Resource parasitism by spiders in response to morphological correlates of prey capture rates in pitchers of the carnivorous pitcher plant, Sarracenia purpurea (Sarraceniaceae)
Marc Sudman
Department of Biology
Abstract--A field-based investigation was conducted to infer whether or not spiders (Frontinella pyramitela) were cueing in on pitcher morphology when choosing foraging sites (web sites) in the pitchers of Sarracenia purpurea. This is a unique example of resource parasitism as these spiders are sheetweb weavers which predominantly weave webs in small shrubs, bushes, etc. I marked a cohort of 134 pitcher plants (colonies) which contained 234 actively trapping, 2nd year pitchers (649 total pitchers). These pitchers were monitored over a one month period for the presence of webs occluding the aperture of pitchers. After 3 weeks of sampling, only 7 pitchers were observed to be occluded by a web. This investigation took place early in S. purpurea growing season; due to the lack of activity in both spiders and pitcher plants, sufficient data were not collected to support or refute my proposed hypothesis. The results of this investigation are inconclusive. Introduction Pitcher plants, Sarracenia purpurea, provide a unique biological system for investigating plant and animal associations. Many studies have investigated various aspects of these associations (Addicot, 1974; Bradshaw and Creelman, 1984; Cochran-Stafira and Von Ende., 1993, 1998; Dudley, 1984; Fish and Hall, 1978; Hardwick and Giberson, 1996; Harvey and Miller, 1996; Hegner, 1926; Jones, 1936; Paterson, 1971; Prankeviscu, 1985; Wray and Brimley, 1943). Aaron Ellison is currently investigating community assembly in a study, "Community assembly in dynamic habitats: Sarracenia purpurea as a model system (in progress)." Ellison’s study focuses on the ecology of S. purpurea and the association between the organisms that live in the pitcher (inquilines) and the entire plant. His investigation will build model systems that deal with how communities get put together and the interspecific interactions that can regulate that process. The carnivorous nature of S. purpurea provides myriad investigations into the evolutionary history of plant and animal associations, while the ease of controlling and manipulating S. purpurea makes this plant an excellent system for biological inquiry. In my time spent with these plants, though, I have found that many interesting investigations can be conducted with these plants in their "natural" habitat, free from manipulation. Because of S. purpurea’s tolerance to low nutrient availability, low pH, and other wetland conditions, studying S. purpurea in its habitat allows you to step into the magnificent and dynamic environment of bogs, fens, peatlands, etc.. Resource parasitism has been observed in spiders, Liniphiidae, (spelling as cited from article) by occluding the aperture of the pitchers of pitcher plants, Sarracenia purpurea (Cresswell, 1991). These spiders spin their webs inside the aperture of the pitcher and capture prey that would have otherwise fallen into the pitcher. This has a substantial effect on the capture amount of an individual pitcher and thus on the resources available to the plant by ways of carnivory. Cresswell reported that out of 233 individual samples observed to be inhabited by a spider (214 individual pitchers sampled 9 times; 233 of these samples recorded the presence of a spider web), only 10 (<0.5%) of the pitchers recorded prey in the pitcher fluid (Cresswell, 1991). In another study, Cresswell found spiders in 30% of 435 samples (87 pitchers sampled 5 times) (Cresswell, 1992). In the latter study, the distribution of webs among pitchers was found to be highly uneven; 30% of the pitchers were never inhabited by spiders and 8% of the pitchers were inhabited on four or more occasions. These spiders are mobile and move their foraging sites often (Cresswell, 1991; Kareiva et al., 1989). In one study by Cresswell, a mean residency time of ca. 7 days was found (Cresswell, 1991). Janetos makes a distinction between active foragers and sit-and-wait predators, assigning sheetweb weavers to the latter group. The decision to stay at a site or leave is a strategically important decision (Janetos, 1982). Spiders expend a lot of energy producing webs. Spider silk is a protein and thus production is costly in energy and materials. Sheetweb weavers (Linyphiids) do not recycle silk and a rather high metabolic activity cost for sheetweb weavers has been calculated, 10.9 cal/mg (Janetos, 1982). All of these data suggest the importance of choosing more opportunistic web sites.
It has been suggested that the spiders do not respond to large-scale spatial variations in capture rates among pitcher population in their choice of residency (Cresswell, 1991). If spiders are actively choosing web sites based on morphological correlates of prey capture in individual pitchers (see Cresswell, 1992; Heard, 1997; Newell and Nastase, 1998; Wolfe, 1980 for these morphological correlates), then frequency of spider inhabitation should correlate with these characteristics; Cresswell found this to not be the case. He reports that frequency of inhabitation was related to pitcher height above the substrate and size of the pitcher (in this study though, he discusses only height, venation coloration, and size as the traits involved in spider choice) (Cresswell, 1992). He suggests that spiders frequented the larger, lower pitchers because they encountered them more often . A spider that can cue in on morphological characteristics related to prey capture rates would be more efficient in its predation than those spiders who must survey a site before spinning their web. This type of response to resource availability cues has been discussed in several papers concerning various taxonomic groups. Heard has suggested that leaf size might provide ovipositing inquilines with a cue indicating expected prey capture, and therefore resource availability (Heard, 1994). In another study, Schuett suggests that Drapetisca socialis prefers regions of trunks covered with a thick layer of epiphytic algae. "Prey availability is assumed to be higher at these places. The results indicate that D. socialis uses the algal cover as a proximate cue for distinguishing prey-rich from prey-poor sites and is thus able to assess the site quality of a patch in advance, instead of sampling different habitats with the associated risk of wasting time, material and energy (Schuett, 1987)." I suggest that the mobile behavior of Linyphiids, which consequently presents "choices" in foraging sites (web sites) to the spider, would be beneficial to a spider if the spider could exploit those "better" presented choices; these being sites with more available resources. This study investigates the inhabitation of pitchers by spiders on an individual pitcher scale. Field data will be collected that can be used in conjunction with the morphological correlates of prey capture to support or refute the hypothesis that spiders are actively choosing individual pitchers with a higher prey capture rate, based on individual pitcher morphology. Description of study site and organisms The design of this study is purely field based. The study site is a small, sphagnous peatland (ca. 2 acres) containing a population of ca. 150 pitcher plants, Sarracenia purpurea. The flora is dominated by Ericads, sedges, a sparse population of Pinus strobus, and an entire mat of Sphagnum spp. S. purpurea are carnivorous, flowering perennials of the family Sarraceniaceae. Their passive trapping strategy consists of pitcher-shaped leaves that collect rain water. The pitchers can be divided into several zones conducive to attracting, trapping, digesting, and absorbing insects and other small animals. The pitcher is surmounted by a zone shaped like a flap, with nectaries lining the crimson-colored venation present on the interior of the flap (Joel, 1986). Both the nectar and venation patterns are attractants to potential prey (Lloyd, 1942; Cresswell, 1992). Small, downwardly-pointing hairs covering this zone presumably make it difficult for insects to move about, thus losing their footing which causes them to fall into the pitcher. Below this flap lies the aperture to the pitcher lumen. Prey that fall into this area are drowned in the water contained within the pitcher and digested primarily by inquilines. The spiders involved in this investigation, Frontinella pyramitela (Linyphiidae), are ubiquitous in the study site and have been observed to construct their webs in the Ericacious shrubs and other flora surrounding S. purpurea (personal observation). Study design
A cohort of 134 S. purpurea were to be monitored over a one month period for the presence of webs occluding the aperture of the pitchers (a demographic study of the population at this study site revealed an average of 1.7 actively trapping pitchers/plant during this investigation and a total of 4.8 pitchers/plant, see Sudman, 1999). At each sampling date, morphological characteristics of those pitchers with webs were to be described. These data were to include aperture diameter, indices of venation coloration and saturation, size of pitcher, and height of pitcher above substrate. These same data were to be collected from pitchers inhabiting a statistically determined patch surrounding the inhabited pitcher. General spider behaviour of those spiders parasitizing S. purpurea pitchers was to be monitored as well.
Independent research project
Jun/99
Results
The investigation was to begin on 17 May/99 and continue through 15 Jun/99. Within a couple weeks of this investigation, I observed only a few (ca. 5) webs occluding the aperture of pitchers. After a complete demographic investigation (see Sudman, 1999), a total of 234 actively trapping pitchers and 649 total pitchers had been observed and out of those only 7 showed signs of webs. These webs did not seem to be inhabited by spiders at the time of sampling and thus were not included in any data set. These actively trapping pitchers were all 2nd year growth. New growth were present at varying stages of development, although all were closed during the sampling period. No empirical data were collected on spider inhabitation/ethology due to lack of spider activity and thus this investigation was not conducted as planned.
Discussion
Based on the results of this investigation (or lack thereof), I can not support nor refute the proposed hypothesis; the results here are inconclusive. Further field studies and/or controlled laboratory experiments might yield conclusive/suggestive data. For personal, logistic reasons, this investigation took place early in S. purpurea growing season. New pitchers had not yet opened and second season pitchers were just beginning to capture prey (Sudman, 1999). Phenological observations reveal that investigations into this association should be conducted later in S. purpurea growing season. Many studies have reported a strong correlation between pitcher age and capture rate (Wolfe, 1981; Heard, 1997; Newell and Nastase, 1998). In all these studies, with slight variations on age and capture amount, younger pitchers are observed catching more prey than old pitchers with greatest capture rates occurring in pitchers ca. 25 days old. Heard also found that the prey of 2nd year pitchers differed taxonomically from that of first year pitchers with most of the difference due to a decrease in Diptera prey in 2nd year pitchers (Heard, 1997). Diptera seem to be the primary prey of F. pyramitela at this study site (personal observation). I suggest that low early season activity in both Sarracenia and Frontinella yielded no appreciable data. Further investigations into this association could provide interesting insight into spider ethology and the effects of this behavior on S. purpurea biology and the inquiline community.
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copyright 1999 Marc Sudman