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A SIMPLE METHOD FOR TRACKING VERTEBRATE-DISPERSED SEEDS.

DOUGLAS J. LEVEY [1]

SARAH SARGENT [2]

Abstract. Tracking vertebrate-dispersed seeds from parent plant to deposition site remains a primary obstacle to understanding the ecological and evolutionary consequences of seed dispersal. We evaluate a new and simple technique for tracking seeds. Fluorescent microspheres (15 [micro]m diameter) are applied to fruits and later recovered in fecal material associated with the fruits' seeds. Trials with captive Cedar Waxwings (Bombycilla cedrorum) demonstrated that (1) percentage recovery of microspheres is high, (2) all defecations containing seeds also contain microspheres, (3) relatively few microspheres are recovered in defecations not containing seeds, and (4) presence of microspheres on fruits does not affect fruit choice. Field trials with five species of fruits demonstrated that, after [tilde]30 d under full sun and high temperatures, photodegradation limits one's ability to detect microspheres. The field trials also showed that an anti-transpirant applied with the microspheres allows them to adhere to fruits without deterring fruit consumption or damaging fruits and that microspheres can be found in fecal samples of wild birds. Our technique is likely to be applicable to any study in which it is necessary to link fecal material with a particular source of food or an individual animal.

Key words: Cedar Waxwings; fluorescence for tracking seeds; frugivory; microspheres; Savannah River Site (Aiken, South Carolina, USA); seed dispersal; seed shadows, estimation; seed tracking, techniques.

INTRODUCTION

Plant population ecologists have long struggled to document fitness consequences of seed dispersal by animals (Van der Pijil 1972, Harper 1977, Howe and Smallwood 1982, Fenner 1985). Given the number of animal-dispersed species and their occurrence across diverse taxa (Gentry 1982, Stiles 1985), it is assumed the consequences can be positive and pervasive. Yet, despite much interest, we have little idea of exactly what the consequences actually are. What, for example, would happen if a plant's primary dispersers went extinct (Cox et al. 1991, Redford 1992, Chapman and Chapman 1995)?

One of the biggest obstacles to studying seed dispersal by animals is the difficulty of tracking seeds and estimating seed shadows. The challenge is especially great for seeds dispersed by birds and bats. Five techniques are in widespread use, but all have major limitations. (1) Direct observations (e.g., Wenny and Levey 1998) are labor intensive and often inefficient. If they are based at a fruiting tree, it is practically impossible to document what happens when a disperser flies out of sight. If they are based on focal observations away from a fruiting tree, it is practically impossible to know a seed's origin. (2) Likewise, seed traps (e.g., Herrera et al. 1994) allow one to document where seeds go but not their origin. Yet, both origin and destination must be known to determine a plant's seed shadow. (3) Magnets or small pieces of metal may be attached to seeds or fruits on or near the parent plant and later found with a metal detector or magnetic locator (Alverson and Diaz 1989, Sork 1984, Mack 1995). This technique requires a large seed (larger than 1 cm). Also, the magnets or metal pieces are difficult to apply to the skin of fruits and are large enough to be easily detected by the disperser, potentially influencing its behavior. (4) Models that incorporate disperser movement patterns and gut retention times can provide estimates of how far and into what habitats seeds are dispersed (e.g., Murray 1988). But they rely on numerous assumptions (e.g., consistency of movement patterns) and an intimate knowledge of the frequency and distance of each movement, as well as the frequency distribution of seed retention times. (5) Genetic techniques (e.g., Dow and Ashley 1996) allow one to link a seed with its parent plant, thereby providing exact dispersal distance and microhabitat information. However, these laboratory-based techniques are expensive, require considerable expertise (e.g., familiarity with genetic fingerprinting), and involve preliminary studies (e.g., to identify genetic markers). They are a lso hampered by the necessity of destructive sampling (at least for small seeds) and by the difficulty of finding widely dispersed seeds in the first place.

Here we evaluate a new method for tracking seeds. By spraying fluorescent microspheres on fruits and then recovering them in fecal samples, we can identify a seed's point of origin and point of deposition. The technique is simple and relatively inexpensive. It is similar to a widely used technique among pollination biologists, in which fluorescent powder is used to track pollen movement.

METHODS

Fluorescent microspheres (15 [micro]m diameter) were purchased from Bangs Laboratories (Fishers, Indiana, USA), which uses a dying process that minimizes photodegradation. Ten grams of microspheres were mixed with 100 mL saline solution and aliquots of this stock solution were then added in a 1:8 ratio to Wilt-Pruf (Wilt-Pruf Products, Essex, Connecticut, USA), an anti-transpirant that forms an inert, clear, and flexible film upon drying. We applied the microspheres to fruits with a portable airbrush (Paasche Airbrush Company, Harwood Heights, Illinois, USA). The process required 5-10 sec per infructescence. Because of foliage and the three-dimensional arrangement of fruits on an infructescence, it was impossible to spray all fruits evenly. Thus, the number of microspheres applied per fruit varied widely; most fruits received hundreds of microspheres.

We describe three sets of trials with captive birds and two field trials. Captive trials focused on Cedar Waxwings (Bombycilla cedrorum), one of the most common seed dispersers at our study site and one of the most frugivorous species in North America (Martin et al. 1951, Witmer 1996). Seven waxwings were captured at a blueberry farm in southern Georgia (USA) in late April 1998 and maintained on a diet of mashed bananas and soy protein (Denslow et al. 1987). They were housed separately in 0.5 X 0.5 X 0.5 m cages and kept at 23[degree]C on a light cycle that mimicked the natural cycle. Each cage was behind a one-way mirror, which allowed for observation of the birds with minimal disturbance.

Recovery trial

The purpose of this trial was to determine whether microspheres survive gut passage and can be easily detected in fecal samples. Each of the seven waxwings was fed four fruits of llex rotunda, a species they commonly consume in Florida (D. Levey, personal observation). Fecal samples were collected for 2 h, well beyond the mean retention time of waxwings feeding on fruit (Holthuijzen and Adkisson 1984, Levey and Grajal 1991, Levey and Martfnez del Rio 1999, Witmer 1998). Each sample was weighed and thoroughly mixed with 3 mL 70% ethanol and a 75-[micro]L sample was immediately removed. This sample was placed on a glass slide and allowed to dry at room temperature. Slides were examined with an epifluorescent microscope equipped with an FITC (fluoroisothiocyanate) filter block. We scanned samples in a systematic pattern, using a Nikon PlanApo 4X objective and occasionally a lox objective to confirm the presence of a microsphere. We estimated the total number of recovered microspheres by multiplying the number o f microspheres found by the number of 75-[micro]L aliquots in the original sample. We calculated percentage recovery by dividing this number by 4 times the average number of microspheres found on 10 fruits randomly selected from those sprayed.

Retention time trial

Because different components of a meal can pass through a fruit-eating bird at different rates (Levey and Grajal 1991, Afik and Karasov 1995), we thought it prudent to determine how closely the gut retention time of microspheres matches that of seeds. A large discrepancy would compromise the technique.

Four I. rotunda fruits were force-fed each bird at time zero. We force-fed because consumption rate affects retention time (Levey and Martfnez del Rio 1999) and our birds differed widely in how many fruits they consumed per feeding bout. Also, they differed greatly in the frequency and duration of their feeding bouts. Force-feeding allowed us to tightly control start time and meal size. Force-feeding does not affect gut retention time in waxwings (Wahaj et al. 1998).

Defecations were collected every 10 mm by removing a sheet of plastic from the bottom of the cage. Samples were treated and examined as described previously.

Preference trial

With respect to human vision, the microspheres we used are invisible and the concentration we applied too dilute to change a fruit's color. We were nonetheless concerned that birds might be able to detect the presence of microspheres and consequently that their consumption of marked fruits would be abnormally high or low. This concern is bolstered by the discoveries that birds have color vision different from that of humans (extending into the near-ultraviolet; Parrish et al. 1984) and that many fruits have strong ultraviolet reflectance (Willson and Whelan 1989).

In a 5-cm-diameter dish, we placed a randomly chosen, sprayed I. rotunda fruit beside a randomly chosen, unsprayed I. rotunda fruit. Fruits were held in place by a small loop of tape stuck to the bottom of the dish and to the bottom of each fruit. The pair of fruits was slipped into each bird's cage and the first fruit taken was recorded. We repeated these presentations 20 times for each bird. Position of the fruits (right vs. left) was randomized each presentation. If a bird picked up a fruit and dropped it, we considered it a choice for that fruit. Dropped fruits accounted for [less than]10% of fruits chosen. For analysis, we considered each presentation an independent event (i.e., n = 20 choices per individual). Birds may learn through experience, however, which means that repeated presentations to the same individual may not be strictly independent. We selected the repeated, multiple-choice design because it mimics what birds encounter in the field as they fly from one infructescence to another, encounte ring fruits on each that appear slightly different. Advantages and disadvantages of this and other experimental protocols to determine food preference are discussed elsewhere (Peterson and Renaud 1989, Roa 1992, Levey and Cipollini 1998).

Weathering trial

Fluorescent microspheres are primarily designed for use in physiological studies. Because the manufacturer was unsure how stable the fluorescent dye would be when exposed to direct sunlight and severe temperatures, we tested for photodegradation. We simultaneously tested the ability of Wilt-Pruf to keep the microspheres from washing or blowing off fruits.

We mixed microsphere stock solution and Wilt-Pruf in a 1:20 ratio, then placed 20 [micro]L of the mixture on 12 glass microscope slides and let them dry at room temperature. In July 1997 six of the slides were placed in a greenhouse (natural light but no precipitation or wind) and six were placed outside (natural light and weather). The coated surface of slides was vertical. One slide from each set was collected after 2, 5, 19, 33, 47, and 345 d and stored in a dark envelope at 4[degree]C until examination. When slides were examined, we estimated the number of microspheres present in one field of view at 10X, and the proportion of these with full, partial, or zero fluorescence.

Field recovery trial

The purpose of this trial was to determine if we could recover microspheres in the field from different species of sprayed fruit. Our study sites were two 128 X 128 m plots of second growth, embedded in loblolly (Pinus taeda) and slash pine (Pinus elliotii) forests at the Savannah River Site, a National Environmental Research Park near Aiken, South Carolina, USA. Within each plot, 16 polyvinyl-chloride pipes (3.3 m tall X 4 cm in diameter) were arranged in a four-by-four grid, with each of the outer 12 pipes 16m from the edge of the plot. Sprayed fruit were usually located in the 32 X 32 m cell delineated by the four pipes in the center of the plot. We used five species of fruits, all common in or around our study sites: Rhus copallina, R. toxicodendron, Myrica cerifera, Cornus florida, and Ilex opaca. For all species, we supplemented naturally occurring fruit with either branches of fruit gathered nearby and fastened to the vegetation or with multiple detached fruits placed in a feeder. Infructescences of R . copallina were sprayed and placed in the plots in January 1998 and remained through the end of our study 5 mo later. Fruits of the other species typically rotted or were removed within 1--2 wk. Consequently, we rarely had marked fruits of more than one of these species in our plots. Over the course of the study, we placed a total of [tilde]500 000 R. copallina fruits, 25 000 M. cerifera fruits, and 1000 fruits of each of the remaining species.

Fecal samples were collected in two types of seed traps. Below 8-mm dowel rods extending horizontally from each of the 16 pipes, we placed 27 x 51 cm plastic trays on the ground. Each was lined with non-woven landscape fabric and covered with 16-mm wire mesh to protect seeds from vertebrate predators. The second type of seed trap consisted of 25-cm-diameter hanging flower pots. We passed the pipe through a hole we made in the bottom of the pot, sealed the bottom with caulk and landscape fabric, and hung it from the top of pipes (n = 16 pots/plot). Traps were checked 1--3 times per week, depending on weather and bird activity. Any fecal sample containing seeds was collected and preserved in 70% ethanol.

For analysis, samples were emptied into 38-mm-diameter petri dishes and immediately scanned in a systematic pattern. For small samples (such as individual seeds with no associated pulp) the material was examined completely. For large samples with mixed contents the material was examined until a minimum of 2 microspheres was encountered, or for up to 10 mm if none was encountered. Seeds and large pieces of material were picked up and turned over with forceps to examine all surfaces. If more than 10 microspheres were present in a sample, two were found relatively quickly. Otherwise, most samples required [greater than]5 mm to process.

RESULTS

Recovery trial

Recovery of microspheres was high, although quite variable (82 [plus or minus] 35% [mean [plus or minus] 1 SD]). The high variation was likely due to error in estimating the number of microspheres on the fruits fed to the birds. (Recall that the number of microspheres per fruit was highly variable and that we estimated the number from a subsample of fruits.) The less-than-complete recovery was likely due to microspheres adhering to our fingers and to the bird's mouth and esophagus during force-feeding.

Retention time trial

Retention times of microspheres and seeds were similar (Fig. 1). In five of seven trials, the peak recovery times (modes) of microspheres and seeds exactly matched. In the two cases that did not match, the modes differed by only one collection period (10 min). Although defecations not containing seeds often contained microspheres, all defecations containing seeds also contained microspheres and most (92 [plus or minus] 9%) microspheres were recovered in defecations that contained seeds. Furthermore, the percentage of seeds recovered in defecations was significantly and positively correlated with the percentage of microspheres ([r.sup.2] = 0.69, P [less than] 0.01; trials combined), again indicating the gut-retention-time curves of seeds and microspheres are similar in shape and position.

Preference trial

We analyzed preference with a G test for heterogeneity (Sokal and Rohlf 1981). The resulting G statistic (G-total) is partitioned into two components, G-pooled and G-heterogeneity. G-pooled tests the null hypothesis that our population of seven waxwings did not distinguish between sprayed and unsprayed fruits--i.e., that the two types of fruits were selected first an equal number of times in preference trials. G-heterogeneity tests the null hypothesis that all individuals showed the same degree of preference.

Overall, waxwings showed no preference for sprayed or unsprayed fruits (G-pooled = 0.01; P [greater than] 0.50; Table 1). There was, however, significant heterogeneity among individuals (G-heterogeneity = 9.72, P [less than] 0.001). When each individual's G value is examined (Table 1), it becomes obvious that one individual's strong preference for unmarked fruit resulted in the significant variation among individuals; all other birds had G values [less than] 1.0 (Ps [greater than] 0.50).

Weathering trial

Microspheres endured outdoor conditions fairly well. In particular, the Wilt-Pruf was very effective at preventing loss of microspheres. Even the slides left outdoors for almost a year had as many microspheres remaining on them as those collected after less than a week. However, photodegradation did occur (Fig. 2). By 19 d, most outdoor and greenhouse microspheres showed partial loss of fluorescence around their edges, but all still had bright spots in their centers. By 33 d, almost all greenhouse microspheres were more noticeably faded; many retained their bright spot. The outdoor microspheres were even more faded. None fluoresced strongly and 3% did not fluoresce at all. After 47 d, [greater than] 90% of greenhouse microspheres still showed partial fluorescence, whereas [greater than] 90% of outdoor microspheres showed no fluorescence.

Field recovery trial

We recovered and analyzed 95 fecal samples. Microspheres were present in 47% of these samples. Fruit species varied widely in the likelihood that microspheres would co-occur with seeds. Most samples containing Rhus toxicodendron, Myrica cerifera, or Cornus florida seeds also contained microspheres, whereas most samples containing R. copallina and Ilex opaca did not (Fig. 3). Much of this variation was likely due to differences in size and surface structure of the fruits. For example, microspheres may have persisted longer on the rough surface of M. cerifera fruits than on some of the species with a smooth surface. Also, R. copallina fruits were in the field for 5 mo, whereas fruits of the other species were typically exposed for [less than]1 mo. Consequently, low recoveries of R. copallina microspheres may have been due to more extensive photo-degradation, compared to other species. Additionally, differences in duration of exposure, as well as differences in the dates of exposure, likely affected the persistence of microspheres on the fruits and in defecations because of numerous periods of unusually heavy rain associated with EI Nino in the winter of 1998. Finally, the low recovery of microspheres in samples containing I. opaca seeds is likely explained by the unusually high abundance of I. opaca fruits in the adjacent forest, These fruits were not sprayed and almost certainly accounted for most of the I. opaca seeds we captured.

DISCUSSION

Our experiments show that fluorescent microspheres can successfully be used for tracking seeds. Microspheres are defecated intact by birds, have equal gut retention times as seeds, can adhere to fruits for long periods, retain their fluorescence under harsh conditions for a minimum of 2-3 wk, are readily consumed by wild birds, and can be recovered from their defecations.

The only caveat revealed by our trials arises because one of our birds showed a distinct preference for fruits not sprayed with microspheres. This suggests that waxwings can visually detect microspheres. It is unlikely that the other six waxwings in our trials had such different optical perception that they failed to detect the microspheres; a more parsimonious explanation is that they could distinguish between fruits with and without microspheres but the presence of microspheres did not affect their feeding behavior. Regardless, birds in the field and in captivity readily ate fruits sprayed with microspheres. The possibility that some birds can detect microspheres does not detract from the usefulness of using microspheres to track seeds they ingest.

Our weathering trials caution against use of fluorescent microspheres in situations where they will be exposed to high temperatures and full sunlight for [greater than]30 d. Our greenhouse samples suggest that protection of microspheres can extend their life. We suspect microspheres would last considerably longer in cool and shaded conditions, such as on understory fruits. A longer life of the microspheres' fluorescence might also be achieved by using larger microspheres. The key point is that microspheres do not permanently retain their fluorescent properties. So many factors likely influence their life-span that we think it prudent to avoid statements about "typical" life-span. Indeed, we recorded fluorescing microspheres in defections containing only R. copallina seeds that were collected [greater than]1 mo after spraying R. copallina, an impossibility according to the findings of our outdoor weathering trial. The microspheres may have persisted longer than expected because they were applied in January an d therefore experienced less harsh physical conditions (lower temperatures and less sunlight) than the microspheres in our weathering trail, which started in the summer.

A further limitation of our technique for tracking seeds may occur when seeds are regurgitated rather than defecated. Our study species, Cedar Waxwing, almost never regurgitates seeds (Levey and Grajal 1991, Witmer 1998); seeds are therefore always associated with pulp in fecal samples. Other species, such as thrushes (Turdinae) and manakins (Pipridae), usually regurgitate the largest seeds they ingest (Levey 1987, Murray et al. 1993, Witmer 1998). Because regurgitated seeds lack fruit skin and because microspheres are applied to skin not seeds, microspheres may not be commonly found with large seeds dispersed by some birds.

The use of microspheres is most appropriate for small-seeded fruits that are removed quickly from the parent plant (because of the relatively short half-life of microspheres in the field). Microspheres will be most easy to find in situations where their dispersal is directed to specific places, such as nests, perches, and display arenas. In situations where seeds are dispersed randomly, it will remain exceedingly difficult to find defecations originating from a given plant's fruits, except in the immediate vicinity of that plant. In these cases, a combination of microspheres and direct watches (to find defecations) may be helpful.

Marking fruits with fluorescent powder is a potential alternative to marking them with fluorescent microspheres. Recent studies suggest ingestion of fluorescent powder by small mammals is not harmful to them, that the powder is passed intact, and that it can be recovered in feces (Stapp et al. 1994, Hovland and Andreassen 1995).

Our technique offers great promise for linking different phases of a plant's life cycle. Very few studies have been able to bridge the gap between seed dispersal by vertebrates and seedling establishment; it represents a significant challenge in the study of seed dispersal and plant population biology (Jordano 1992, Willson and Whelan 1993, Jordano and Herrera 1995, Wenny and Levey 1998). Because microspheres can be detected easily and non-destructively and because their dispersal when attached to fruits mimics that of seeds, they allow one to follow the dispersal and fate of seeds from known sources.

ACKNOWLEDGMENTS

This work was funded by a cooperative agreement between the University of Florida and the USDA Forest Service Southern Research Station and the Department of Energy at the Savannah River Natural Resources Institute. We thank John Blake for his support and encouragement, Cynthia Renk and Kim Coffey for help in the field, Hiedi Bissell for help with captive birds, and Lou Guillette, Andy Rooney, and Joe Erlichman for help with microscopy.

(1.) Department of Zoology, P.O. 118525, University of Florida, Gainesville, Florida 32611

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             Cedar Waxwing fruit preference. G statistics are
         provided for each bird (df = 1) and sum to G-total, which
          is then partitioned into G-pooled and G-heterogeneity.
     Bird       Preference   G
      A             4      7.71 [**]
      B            11      0.20
      C            10      0.00
      D            11      0.20
      E            12      0.81
      F            12      0.81
      G            10      0.00
G-total                    9.72 [**]
G-pooled                   0.0001
G-heterogeneity            9.72 [**]
Note: Data reported for "preference" are the numbers of
trials out of 20 trials in which seven Cedar Waxwings chose
a fruit marked with fluorescent microspheres over an unmarked fruit.
(**.)P[less than]0.001
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Author:LEVEY, DOUGLAS J.; SARGENT, SARAH
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Date:Jan 1, 2000
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