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A Test of Group Foraging by the Carnivorous Plant, Sarracenia flava: Are Pitcher Plants Like Wolves?

INTRODUCTION

Predators often forage in groups and understanding the purpose of such group foraging has been a goal of many past ecological and behavioral studies (Beauchamp, 2013). Group foraging may allow larger (Brown and Alexander, 1994; Creel and Creel, 1995) or more dangerous prey to be captured or may make it easier to locate distributed prey (e.g., Sutton et al, 2015). It may also allow predators to create aggregations of prey, allowing more efficient prey capture by groups than by individuals (Benoit-Bird and Au, 2009). In other situations group foraging can actually have negative effects on per-predator feeding success but instead contribute in other ways to predators, such as increasing social interactions (Packer et al., 1990).

Carnivorous plants consume insect prey to supplement soil sources for nutrients such as nitrogen or phosphorus (Juniper et al., 1989). Although carnivorous plants are photosynthetic and use light for energy, they still must find or attract prey, capture the prey, and then digest the prey to obtain limiting resources. Like most other predation, carnivory involves one organism capturing and eating another. The expectation that this should lead to traits or behaviors that increase foraging efficiency (e.g., Clark and Mangel, 1986) should be no different for carnivorous plants than for wolves or lions. In fact optimal foraging by plants for nutrients has been documented previously in the arrangement of ramets and stolons of clonal plants in patchy environments (e.g., Sutherland and Stillman, 1988; Evans and Cain, 1995), as well as in the allocation of resources to plant parts (e.g., McNickle and Cahill, 2009).

Comparing carnivorous plants to packs of foraging wolves may seem a bit fanciful. A more conventional context might be to relate the predator-prey relationship between carnivorous plants and their insect prey to the mutualism that occurs between plants and their animal pollinators. For example it has been shown that inflorescence size can affect rates of pollinator visitation on plants (Rathke, 1981), as well as pollinator behavior on individual flowers (e.g., Schmid-Hempel and Speiser, 1988). However, predator-prey systems have very different dynamics than mutualisms, as the plant kills and consumes animals. Further, carnivorous plants often occur in groups of different size or density, which creates the potential for what is effectively group foraging. Plants do have some control over group size, through seed dispersal, plant growth form, and the arrangement of traps in time and space. Therefore, it is conceivable group foraging could be an adaptive trait (Clark and Mangel, 1986), with selection in carnivorous plants for the arrangement and timing of trap production in a manner than maximizes rates of prey capture and plant fitness.

Here we first quantified the distribution of group sizes for the pitcher plant, Sarracenia flava. Then we experimentally tested the effect of pack or group size on the per-group and per-individual capture rates of this carnivorous pitcher plant. Individual plants of S. flava were placed in the field at different densities for a 2 wk period. After this time prey masses in each leaf were determined to quantify the effects of density on total group and per-leaf prey capture rates. Prey were also identified to insect order; this is the first published study of both the rate and types of prey captured by this carnivorous species. Finally, we compared the optimum group size with the observed group size to ask if plants were arrayed in a manner that might maximize their individual capture rates.

MATERIALS AND METHODS

Sarracenia flava (the yellow or trumpet pitcher plant) is native to the southeastern coastal plain of the U.S.A., occurring from New Jersey to Alabama. This species occurs in a wide variety of habitats but is most commonly found in nutrient poor, sandy, wet soils with no or low tree cover. In north Florida S. flava is common in open wet savannahs and in ecotones between streams and forests and flowers in late March and April. Leaves are generally produced after plants flower in the spring, with most leaves produced either in the late spring or early fall. The tall (to 1 m) tubular leaves are bright yellow, with the uppermost portion flared out to create a funnel and capped with a hood which prevents rain from entering the pitcher. At the inside back of the hood is a bright red patch colored by anthocyanins that may act as a flower-mimic to attract insect prey. The exterior of the leaf contains nectar-secreting cells, particularly focused around the edge of the hood and the back of the open leaf. The nectar has been shown to contain coniine (Mody et al, 1976), an alkaloid drug that may stupefy insects and help with prey capture, and the leaf emits volatiles, which may mimic the smell of fruit or flowers (Jurgens et al., 2009). Leaves arise from a rhizome (approximately 2 cm diameter), with new rhizomes produced each year in the same direction as the old rhizome. The old rhizome then dies back and branching is rare; the net result is a relatively linear progression of a single ramet across a field.

Because 5. flava occurs in sensitive habitats, the precise locations of these studies are only available on request to T. Miller. However, all portions of this study were conducted in the Apalachicola National Forest near Wilma, Florida U.S.A. (30.1544[degrees]N, 84.9644[degrees]W). A population was censused on July 8, 2016 to determine the distribution of group sizes. All plants in a 30 X 30 m area (n = 51) were censused by identifying the number of leaves coming from the same ramet. Each plant was a minimum of 0.5 m from the next plant; plants are often widely dispersed in open fields in this manner. Only green leaves that appeared to be available for prey capture were counted.

Seeds were collected from several natural populations of S. flava in the Apalachicola National Forest in 2001, then germinated and grown in a greenhouse. These plants were maintained in the greenhouse at Florida State University, with occasional repotting of clonal material. All plants were grown in 15 X 15 X 17 cm pots, using a 2:1 mixture of sphagnum peat and local sand. Eighty healthy plants in pots were used in this experiment, each with two to four functional leaves. For each of the 80 plants, one healthy young leaf was identified that was similar in size (mean height = 42 cm) and color to the others and marked to later quantify prey capture. The other leaves on the plants were not monitored. Because plants grown in the greenhouse may have already captured some prey, a small wad of cotton was pushed as far down each leaf as possible in order to separate earlier prey from those captured during the experiment (Cresswell, 1991).

The 80 plants were randomly assigned to one of five blocks and, within each block, the plants were further divided into "groups" of one, two, four, or eight plants (approximately 2, 4, 8, and 16 leaves per group), with the single plant treatment repeated twice per block, but other group sizes only with one representative per block. We have observed natural group sizes that vary from 1 to >30 leaves; however, it is difficult to determine if the groups consist of single or multiple clones (T. Miller, pers. obs.). The group sizes used in this experiment are similar to those found in natural S. flava populations. On July 10, 2013 the plants were transported to an area of the Apalachicola National Forest near Wilma, Florida U.S.A., where a large natural stand of S. flava occurs. Each of the five blocks was randomly assigned space in an open area near this natural population, such that each block was a minimum of 5 m from any naturally occurring plants and 6 m from the nearest block. Plants within blocks were arranged in the appropriate density groups, with each group at least 3 m from the next. Treatments were randomized within blocks and the plants were left in the field for 7 d before being retrieved. All the days of the experiment were sunny with no rain; the weather was typical for this habitat and season, with average daily highs of 32 C and nightly lows of 23 C.

The plants were retrieved from the field on July 17, 2013 and brought to the lab. The marked leaves were cut off each plant, then carefully sliced open to remove the prey. The prey from each leaf was placed in a separate covered petri dish and then placed in a freezer to euthanize any prey still alive. Each prey item was identified to the order or family level (as done by Cresswell, 1991; Heard, 1998), then the entire sample for each leaf was dried in an oven at 60 C for 4 d and later weighed. A subsample of insects from each group was also weighed and then used to estimate the mass of each order or family.

Dependent variables were determined for one leaf on each plant; because the group size of one plant was represented twice in each block, these plants were first averaged so that all treatments were effectively represented once in each block. Then the sum of the prey mass and the per-leaf average prey mass were determined for each group within each block, yielding n = 5 for each group size. To ask if increasing group size affected either the estimated prey mass per group or the average prey mass per leaf, nonparametric Spearman's rank correlations were determined. Spearman's correlations were also used to test for significant effects of group density on per-leaf abundances within prey types. Only the five prey types with greater than 20 individuals were investigated (Formicidae, Hemiptera, Diptera, Coleoptera, and Apoidea) and Benjamini-Hochberg corrections were used to account for multiple comparisons. All analyses were conducted using the R statistical package (R Core Team, 2016).

RESULTS

In the plant size census, almost all the individuals consisted of one to five leaves, with over half the plants having two leaves (Fig. 1). In all cases the leaves appeared to emerge from the same rhizome.

In the leaves from the group size experiment, the prey were partially decomposed and we were not able to separate prey types by mass, but identification was usually possible. The 80 leaves contained a total of 415 identifiable prey; however, the capture rates by different leaves were highly skewed, with several leaves capturing no prey over the 7 d period and one leaf capturing 51 prey (Fig. 2a). By numbers of individuals, ants made up the largest taxonomic group, but bees and wasps made up over half the prey by mass, followed by beetles and true bugs (Fig. 2b).

There were also 45 flesh flies, Fletcherimyia spp, in the harvested leaves; flesh flies are not prey but instead use the pitcher plant leaves as an aquatic habitat for their larvae (Miller and Kneitel, 2005). These sarcophagids were not identified to species but are likely F. rileyi or F. jonesi, both of which have been identified from S. flava in nearby bogs (Underwood, 2009). Fletcherimyia larvae are thought to be cannibals, such that each leaf will eventually host a single individual (Rango, 1999). While most leaves had none or one individual, one leaf had six individuals.

Capture rates were determined both at the group and individual-leaf levels. The mass of prey captured per group significantly increased with the number of plants per group (Spearman's rho = 0.737, P < 0.001). There was no significant effect of group size on per-leaf capture of prey over the 7 d experiment (Spearman's rho = 0.171, P = 0.47). There were also no significant effects of group size on the number of individuals from specific prey types captured per-leaf (Formicidae, rho = -0.525, P = 0.088; Hemiptera, rho = -0.525, P = 0.961; Diptera, rho = -0.525, P = 0.961; Coleoptera, rho = -0.525, P = 0.961; Apoidea, rho = -0.525, P = 0.469).

DISCUSSION

The size of the foraging group has been shown to potentially increase (e.g., Major, 1978; Yip et al., 2008) or decrease (e.g., Buckel and Stoner, 2004) the rate or amount of per-individual prey capture in foraging animals. In this study we asked if carnivorous plants occur in particular group sizes and if this "pack size" affects prey capture rates per leaf. The growth form of the S. flava appears to generally produce small group sizes, with most plants hating only two active leaves. Therefore, we would predict per-leaf capture rates would be highest at our smallest group sizes.

Increasing group size of the yellow pitcher plant, S. flava, does lead to higher rates of prey capture per group (Fig. 3a), likely because larger groups can attract more prey. However, this increase in capture rates is in proportion to the number of plants and leaves present, such that the per-leaf capture rates were not affected by group size (Fig. 3b). Because different insects will be attracted by different plant traits, the effects of group size on the abundance within different prey groups were also analyzed. There were no significant effects of group size on numbers of prey captured per-leaf within specific insect groups.

Many prior studies of group foraging have found an advantage for larger or intermediate size groups in maximizing per-individual capture rates (previews in Giraldeau and Caraco, 2000; Beauchamp, 2013). Larger groups can be important for attracting more prey or capturing larger prey through social interactions among predators, although this may come at the expense of increased competition for captured prey. Whereas the potential for attracting more prey exists for pitcher plants, no such advantages were found. This lack of an effect of group size on per-individual capture rates has also been found on occasion in foraging animals (e.g., Jedrzejewski et al., 2002). Although no previous study has investigated the effects of group size per se on prey capture in carnivorous plants, one experiment did manipulate plant density in Sarracenia purpurea, finding no difference between per-leaf capture rates in half-ambient vs. ambient densities of plants (Cresswell, 1991).

It may be any advantage or disadvantage to prey size is context dependent. For example per capita capture rates of prey decline with pack size in wolves; however, larger packs have a much lower loss of killed prey to scavenging crows (Vucetich et al., 2004; see also Hyodo et al., 2014, Sutton et al, 2015). Overall, individual wolves in packs have higher prey intake when crows are present. Our results are limited to a single week in July and perhaps a similar context-dependent advantage or disadvantage to plant density might occur in other seasons or locations.

This is also the first study to document the types and amounts of prey captured by S. flava. The brightly colored leaves captured an average of 1.07 mg prey/day, which is mostly Apoidea but includes a diversity of other taxa (Fig. 2b). Leaves are typically around 40-50 cm in height, with nectaries all along the outer leaf, particularly concentrated along the edge and lower side of the hood (Miller, pers. obs.). These nectaries may be why ants are the dominant prey by number, as ants are probably not attracted by the color or scent of the leaves. Bees, true bugs, and spiders are fewer in number but make up more of the total prey mass; these prey may be attracted to the leaves as flower mimics, while the flies may be attracted by the scent of other dead prey in the leaf or by the nectar. Sarracenia flava appears to have a more diverse diet than other pitcher plant species, such as Sarracenia alata (Green and Horner, 2007) and Sarracenia minor (Moon et al., 2010) that both specialize on ants. Sarracenia purpurea is probably the best studied species with the widest distribution and is also thought to specialize on ants (Miller and Kneitel, 2005; Miller and terHorst, 2012) and dipterans (Cresswell, 1991).

It is well known that scientists are reluctant to publish nonsignificant results (e.g, Scargle, 2000). In this case the lack of a strong correlation between average leaf capture rate and group size suggests other factors may be more important than capture rate for determining plant fitness. For example plant arrangement may still be important for foraging for light or pollinators, or avoiding herbivores, or even for below-ground interactions such as nutrient and water uptake. If these factors play a role, then the nonsignificant results in this paper are valuable for suggesting new directions for work on optimal plant growth form.

Acknowledgments.--This work was conducted as part of a Directed Independent Study by CS at Florida State University. The authors wish to thank Rachel Pool for help in the field and Will Ryan, Maggie Vogel, and Jen Kennedy for comments on the manuscript.

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Submitted 6 March 2017

Accepted 20 September 2017

CHRISTIAN SAVAGE and THOMAS E. MILLER

Department of Biological Science, Florida State University, 319 Stadium Drive, Tallahassee, 32306

Caption: Fig. 1.--The distribution of leaf number per plant (n = 51) in a natural population of Sarracenia flava in the Apalachicola National Forest

Caption: Fig. 2.--Patterns of prey capture in 80 leaves of the yellow pitcher plant, Sarracenia flava, in July 2013. Leaves were placed in an open area near a natural population of S. flava in the Apalachicola National Forest near Wilma, Florida for seven days, (a) The distribution of prey number captured per leaf, (b) The taxonomic distribution of the types of prey captured by estimated proportion of total mass, down to order or family

Caption: Fig. 3.--The effects of number of plants per group (group size) on the amount of prey captured (a) per group and (b) per leaf from an experiment using 80 plants placed in a field in the Apalachicola National Forest, near Wilma, Florida
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Author:Savage, Christian; Miller, Thomas E.
Publication:The American Midland Naturalist
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Date:Jan 1, 2018
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