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0 Department of Biological Sciences, University of Nevada, Las Vegas, Nevada 89154-4004 USA
Received for publication April 13, 1999. Accepted for publication August 24, 1999.
ABSTRACT
Field studies investigating the impact of ants on the reproduction of plants bearing extrafloral nectaries have traditionally focused on seed production, a component of female fitness. The purpose of this study was to test whether ants can affect the pollen viability, a component of male fitness, when they visit flowers of the shrub Acacia constricta. Acacia constricta inflorescences hand-pollinated with flowers over which Formica perpilosa ants had crawled set significantly fewer seed pods than inflorescences hand-pollinated by control flowers that had no contact with ants. Many ant species secrete antibiotic substances onto the integument that render pollen inviable, and these secretions are probably the mechanism for reduced pollen viability in this study. The ratio of seed pods produced by self-pollinated inflorescences to those produced by cross-pollinated inflorescences was 0.16, indicating that A. constricta is largely self-incompatible. Because F. perpilosa workers forage primarily on the acacia tree under which they nest, they are unlikely to serve as efficient vectors of outcrossing. Previous work showed that A. constricta shrubs with F. perpilosa ants produce approximately twice as many seeds as similarly sized plants not so associated. The results indicate that association with F. perpilosa could cause a reproductive trade-off for A. constricta: benefits to female function may be accompanied by costs to male function. Selection to discourage ant visitation to flowers may have affected the pollination biology of this and other ant-associated plant species.
Key Words: Acacia constricta • ants • extrafloral nectaries • Fabaceae • male fitness • mating system • pollen viability • seed production, self-incompatibility
The adaptive significance of extrafloral nectaries has been of interest to evolutionary biologists for over a hundred years (Bentley, 1977a
; Buckley, 1982
; Beattie, 1985
; Keeler, 1989
; Huxley and Cutler, 1991
). Currently, the only well-accepted hypothesis for the evolution and maintenance of extrafloral nectaries is that ants kill or dislodge herbivores from plant tissues, thereby reducing the loss of plant tissue to herbivores (Bentley, 1977a
; but see Becerra and Venable, 1989
). Empirical studies testing this hypothesis often measure levels of leaf damage or numbers of herbivores and assume, implicitly or explicitly, that a negative correlation exists between the level of leaf damage and the ability of the plant to reproduce (Janzen, 1966
; Koptur, 1984
; Costa, Oliveira-Filho, and Oliveira, 1992
; Fiala et al., 1994
). Where effects on reproductive success are directly quantified, fruit or seed production (reproduction through female function), rather than the success of pollen at fertilizing ovules (reproduction through male function) has been used exclusively as an estimate of the plant's reproductive success (Bentley, 1977b
; Inouye and Taylor, 1979
; Koptur, 1979
; Schemske, 1980
; Stephenson, 1982
; O'Dowd and Catchpole, 1983
; Horvitz and Schemske, 1984
; Kelly, 1986
; Koptur and Lawton, 1988
; Wagner and Kurina, 1997
).
The bias toward estimating female fitness is, of course, not restricted to ant–plant studies; plant ecologists have traditionally ignored the contribution of male fitness to plant reproductive success. However, a recent and growing body of work has begun to focus attention on how environmental variation impacts male plant fitness (e.g., Young and Stanton, 1990
; Snow, 1994
; Mutikainen and Delph, 1996
; Strauss, Conner, and Rush, 1996
; Delph, Johannsson, and Stephenson, 1997
). Consideration of how ants affect reproduction through male, as well as female, function is central to understanding how ants affect total plant reproductive success and selection on characters such as extrafloral nectaries.
Researchers have recognized for some time that ants can disrupt, as well as enhance, plant reproduction. Ants can reduce the frequency of visitation by insect pollinators by behaving aggressively or by "robbing" flowers of nectar (McDade and Kinsman, 1980
; Willmer and Corbet, 1981
; Herrera, Herrera, and Espadaler, 1984
; Rico-Gray, 1989
; Buys, 1990
; discussed by Willmer and Stone, 1997
). Studies that estimate the outcome of ant visitation to plants bearing extrafloral nectaries by measuring fruit or seed production take these potential losses into account by measuring the standing crop, or the net effect of ants on female reproduction. Ant effects on male fitness will be more complicated to measure. Ants might enhance male fitness indirectly by reducing herbivory or otherwise increasing the plant's access to resources (Oliveira, 1997
; Wagner, 1997
). But visiting ants could have direct, negative impacts on male fitness through physical contact with pollen.
Many ant species secrete broad-spectrum antimicrobial substances onto the integument (Beattie et al., 1986
; Veal, Trimble, and Beattie, 1992
), and a considerable body of laboratory work has demonstrated that contact with ants can damage pollen as well as bacteria and fungi (Beattie et al., 1984, 1985
; Hull and Beattie, 1988
; Peakall, Angus, and Beattie, 1990
). Beattie et al. (1984)
and Peakall, Handel, and Beattie (1991)
noted that contact-related pollen damage may help to explain why ants are rarely effective pollen vectors. The potential for ants to damage pollen also has important implications for the evolution and maintenance of extrafloral nectaries. By drawing ants onto plants, extrafloral nectaries place ants in the vicinity of floral structures, where they may interfere with male, as well as female function.
A reduction in pollen viability, however, does not necessarily imply a reduction in male fitness. When ants do act as pollinators, the benefits of pollen transfer can outweigh negative effects on pollen viability (Gómez and Zamora, 1992
). Although ant pollination appears to be rare (Peakall, Handel, and Beattie, 1991
), it has been documented for a handful of plant species (Peakall, Handel, and Beattie, 1991
; Gómez and Zamora, 1992
; Ramsey, 1995
; Gómez et al., 1996
). In such cases, pollen is often carried on ant's body by hairs, stalk-borne pollinia, or stigmatic secretions, minimizing contact between pollen and the ant's integument (Peakall and Beattie, 1989
; Peakall, Angus, and Beattie, 1990
; Beattie, 1991
; Gómez and Zamora, 1992
; Ramsey, 1995
). Plant species for which ant-pollination is known tend to be self-compatible (Peakall and Beattie, 1991
; Ramsey, 1995
). Although few studies have directly measured levels of selfed vs. out-crossed pollination by ants (Peakall and Beattie, 1991
), most ant pollination probably results in self-pollination (reviewed by Beattie, 1991
; Peakall, Handel, and Beattie, 1991
). In general, ants do not move directly from the flowers of one plant to the flowers of another, particularly when foraging on large plants with numerous nectar sources.
In the southwestern United States, the ant Formica perpilosa associates with Acacia constricta and other shrubs bearing extrafloral nectaries. Colonies of F. perpilosa nest at the base of these shrubs and ants forage primarily on the foliage, collecting extrafloral nectar, arthropod prey, and insect exudates. Association with F. perpilosa benefits A. constricta reproduction through female function: plants with basal ant nests produce about twice as many seeds as similarly sized plants without basal ant nests (Wagner, 1997
). Plants with basal nests have many more ants on the foliage than those without nests; however, ant exclusion experiments have demonstrated that the presence of ants on the foliage does not in itself increase seed set over controls (Wagner and Kurina, 1997
). Instead, increased seed production appears to result from high concentrations of nutrients and high mineralization rates in ant nest soils (Wagner, 1997
).
The purpose of this study was to determine whether physical contact with F. perpilosa ants decreases A. constricta pollen viability under field conditions. Most previous estimates of ant effects on pollen quality have been conducted in the laboratory, using pollen germination assays and fluorochromatic techniques for assessing membrane viability (e.g., Beattie et al., 1984, 1985
; Hull and Beattie, 1988
; Peakall, Angus, and Beattie, 1990
). To my knowledge, only one experimental study prior to this one investigated ant effects on the ability of pollen to fertilize ovules (Ramsey, 1995
). In that study, contact with Iridomyrmex ants significantly reduced Blandfordia grandiflora pollen germination as measured in the laboratory, but the field bioassay revealed no effect of ant contact on seed set. Here, I used a similar field bioassay to test the effect of ant contact on the ability of A. constricta pollen to fertilize ovules. In order to evaluate the likelihood that ants are effective pollinators of A. constricta, I also tested for self-compatibility.
MATERIALS AND METHODS
The study population was located 5 km northeast of Portal, Arizona, in desert scrub habitat dominated by Acacia constricta and Prosopis juliflora. All experiments were conducted during August and September 1997, within an area of ~1 ha.
Acacia constricta is leafless in the winter and spring and produces leaves and flowers in response to summer rains (Bowers and Dimmit, 1994
), which usually begin in July at the study site. Both leaf and flower production cease by September, when a crop of seeds is produced. Leaves are shed in December or January. Leaves possess an average of 2.0 extrafloral nectaries along the rachis (SE = 0.2, N = 31 plants, data are averages of 5 leaves per plant; overall range 0–5 nectaries per leaf). Plants old enough to flower range in height from 0.5 to 3 m. Plants produce large numbers of inflorescences; intermediately sized plants typically have several hundred inflorescences at the peak of flowering (Wagner and Kurina, 1997
). Inflorescences are yellow, spherical, ~10 mm in diameter and composed of ~20–50 florets. Inflorescences are interspersed with leaves along the branches. The most common putative pollinator is the honey bee, Apis mellifera, which is cultivated in the area. Bees only visit inflorescences on the day the buds open. On the second day, inflorescences are noticeably drier and duller in color; on the third day they are withered and brown.
Workers of the ant Formica perpilosa are ~5–9 mm in length with a shiny integument and few hairs. At the study site, colonies nest exclusively at the bases of A. constricta and P. juliflora. In the summer months, colonies often establish auxiliary nests under trees surrounding permanent nests. Workers forage primarily on the foliage of nest trees. Numbers of workers are considerably higher on the foliage of plants with basal ant nests (36 ± 47 SD, N = 15 plants) than on nearby plants of equal size without basal nests (3 ± 4 SD, N = 15; data from Wagner, 1997
). Acacia constricta flowers produce no detectable nectar; F. perpilosa ants visit inflorescences to forage for small insects and to visit ant-tended herbivores (Wagner and Kurina, 1997
; D. Wagner, unpublished observations).
Ants and pollen viability
To test the effect of ant contact on pollen viability, I compared the fruit set following hand-pollination using pollen that had, and had not, contacted ants. I designated three plants, located an average of 36 m apart (SD = 12 m), as pollen donors. These plants were chosen on the basis of their large size (2.5–3 m in height) and abundant (>1000) inflorescences. Inflorescences were collected on the day they opened from pollen donor plants and placed by threes into 30-mL vials equipped with mesh lids. Vials were randomly assigned as ant treatment or no-ant controls. Six F. perpilosa ants, aspirated from the vegetation of a nearby plant, were added to each treatment vial. This ratio of ants to inflorescences (2:1) was chosen because two ants is generally the maximum observed on a single inflorescence (personal observation). All vials (treatments and controls) were placed into an insulated container at ~25°C for 30 min, and during this period ants were allowed to crawl on inflorescences in the treatment vials. Lids were then removed from the ant-containing vials, and the ants were allowed to exit the vial. No loose pollen was noted in either set of vials following the removal of ants. All vials were stored in the insulated container until pollinations for the day were complete.
Pollen recipients (N = 6) were chosen haphazardly from the set of plants bearing at least 100 inflorescences. These plants were, on average, 10 m (SD = 6) from the nearest pollen recipient plant and 22 m (SD = 4) from the nearest pollen donor plant. On each plant, two flowering branches (each ~0.5 m long) were cleared of all open inflorescences and enclosed in bags made from fine-mesh fabric (mesh openings ~0.8 mm). One bag was assigned by coin toss to contain ant-treated pollinations and the other control pollinations, to avoid cross-contamination within bags. The next morning, and for five consecutive days, I hand-pollinated all newly opened inflorescences (14–38 inflorescences per plant in total) with ant-treated or control pollen, as appropriate. To hand-pollinate an inflorescence, I held the pollen donor inflorescence with forceps and brushed it against all sides of the pollen recipient inflorescence for 10 s continuously, ensuring that all recipient stigmas contacted the stamens of the donor. Pollinated inflorescences were then marked with wire ties attached just distal to the petiole. Each branch was quickly rebagged after the pollinations on that branch were completed. Hand-pollinations were carried out between 0530 and 0900, the time of greatest bee activity.
Fruit set was scored in mid-September. I determined the numbers of flowers that produced fruit by (1) counting the number of visible seed pods and (2) dissecting any flowers that remained attached to the petiole on marked inflorescences. Dissected flowers were scored as setting fruit if they possessed a distinctly swollen ovary.
Data were compiled as the difference (control-ant-exposed pollen) in the number seed pods produced per pollinated inflorescence for each pollen donor-pollen recipient combination (N = 18 combinations). I then analyzed the compiled data in two ways. First, I tested whether the effect of ants on pollen varied among pollen donor and pollen recipient individuals using a two-way ANOVA. Second, I tested whether the difference in seed pod production was significantly greater than zero using a t test. The standard error for this test was calculated including the variance components contributed by differences among pollen donors and among pollen recipients, which led to a somewhat larger standard error than the crude standard error and a more conservative t test.
Self-compatibility
Self-compatibility was tested by hand-pollinating inflorescences using pollen from the same and different individuals. I used 12 plants as pollen recipients, ranging in height from 1 to 3 m and located ~6 m (SD = 3 m) on average from the nearest pollen recipient neighbor. I removed all open inflorescences from three branches on each of ten plants and bagged the branches as above. On each plant, one branch was assigned at random to the self-pollination treatment and another to the cross-pollination treatment; the remaining bag served as a source of pollen for selfing. Each morning for 10 d, I hand-pollinated all newly opened inflorescences. To outcross inflorescences I used inflorescences from one of ten pollen donor plants. Pollen donors were located, on average, 24 m apart (SD = 9 m) and were no closer than 15 m to a pollen recipient.
Fruit set was measured as described above. I calculated fruit set as the number of seed pods produced per pollinated inflorescence. Data for self-pollinated and outcrossed inflorescences violated the assumption of equal variances, so the treatments were compared with a nonparametric test for paired variates.
RESULTS
Ants and pollen viability
All pollen donor and pollen recipient plants had similar responses to pollination with ant-exposed pollen: there was no significant effect of pollen donor (F2,10 = 1.4, P = 0.3) or pollen recipient (F2,10 = 1.8, P = 0.2) on the difference (controls - ant-treated) in the number of pods produced per inflorescence. Ant contact reduced pollen viability (Fig. 1). Overall, pollen exposed to ants produced 1.1 pods/inflorescence (SE = 0.3, N = 78), whereas control pollen produced 3.2 pods/inflorescence (SE = 0.7, N = 74). The within-plant difference in numbers of pods per pollinated inflorescence (control pollen - ant-exposed pollen) was significantly greater than zero (mean difference for control - ant-exposed pollen = 2.0, SE = 0.87, N = 18, one-tailed t = 2.4, P = 0.02).
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The results demonstrate that contact with F. perpilosa ants causes a significant reduction in pollen viability for A. constricta. Two possible mechanisms could account for this result. First, contact with secretions produced by the ant's metapleural glands may have rendered pollen inviable (Beattie et al., 1984, 1985, 1986
). The surface secretions of many ant species, including the congener F. obscuripes, cause a decrease in pollen viability as measured in the laboratory (Hull and Beattie, 1988
). Second, although I noted no free pollen in vials following the removal of ants, ants may have dislodged pollen by walking on inflorescences. In either case, the outcome of ant contact is likely to be the same on the host plant as in the vials used in this experiment: a reduction in the amount of pollen available to fertilize ovules.
Under natural conditions, the degree to which ants reduce pollen viability or availability will depend on the frequency and timing of ant visitation to flowers. My observations suggest that although ants do visit acacia inflorescences, visitation is infrequent. Selection imposed by ants through loss of pollen may have affected the floral attractiveness of A. constricta and other ant-associated species to ants in ways that mitigate pollen damage or loss. For example, A. constricta has little or no floral nectar, a possible adaptation to discourage ants from visiting flowers. The African acacia A. zanzibarica, which also lacks floral nectar, actively deters ants from visiting newly opened inflorescences by secreting a substance that ants avoid (Willmer and Stone, 1997
). Whether A. constricta produces such a substance is not known.
It is unlikely that F. perpilosa ants act as effective vectors for A. constricta pollen. Workers possess few hairs and little sculpturing on the integument; they are poorly equipped to carry pollen, especially in ways that minimize contact between pollen and integument. Moreover, the results presented here indicate that A. constricta is largely self-incompatible, and F. perpilosa is unlikely to promote effective outcrossing. In general, when worker ants function as pollinators, they appear to promote selfing rather than outcrossing (Brantjes, 1981
; Peakall and Beattie, 1989
; Peakall, Angus, and Beattie, 1990
; Peakall and Beattie, 1991
; Ramsey, 1995
). Formica perpilosa ants forage primarily on the plant under which the colony nests (unpublished observations) and so probably do not move significant quantities of pollen from one plant to another.
Recent studies have suggested that herbivory can reduce male fitness (Frazee and Marquis, 1994
; Quesada, Bollman, and Stephenson, 1995
; Strauss, Conner, and Rush, 1996
). Ants could therefore play an indirect, positive role in male fitness by reducing herbivore abundance on plants. For example, the shrub Caryocar brasiliense visited by ants had lower levels of infestation by herbivores and larger numbers of flowers than those from which ants were excluded (Oliveira, 1997
). Acacia constricta plants visited by F. perpilosa also produced more inflorescences than plants with ants excluded (Wagner and Kurina, 1997
). The mechanism for ant-associated increase in A. constricta flower number is not known; ants did not reduce herbivore abundance and both ant-excluded and control plants had ant nests at the base early in the study (Wagner and Kurina, 1997
). However, regardless of the mechanism, a larger floral display and greater attractiveness to pollinators might serve to offset losses of pollen viability due to contact with ants. Further study will be necessary to understand the overall impact of ants on male function under natural conditions.
The results of this bioassay contribute to our understanding of how ants affect plants by demonstrating that ant contact can depress the ability of pollen to fertilize ovules under field conditions. For A. constricta, association with ants, maintained through the presence of extrafloral nectaries, involves potential costs as well as benefits; increases in seed production associated with proximity to F. perpilosa nests may be accompanied by decreases in pollen viability when ants contact flowers. The study is, however, only a small step toward understanding how ant association affects, or has in the past affected, male plant fitness in this system. Pollen viability is only a component of fitness, and the extent to which ant behavior currently affects reproduction through male function is unknown. Despite the difficulties of studying male fitness, future studies that focus on both male and female aspects of plant reproduction will lead to a better understanding of how ants shape plant characters in general and will contribute to, and perhaps alter, current views on the evolution and maintenance of extrafloral nectaries.
FOOTNOTES
1 The author thanks Lincoln E. Moses for designing one of the statistical analyses; Carol Boggs, Simon Emms, Nathan Sanders, Paul Schulte, and Christopher Wheat for improving the manuscript; and the staff of the Southwestern Research Station of the American Museum of Natural History for their assistance. 
2 Phone 702-895-4421, FAX 702-895-3956, e-mail: dwagner{at}ccmail.nevada.edu
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= pollen on which ants had walked, 
= control pollen. Error bars are mean standard errors; numbers above bars are the total number of inflorescences pollinated on six plants