohort A upon opening and at approximately 3 wk after opening (on 15 Apr. and 13 May, respectively) were similar to those on pitchers of Cohort B upon opening and at approximately 3 wk after opening (on 4 Jun. and 25 Jun., respectively). An increase in nectar concentration a few days after pitcher opening has also been reported in Nepenthes rafflesiana (Bauer et al., 2009) and suggested in Sarracenia purpurea (Wolfe, 1981).
RELATIONSHIP BETWEEN PREY CAPTURE AND PITCHER CHARACTERISTICS
Prey capture has been reported to be positively related to pitcher size in several studies (Cresswell, 1993; Heard, 1998; Green and Horner, 2007; Bhattarai and Horner, 2009). Bhattarai and Horner (2009) demonstrated that the relationship between prey capture and pitcher size in Sarracenia alata was not due to differences in capture area alone, but instead was consistent with the hypothesis that larger pitchers produce more attractants. In the present study, we also found a positive relationship between pitcher size and prey capture in the mid-season cohort, but the coefficients of determination were low.
When we regressed mean intact insect capture from the four main collections (the three sampling periods for Cohort A and the single period for Cohort B) on mean nectar concentrations for those collections, we found a highly significant, positive relationship (Fig. 4). This suggests that pitchers in the population with the highest nectar concentration (i.e., those that have been open for approximately 3 wk) lure a greater number of foraging insects and/or entice insects to spend more time foraging, increasing the probability of capture. Nectar has been suggested as an attractant in a number of studies (e.g., Joel, 1986; Juniper et al., 1989; Bennett and Ellison, 2009). A relationship between nectar concentration on pitchers and insect capture rates in situ has been demonstrated in this study and by Cresswell (1993). Foraging insects may be lured by the nectar itself, or they may be alerted to the nectar by visual cues such as pitcher coloration (Schaefer and Ruxton, 2008; this study). They may also be lured by odors (Jaffe et al., 1995; Moran, 1996; Bauer et al., 2009; Jurgens et al., 2009) or by a combination of characteristics such as visual and olfactory cues (Juniper et al., 1989; Green and Hornet, 2007; Bhattarai and Horner, 2009). More foraging studies of insects at carnivorous plants such as those carried out by Newell and Nastase (1998) are needed (Juniper et al., 1989).
SEASONAL VARIATION AND DIFFERENCES BETWEEN COHORTS IN PREY CAPTURE
The mass of intact insects captured per day in pitchers of Cohort A was maximal 3 wk after pitchers opened and then decreased as pitchers aged. This pattern, which was similar to the pattern observed in nectar on the peristome, could result from a decrease in prey attraction as pitchers age, a decrease in efficiency of prey capture and/or retention by older pitchers, and/or a decrease in prey availability as the growing season progressed. Additionally, the lower number of intact insects recovered from older pitchers could actually be due to a greater rate of decomposition due to the higher temperatures later in the growing season. A decrease in prey availability during the growing season is unlikely, because the mass of detritus and the total mass captured per day by the late-season cohort (Cohort B) were significantly greater than in the early-season cohort (Cohort A). There is no reason to suspect that the retention of prey decreases as the growing season progresses. However, the efficiency of prey capture may decrease as pitchers age. For example, if the nectar serves not only as an attractant but also as a slippery mucilage that causes visiting insects to lose their foothold (Bauer et al., 2008), then the decrease in nectar as pitchers age could lead to a lower efficiency of prey capture. Although this effect of nectar has been demonstrated in Nepenthes (Bauer et al., 2008), it has not been demonstrated in Sarracenia. Higher temperatures leading to a higher rate of decomposition cannot be discounted, but this would lead to a lower value of total mass of prey captured later in the season (which wasn't observed), not to the observed lower numbers of prey. Thus, it seems that a decrease in prey attraction is a plausible explanation for the decrease in the capture of intact insects in pitchers older than 3 wk. Future studies on prey capture should always include concomitant measurement of prey availability (Givnish, 1989; Ellison and Gotelli, 2009). When doing so, researchers need to ensure that the methods employed to measure prey availability are appropriate and relevant to their study. For example, pitfall traps, sticky traps, vacuums, and direct observation of visitors to carnivorous plants all measure different assemblages of organisms with different levels of effectiveness. Therefore, it would be valuable to know the relationship between prey capture in carnivorous plants and insect abundance measured by these different methods of assessment.
At the time of maximal prey capture (i.e., 3 wk after pitcher opening), there were differences between cohorts in the relationship between capture rate and pitcher size. Pitchers in the mid-season cohort (Cohort B) had a higher rate of insect capture per unit size than pitchers in the early-season cohort (Cohort A; Fig. 3). Since nectar concentration was not different between pitchers of the two cohorts, this suggests that the availability of insects (potential prey) may have been higher in Jun. than in May and/or that attractants other than nectar (e.g., nectar guides, odors, etc.) differ between cohorts. It is also interesting that the qualitative composition of captured prey differed between early- and mid-season cohorts of pitchers. A greater proportion of the mass of intact prey in the mid-season cohort of pitchers consisted of ants. Several authors have suggested that different species of carnivorous plants "specialize" on different groups of insects or partition available prey (e.g., ants vs. flying insects; Gibson, 1983; reviewed in Givnish, 1989;Juniper et al., 1989). Whether the differences in prey capture by early- and mid-season cohorts of pitchers in this study represent prey partitioning or specialization would depend on studies of prey availability (Givnish, 1989; Ellison and Gotelli, 2009).
Future studies are needed to understand the environmental determinants (e.g., light, prey, and abiotic nutrient availability, etc.) and the costs and benefits of the production of different sized pitchers in different cohorts (Butler and Ellison, 2007). In order to address this, it would be necessary to determine differences between cohorts in (1) the cost of production (in carbon and nutrients) of pitchers, including the cost of producing attractants; (2) the total mass, caloric content, and nutrient content of prey captured during the life of pitchers; and (3) the balance of photosynthesis and respiration over the life of pitchers. It is essential that the appropriate measure of cost be used in these studies. Because carnivorous plants occupy habitats characterized by high light availability but nutrient-poor soils, it is probable that nitrogen and/or phosphorus, not carbon, limits their growth and reproduction. Therefore, we hypothesize that the carbon allocated to the production of attractants such as nectar, volatile olfactory attractants such as mono- and sesquiterpenes, and coloration by flavonoids may not be growth-limiting expenditures. In fact, the production of these attractants may be virtually cost-free with regard to the impact on growth and reproduction. Instead, it is probably the nutrient cost of producing pitchers (including attractants), rhizomes, and roots, balanced by the benefits in carbon and nutrient gain from these organs, that determines the cost-effectiveness of different strategies of allocation (see Adamec, 2010). Furthermore, the carbon and nutrient balance of tissue production and resource capture may vary among cohorts.
Acknowledgments.--The U.S. Department of Agriculture Forest Service, Kisatchie Ranger District, generously allowed access to the sites. Generous financial support was provided by the Texas Christian University Research and Creative Activities Fund. Helpful comments from A. Ellison, S. Franklin, and two anonymous reviewers substantially improved the quality of the manuscript.
SUBMITTED 3 MARCH 2011
ACCEPTED 26 AUGUST 2011
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JOHN D. HORNER, (1) JULIE CROSS STEELE, CHRISTOPHER A. UNDERWOOD AND DANIEL
Department of Biology, Box 298930, Texas Christian University, Fort Worth 76129
(1) Corresponding author: e-mail: J.Horner@TCU.edu; Telephone: (817) 257-6181; FAX: (817) 257-6177
TABLE 1.--Summary of sampling regime. X--pitcher characteristics measured-sampled; C-prey capture determined Date Cohort 15 Apr. 12-May 4 Jun. 24 Jun. A X XC XC XC X XC TABLE 2.--Summary of ANOVA of the effects of sample date, cohort, and their interaction on pitcher characteristics Source of Trait variation df MS F P Funnel Date 3 0.08 0.21 0.891 diameter Cohort 1 8.18 20.17 <0.001 Date X Cohort 1 0.14 0.34 0.561 Error 207 0.41 Number of Date 3 808.38 45.73 <0.001 secondary Cohort 1 880.45 49.81 <0.001 nectar guides Date X Cohort 1 87.50 4.95 0.027 Error 199 17.68 Nectar Date 3 3022.60 34.26 <0.001 Cohort 1 90.28 1.02 0.313 Date X Cohort 1 746.81 8.46 0.004 Error 185 88.23 TABLE 3.--Correlation coefficients among measurements of plant size. Values are Pearson's partial correlation coefficient (top row) and P (two-tailed). n = 213 Diameter Hood width Hood height Height 0.752 0.617 0.708 <0.001 <0.001 <0.001 Diameter 0.824 0.875 <0.001 <0.001 Hood width 0.864 <0.001 TABLE 4.--Summary of ANOVAs of the effects of date and cohort on prey capture Source of Trait variation df MS F P Total insect Date 2 0.36 3.44 0.034 mass Cohort 1 0.034 0.36 0.550 Error 258 0.11 Detritus mass Date 2 5.48 2.80 0.062 Cohort 1 9.80 5.01 0.026 Error 258 1.96 Total capture Date 2 3.16 1.38 0.252 mass Cohort 1 11.05 4.84 0.029 Error 258 2.28
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