Harvester Ants Reduce Seed Survivorship in Slickspot Peppergrass, a Rare Mustard Endemic to Idaho

Boise State University ScholarWorks

Biology Faculty Publications and Presentations Department of Biological Sciences

12-2020

Jennifer A. Brown Boise State University

Ian C. Robertson Boise State University

Harvester ants reduce seed survivorship in slickspot peppergrass, a rare mustard endemic to Idaho

JENNIFER A. BROWN1 AND IAN C. ROBERTSON1,*

1Department of Biological Sciences, Boise State University, 1910 University Dr., Boise, ID 83725

ABSTRACT.—Seed predation can significantly reduce the reproductive success of individual plants and their populations. The consequences of seed predation often are most pronounced for rare plant species, in which loss of seeds can have a disproportionate effect on populations. The present study examined the effects of seed predation by Owyhee harvester ants (Pogonomyrmex salinus) on seed survivorship in slickspot peppergrass (Lepidium papilliferum), a rare mustard endemic to sagebrush-steppe habitat in southwestern Idaho. Within sagebrush-steppe, L. papilliferum is restricted to microsites known as “slick spots”—shallow depressions of soil characterized by distinct clay layers and surface water retention that is higher than that of surrounding areas. Harvester ants frequently nest in L. papilliferum habitat and readily consume the plant’s seeds. We conducted a controlled field experiment at a population of L. papilliferum in 2012 to quantify seed loss to individual plants as a result of seed predation by harvester ants. Across 20 slick spots, plants exposed to harvester ants experienced a median reduction in seed survivorship of 89.2% (interquartile range, 69.3% to 93.9%) relative to plants in the same slick spot that were matched for size and shielded from ants. The proportion of seeds that plants lost to seed predation was more variable and significantly lower in slick spots with >150 plants than in those with fewer plants, suggesting that a threshold to the number of seeds that can be collected and consumed by ants may occur within the natural range of plant densities found in slick spots. Our results suggest that slick spots supporting large numbers of L. papilliferum in a given year may be buffered from the effects of predation, whereas those with relatively few plants are particularly vulnerable to high levels of seed loss to harvester ants.

RESUMEN.—La depredación de semillas puede reducir significativamente el éxito reproductivo de las plantas individuales y sus poblaciones. Las consecuencias de la depredación suelen ser más evidentes en las especies de plantas exóticas, potencialmente teniendo un efecto desproporcionado en las poblaciones. En el presente estudio, investigamos los efectos de la depredación de las hormigas Pogonomyrmex salinus en la supervivencia de las semillas de las hierbas Lepidium papilliferum, una planta de mostaza endémica al hábitat de estepas de artemisas del sudoeste de Idaho. Dentro de las estepas de artemisas, la L. papilliferum se restringe a micrositios conocidos como “zonas resbaladizas”, depre- siones del suelo caracterizadas por distintas capas de arcilla y retención de agua superficial, mayor a la de las áreas circundantes. Las hormigas Pogonomyrmex salinus con frecuencia anidan en el hábitat de las L. papilliferum y rápida- mente consumen las semillas de la planta. En 2012, realizamos un trabajo de campo controlado en una población de L. papilliferum, para cuantificar la pérdida de semillas en plantas individuales como resultado de la depredación por parte de las hormigas Pogonomyrmex salinus. En 20 zonas resbaladizas, las plantas expuestas a las hormigas experimen- taron una reducción promedio de la supervivencia de sus semillas del 89.2% (rango intercuartil, 69.3%–93.9%) relativo a otras plantas de igual tamaño en la misma zona, que fueron protegidas de las hormigas. La proporción de semillas perdidas como consecuencia de la depredación fue más variable y significativamente menor en las zonas resbaladizas con >150 plantas, que en aquellas zonas con menos plantas, sugiriendo que podría haber un umbral en la cantidad de semillas que las hormigas pueden recolectar y consumir, dentro de la distribución natural de las plantas encontradas en estas zonas resbaladizas. Nuestros resultados indican que las zonas resbaladizas con grandes cantidades anuales de L. papilliferum pueden estar protegidas de los efectos de la depredación, mientras que aquellas con relativamente pocas plantas son particularmente vulnerables a altos niveles de pérdida de semillas a causa de la depredación por parte de las hormigas Pogonomyrmex salinus.

Harvester ants in the genus Pogonomyrmex from the environment, which can alter the com - are important seed consumers in the arid and position of plant communities and the dynam- semi arid grasslands of North America (MacMa- ics of populations (Reichman 1979, Inouye hon et al. 2000). Their foraging activities have et al. 1980, MacMahon et al. 2000). The det - the capacity to remove large numbers of seeds rimental effects of seed predation may be

*Corresponding author: [email protected] ICR  orcid.org/0000-0002-6233-8221

483 484 WESTERN NORTH AMERICAN NATURALIST (2020), VOL. 80 NO. 4, PAGES 483–491 particularly consequential for rare plants, in of foragers to food patches decreases individ- which any loss of seeds could limit or prevent ual search times and increases the cumulative population recovery (Ancheta and Heard 2011). number of seeds collected from patches (Mac - Because seed predation can be a major con- Ma hon et al. 2000). Because L. papilliferum is tributing factor to low recruitment of individu- restricted to growing in slick spots, its seeds als in rare plant populations (Crawley 2000, become concentrated in dense patches that Albert et al. 2005), measuring the effect of seed harvester ants can readily exploit. While these predation on seed survivorship under natu ral concentrated patches of seeds may facilitate conditions is an important first step in the assess- seed predation, the proportion of seeds lost by ment of how seed predation may impact vital individual plants should be subject to a dilu- rates of a rare species. Here we measure the tion effect (Wenninger et al. 2016) once seed effects of seed predation by Owyhee harvester availability in a patch exceeds the consump- ants, Pogonomyrmex salinus (Olsen) (Hyme - tion threshold of the predators (Janzen 1971, noptera: Formicidae), on seed survivorship in Kelly 1994). slickspot peppergrass, Lepidium papilliferum In a preliminary analysis of seed loss to (L. Hend.) A. Nelson & J.F. Macbr. (Brassi - harvester ants, White and Robertson (2009) caceae), a rare mustard endemic of sagebrush- reported that ants removed, on average, at steppe habitat in southwestern Idaho. least 40% of mature fruit directly from L. papil - Within sagebrush-steppe, L. papilliferum is liferum plants, and scavenged seeds from the restricted to microsites known as “slick spots” ground beneath the plants. However, the study (Moseley 1994)—shallow depressions of natric did not assess the combined effects of pre- and soils characterized by distinct clay layers and postdispersal seed loss to individual plants, surface water retention that is higher than that nor did it consider the possibility of a dilution of surrounding areas (Fisher et al. 1996). The effect (via predator satiation) in response to unique habitat requirements of L. papilliferum, total seed availability within slick spots. Subse - along with the plant’s limited range and declin- quent research found that predispersal seed loss ing numbers (Mancuso and Moseley 1998, Bond (i.e., fruit removal), while sometimes intense, 2017), has raised concerns about the species’ occurs sporadically and often represents only long-term viability. Range-wide declines in a portion of total seed loss (Robertson unpub- L. papilliferum have been largely attributed to lished data). More often, ants collect seeds the loss of suitable habitat as a result of urbani - from the soil surface beneath plants after the zation, agriculture, livestock grazing, the spread seeds dehisce from their fruits (Jeffries 2016, of invasive species, and increased wildfire fre- Schmasow and Robertson 2016). quency (Moseley 1994). More recently, seed In the present study, we compared seed sur- predation by Owyhee harvester ants has been vivorship of L. papilliferum plants that were identified as a potentially important source of exposed to harvester ants relative to size- seed loss that may contribute to population matched plants in the same slick spot that were declines of the species (United States Fish and protected from ants. We also tested whether the Wildlife Service 2016). proportion of seeds lost by plants exposed to Owyhee harvester ants, like many other harvester ants, which we established via a com- Pogo nomyrmex species, collect and consume parison of seed numbers with their size-matched seeds from a variety of small-seeded plant and protected counterparts, was inversely species (MacMahon et al. 2000). Among the related to the total number of plants present seeds available to Owyhee harvester ants, in a slick spot. We predicted that the foraging those of slickspot peppergrass are often over- activities of harvester ants would significantly represented in the ant’s diet (Schmasow and reduce seed survivorship at levels equal to Robertson 2016). The vulnerability of L. papil- or exceeding those reported by White and liferum seeds to predation by P. salinus may be Robertson (2009), and that the proportion of enhanced by the combined effects of the ant’s seeds harvested from individual plants would foraging behavior and the plant’s specialized decrease as the number of L. papilliferum habitat requirements. Like many Pogonomyr- plants within a slick spot increased, at least mex species, P. salinus forages collectively along once the number of seeds available in the trunk trails that lead to food patches (Janzen slick spot reached the colony’s threshold for 1971, Hölldobler and Wilson 1990). Mobilization consumption (i.e., satiation threshold). BROWN AND ROBERTSON ♦ SLICKSPOT PEPPERGRASS SEED PREDATION 485

METHODS sparsely populated (Miller and Kinter 2018). Owing to L. papilliferum’s limited distribution, Study Area specific habitat requirements, and declin ing We conducted the study from June to Octo- numbers, the plant was granted federal protec - ber 2012 at a population of L. papilliferum tion as a threatened species in 2016 (United located near Melba, Idaho. The site was cho- States Fish and Wildlife Service 2016). It exhib- sen because it supports a relatively large popu- its 2 life history patterns—annuals that germi- lation of L. papilliferum and has an abundance nate, reproduce, and die within a single season, of har vester ant colonies (~25.5 colonies/ha). and biennials that exist as vegetative rosettes Overstory vegetation consisted of sparsely dis- in their first year and reproduce and die in their tributed patches of Artemisia tridentata (big second year (Meyer et al. 2005). An average- sagebrush) and Ericameria nauseosa (rubber sized biennial (~12–15 cm in overhead diame- rabbitbrush), while the understory was domi- ter) produces 1200–1700 seeds, whereas annu- nated by Poa secunda (Sandberg bluegrass), als usually produce fewer than 250 seeds Bromus tectorum (cheatgrass), and Sisymbrium (Schmasow 2015). The plant’s flowers, which altissimum (tall tumble mustard). typically bloom from mid-May to late June, rely on outcrossed pollination mediated by insects Study Species (Robertson and Klemash 2003). Each mature OWYHEE HARVESTER ANTS.—Pogonomyrmex fruit, or silicle (Holmgren et al. 2005), bears sali nus, the northernmost member of the genus, 2 seeds that drop to the ground when the fruit occurs from southwestern Canada through dehisces late in summer. These seeds become Idaho, Washington, Oregon, northeastern Cali- part of a persistent seed bank that in some years fornia, Nevada, and western portions of Utah, may represent the majority of the population Montana, and Wyoming (Cole 1968, Taber (Mancuso and Moseley 1998). Seeds can remain 1998). A mature colony typically consists of viable in the seed bank for up to 12 years 5000 to 10,000 workers (MacKay 1981, Johnson (Meyer et al. 2005), perhaps longer. 2000), and, like other Pogonomyrmex species, may survive 15–20 years, sometimes longer Seed Predation Experiment (Porter and Jorgensen 1988, MacMahon et al. We selected 20 slick spots that were occu- 2000), as long as the founding queen survives pied by flowering L. papilliferum and located and continues to lay eggs (Gordon 1991). Colo - within 8 m of an active P. salinus colony. This nies are active aboveground from spring to distance is well within the 12-m foraging range autumn whenever surface temperatures are typical of harvester ants (Jorgensen and Porter sufficiently warm (Crist and MacMahon 1991, 1982, MacMahon et al. 2000, personal obser- Taber 1998). Daily foraging activity usually vations). Each ant colony foraged within only occurs in the morning and late afternoon, with one slick spot occupied by L. papilliferum. We periods of inactivity during the hottest por- recorded the total number of flowering L. tions of the day (Hobbs 1985, Crist and Mac - papilliferum plants in each slick spot. Although Mahon 1991). Pogonomyrmex ants are single- we did not enumerate these plants by size, load, central place foragers (Stephens et al. most of the flowering plants in slick spots were 2007). They forage up to 20 m from their nest, either midsized biennials (12–15 cm in diame- with a majority of foraging occurring within ter) or vegetative (i.e., nonflowering) biennial 12 m of the nest (MacMahon et al. 2000, White rosettes. Very few flowering annuals were pres- and Robertson 2009). When P. salinus nests are ent at the site in 2012. in close proximity to one another (i.e., <20 m Within each slick spot, we selected 2 flower- apart), neighboring colonies share nonover - ing L. papilliferum plants matched for size lapping boundaries in the areas between their (overhead surface area), flowering phenology, nests (Howell and Robertson 2015). and distance from the ant colony. One plant SLICKSPOT PEPPERGRASS.—Lepidium papil- from each pair was randomly assigned to the liferum is a small mustard endemic to sage- treatment (ants excluded) and the other to the brush-steppe habitat in southwestern Idaho. control (access by ants). To prevent access by Presently, there are fewer than 100 known ants, we fixed a 15-cm-high, 30-cm-diameter locations where the plant occurs, and many plastic barrier 2 cm deep in the soil around of these locations are heavily disturbed and the base of each treatment plant. Metal stakes 486 WESTERN NORTH AMERICAN NATURALIST (2020), VOL. 80 NO. 4, PAGES 483–491 were used to secure each barrier firmly to the 20 slick spots included in our study, we con- ground. We placed a similar barrier around ducted observations at each of those slick spots each control plant; however, supports were several times per week from June through Sep- used to elevate these barriers 3–5 cm above tember. During each set of observations, we the ground to permit access by harvester ants. noted (1) the presence of harvester ants in the Metal stakes were used to hold the barriers slickspot and whether these ants were collect- in place. We affixed wire mesh over the tops ing and transporting L. papilliferum fruits and/or of all barriers to exclude vertebrates while seeds to their nest, (2) physical signs that ants allowing access to plants by insect pollinators. had clipped seed-bearing fruits directly from To account for the possibility that the eleva- L. papilliferum plants (see Fig. 1a in White ted barriers around control plants may have and Robertson 2009), and (3) the presence of allowed L. papilliferum seeds to disperse beyond L. papilliferum fruit husks in the middens of the perimeter of their barriers, thereby con- nest mounds. In mid-July, at 16 of the 20 ant founding any effects of seed predation with colonies, we aspirated 15–30 harvester ants as seed drift, at 10 of the 20 slick spots we they returned to their respective nests. Ant selected a third L. papilliferum plant that was activity at the remaining 4 colonies was deemed matched with the other 2 for size, flowering too low at the time to permit sufficient sam- phenology, and distance from ant colony. We pling. The ants we aspirated were placed in first placed an elevated 30-cm-diameter bar- glass vials, one vial per colony, along with any rier around these plants, as described previ- food items they were carrying (note: when ously for control plants. We then centered a aspirated, harvester ants steadfastly hold onto larger plastic barrier, 60 cm in diameter and food in their mandibles). In the laboratory, we 15 cm in height, around the elevated barrier. viewed the contents of each vial under 10× This larger barrier was fixed 2 cm deep in the magnification and recorded the number and soil and secured in place with metal stakes. identity of all seeds present. Wire mesh was secured over the top of the Statistical Analyses elevated barrier. Any seeds that drifted beyond the perimeter of the inner barrier would be Using R version 3.5.3 (R Development Core confined to the soil between the inner and Team 2013), we conducted a paired t test to outer barriers. analyze the “access by ants” and “ants excluded” In mid-October, once fruits had dehisced data (n = 20) from the seed predation experi- and dropped their seeds to the ground and ment. Prior to analysis, we log-transformed all signs of foraging within slick spots had seed counts to achieve a normal distribution ceased, we collected the upper 1 cm of soil of the residuals and homogeneity of variance. located within the perimeter of the 30-cm We then used the packages ‘car’ and ‘lme4’ in barrier surrounding each plant. The soil sam- R to conduct a likelihood ratio test on the data ples were placed in paper bags, one bag per that included the “seed drift” data from the plant, and returned to the laboratory. We sifted seed predation experiment (n = 10). These individual samples through a series of increas- data were fit into a generalized linear mixed ingly finer sieves (1.4 mm, 850 mm, 710 mm, model with “number of seeds on soil” as a func- 500 mm, and 250-mm-diameter mesh; Hogen- tion of treatment (i.e., access by ants, ants togler & Co., Inc., Columbia, MD) and counted exclu ded, or seed drift). We included overhead the L. papilliferum seeds trapped by each layer flowering area as a fixed effect. Slick spot was of mesh. We counted only “sound” seeds (Crist added as a random effect to account for the and MacMahon 1992). A seed was considered influence that individual slick spots may have sound (and presumably viable) if it was intact had on seed production by treatment and and withstood light pressure from forceps with- control plants. A planned comparison of the out breaking. Seeds that were not sound typi- least-squares means of the 3 treatment levels cally consisted of seed coats and little or no was conducted using a Tukey’s HSD test in endosperm. R package ‘lsmeans.’ To confirm that there were no significant Foraging Observations treatment-related differences in the overhead To confirm that harvester ants were active flowering area of the plants in our experiment, and foraging on L. papilliferum seeds in all we used a generalized linear mixed model to BROWN AND ROBERTSON ♦ SLICKSPOT PEPPERGRASS SEED PREDATION 487

high density (e.g., 1–75 and >75, followed by 1–100 and >100, and so on). We repeated the test until a significant difference was found or we ran out of comparisons.

RESULTS Seed Predation Experiment There was no statistically significant difference in the overhead flowering area of plants selected for the treatment, control, and seed drift groups (c2 = 0.602, df = 2, P = 0.74). Significantly more seeds were present on the soil surface beneath plants from which ants were excluded than beneath plants that were exposed to ants (Fig. 1; paired t test on transformed values: t19 = −7.98, P < 0.0001). In Fig. 1. Boxplot chart showing the number of Lepidium the comparison of the 20 matched pairs of papilliferum seeds (untransformed values) remaining as a function of barrier treatment (n = 20). The 75th and 25th plants, the median reduction in seeds when percentiles are indicated by the upper and lower limits of ants had access to plants was 89.2% (inter- each box, respectively. The upper and lower ends of the quartile range, 63.9% to 93.9%). This range whiskers represent the 90th and 10th percentile, respec- included 2 instances in which control plants tively. The thick horizontal line within the box represents the median. Different letters above the bars indicate signifi - showed no reduction in seeds compared to cant differences between the groups based on a means their paired treatments, even though ants were comparison of log-transformed values. observed foraging beneath L. papilliferum in those slick spots. When these 2 cases were conduct a likelihood ratio test that compared removed from the analysis, the median reduc- overhead flowering area as a function of treat- tion of seeds when ants had access to plants ment. Slick spot was included as a random increased to 89.8% (interquartile range, 77.8% effect. The values for overhead flowering area to 94.2%). were not distributed normally in any of the The use of barriers to exclude harvester treatments or controls. Log-transformation of ants from access to L. papilliferum had a statis- flowering area values created a normal distri- tically significant effect on the number of bution in all but the controls (i.e., access by seeds remaining on the soil surface when we ants), whereas squaring worsened the distri- compared values of the smaller subset of cases bution. Therefore, we used log-transformed (n = 10) in which all 3 barrier types were pres - values. The overhead flowering area met the ent in a slick spot: access by ants, ants assumption of homoscedasticity prior to and excluded, and seed drift (Fig. 2; c2 = 17.18, after transformation. df = 2, P = 0.0002). Specifically, significantly We used a Wilcoxon rank-sum test in R more seeds were present on the soil directly package ‘coin’ to test whether there was a beneath plants in the seed drift treatment (i.e., point at which an increased number of flower- plants with a raised inner barrier and sealed ing L. papilliferum in a slick spot was associ- outer barrier) than beneath plants that were ated with a significant decrease in proportion exposed to ants (means comparison: P = of seeds lost by individual plants, in which 0.0033). By contrast, there was no significant proportion of seeds lost = (1 − [number of difference between the number of L. papil- seeds from plant exposed to ants / number of liferum seeds beneath plants in the seed drift seeds from plant shielded from ants]). We treatment and the number in the ants-excluded began by comparing values from slick spots treatment (means comparison: P = 0.81). These with 1–50 L. papilliferum plants (low density) results indicate that seed drift does not explain to those with >50 plants (high density). We the low number of seeds found beneath L. then increased the range of values for low papilliferum plants that were exposed to ants. density in increments of 25 and made a corre- Control plants (i.e., caged plants that were sponding adjustment to the range of values for accessible to ants) in slick spots with ≤150 488 WESTERN NORTH AMERICAN NATURALIST (2020), VOL. 80 NO. 4, PAGES 483–491

Fig. 3. The proportion of seeds removed from individual Lepidium papilliferum plants as a function of the number of flowering plants within slick spots. The dotted line indicates the inflection point where the proportion of seeds removed was significantly different between slick Fig. 2. Boxplot chart showing the number of Lepidium spots containing >150 plants and ≤150 plants based on papilliferum seeds (untransformed values) remaining as a a Wilcoxon rank-sum test (P = 0.024). Filled and open cir- function of barrier treatment when only slick spots with cles represent low- and high-density slick spots, respec- the seed drift group are included (n = 10). The 75th and tively. The solid vertical bars show the standard error + 25th percentiles are indicated by the upper and lower (–SE) of the mean proportion of seeds removed by ants limits of each box, respectively. The upper and lower ends for both the high- and low-density slick spots. The mean + of the whiskers represent the 90th and 10th percentile, removal for low-density slick spots was 0.87 – 0.03 com- + respectively. The thick horizontal line within the box pared to 0.51 – 0.17 for high-density slick spots. represents the median. Different letters above the bars indicate significant differences based on a means comparison of log-transformed values. ants. Lepidium papilliferum fruits and seeds made up 74% percent of the 127 food items we collected from 370 ants aspirated near nest flowering L. papilliferum (“low density,” n = entrances (n = 16 colonies, x– = 70% L. papil- 14, range 28 to 137 flowering plants) lost a liferum seeds or fruit per colony [range 0% to significantly higher proportion of their seeds 100%]). than those in slick spots with >150 flowering L. papilliferum (“high density,” n = 6, range DISCUSSION 181 to 647 flowering plants) (0.87 +– 0.03 ver- + sus 0.51 – 0.17, respectively; Fig. 3; Wilcoxon Owyhee harvester ant colonies are a promi- rank-sum test, z = −2.23, P = 0.024). No nent feature of many L. papilliferum popula- other pairings of pooled data for low- and tions throughout the species’ range. In a recent high-density slick spots showed a statistically survey, harvester ant colonies were found at significant difference in the proportion of seeds 28 of 39 (72%) sites occupied by L. papil- lost by control plants. liferum (Miller and Kinter 2018). While the Foraging Observations number and density of ant colonies on the landscape varies among populations (Robert- We observed harvester ants foraging in all son and Robertson 2020), in many locations, 20 slick spots, and L. papilliferum fruit husks including our study site, nearly all slick spots were present in the middens of all 20 har- occupied by L. papilliferum are situated within vester ant colonies associated with a slick spot. 10 m of an ant colony (Robertson unpublished In 16 of those slick spots, we observed ants data). We have shown that in such circum- climbing on L. papilliferum, and in 11 we stances, harvester ants are capable of remov- found individual plants with signs of fruit that ing a large proportion of the seeds produced had been clipped from the plant. We found no by L. papilliferum, at least when the number signs of clipped fruits on plants situated of plants in slick spots is ≤150. Given the within barriers sealed to the ground, nor did longevity of harvester ant colonies (14–30 we find any harvester ants within the cages, years—Porter and Jorgenson 1988), those which suggests that these barriers were effec- colonies located near slick spots with L. papil- tive at preventing seed predation by these liferum represent a persistent source of annual BROWN AND ROBERTSON ♦ SLICKSPOT PEPPERGRASS SEED PREDATION 489 seed mortality and a drain on recruitment to For example, in high-density slick spots, once the soil seed bank. the total number of seeds available exceeded Plants exposed to harvester ants experi- a colony’s capacity or need to retrieve them, enced a median loss of 89.2% of their seeds some plants may have largely escaped or expe- relative to size-matched plants that were rienced lower levels of seed predation than shielded from ants. We attribute these losses others. There is no reason to expect seed pre- to seed predation by ants and not to the effect dation to be spread evenly across all plants in of seeds drifting beyond the perimeters of the a slick spot when the patch contains more raised barriers that surrounded control plants seeds than a colony can utilize. For example, (Fig. 2). This conclusion is supported by our both the timing of seeds reaching the soil sur- observations of harvester ants foraging within face and the distance ants must travel to reach slick spots and returning L. papilliferum seeds specific plants may influence the timing and to their nests, and by the presence of L. papil- intensity of seed predation on individual plants. liferum fruit husks in the middens of all nests Although we did not account for the age or associated with the study. In a previous study, size of colonies in our study, differences in White and Robertson (2009) reported average these parameters may also have influenced the predispersal seed losses in excess of 40% to satiation threshold of colonies (Gordon 1991) individual L. papilliferum plants, but they and contributed to variability in the propor- were unable to provide more precise assess- tion of seeds lost to ants. ments because as fruits matured it became Predator satiation is generally associated increasingly difficult to distinguish between with massive, synchronous reproductive events seeds depredated by ants and those that had by plants. In alpine ash, Eucalyptus delegaten- dropped following dehiscence of fruits. We sis, the synchronous release of large numbers overcame this limitation in the present study of stored seeds following fire results in satia- by measuring the combined effects of pre- and tion of granivorous ants and a greater number postdispersal seed losses. of emergent seedlings (O’Dowd and Gill 1984, The proportion of seeds lost by control see also Andersen 1987). Similarly, mast seed- plants in high-density slick spots (>150 plants) ing, the intermittent and synchronous produc- was significantly lower compared to control tion of large seed crops by a population of plants in low-density slick spots (≤150 plants) perennial plants, is generally viewed as a (Fig. 3). The lower levels of seed loss experi- strategy to reduce the impact of seed preda- enced by control plants in high-density slick tion through predator satiation (Janzen 1971, spots may be a result of predator satiation, Kelly 1994). In slickspot peppergrass, popula- which in harvester ants can result when the tion sizes fluctuate widely in response to the seed storage capacity of a nest is exhausted amount and timing of precipitation during (Whitford and Ettershank 1975, Rissing 1989) the previous winter (Kinter et al. 2013, Bond or more generally when the food require- 2017). In favorable years, large seed crops ments of a colony are met (Gordon 1991). within slick spots may result in predator satia- Alternatively, once a sufficient number of L. tion, thereby allowing many seeds to survive papilliferum seeds had been collected by for- and enter the seed bank. By contrast, in unfa- agers, colonies associated with high-density vorable years when seed crops are low, seed slick spots may have shifted their foraging predation may severely limit recruitment of efforts to other types of seeds to meet the seeds to the seed bank. colony’s nutritional requirements (Kay 2004). Many studies have shown that foraging Further study is needed to address these decisions of harvester ants can change in possibilities given that little is known about response to the types of seeds available near the seed capacity or nutritional requirements nests (e.g., Crist and MacMahon 1992, Pirk et of P. salinus. al. 2009, Miretti et al. 2019). While research to While low sample size may have contributed date suggests that P. salinus prefers L. papil- to the high variability in proportion of seeds liferum seeds to other seeds commonly avail- lost to ants in slick spots with >150 plants, the able (Schmasow and Robertson 2016), it would comparative lack of variability in slick spots be informative to compare the intensity of seed with fewer plants (apart from 2 cases) suggests predation on L. papilliferum among popula- that other factors may have been responsible. tions and years to determine whether the 490 WESTERN NORTH AMERICAN NATURALIST (2020), VOL. 80 NO. 4, PAGES 483–491 results of our study are widely applicable. It is and Krista Summers for assistance in the field possible that the intensity of seed predation and laboratory; Julie Heath and Laura Bond by harvester ants might differ among popula- for assistance with statistical analyses; and tions in response to the local plant community Julie Heath and Marcelo Serpe for helpful or other factors unique to sites. comments on the manuscript. Despite an abundance of research on the foraging ecology of Pogonomyrmex ants, there LITERATURE CITED are few estimates of annual seed intake by colonies, and those that exist are best viewed ALBERT, M.J., A. ESCUDERO, AND J.M. IRIONDO. 2005. Assessing ant seed predation in threatened plants: a as rough approximations given differences in case study. Acta Oecologica 28:213–220. the types of seeds collected by harvester ants ANCHETA, J., AND S.B. HEARD. 2011. Impacts of insect her- and the need to extrapolate short-term mea- bivores on rare plant populations. Biological Conser- surements of foraging rates to seasonal vation 144:2395–2402. ANDERSEN, A.N. 1987. Effects of seed predation by ants intakes. Crist and MacMahon (1992) and Pirk on seedling densities at a woodland site in SE Aus- and Lopez de Casenave (2006) estimated that tralia. Oikos 48:171–174. colonies of P. occidentalis and P. rastratus col- BOND, L. 2017. Trends in counts of slickspot peppergrass lect ~60,000 and ~81,000 seeds, respec- (Lepidium papilliferum) on habitat integrity and population monitoring transects, 2005–2015. Report pre- tively, per season. Tschinkel (1999) found that pared for United States Fish and Wildlife Service, colonies of P. badius stored up to 300,000 Boise, ID. seeds within their nests, although it is unclear COLE, A.C. 1968. Pogonomyrmex harvester ants: a study whether these stores were accumulated in a of the genus in North America. University of Ten- single season or over longer periods of time. nessee Press, Knoxville, TN. CRAWLEY, M.J. 2000. Seed predator and plant population While there are no estimates of seasonal seed dynamics. Pages 167–182 in M. Fenner, editor, Seeds: intake by P. salinus colonies, it is reasonable the ecology of regeneration in plant communities. to assume that the intake would be similar to 2nd edition. CABI Publishing, Wallingford, United other Pogonomyrmex species. Our finding Kingdom. CRIST, T.O., AND J.A. MACMAHON. 1991. Foraging patterns that the proportion of seeds lost by plants of Pogonomyrmex occidentalis (Hymenoptera: Formi- declined when plant numbers in slick spots cidae) in a shrub-steppe ecosystem: the roles of exceeded 150 (~200,000 seeds—Schmasow temperature, trunk trails, and seed resources. Envi- 2015) provides a sense of how seed survivor- ronmental Entomology 20:265–275. CRIST, T.O., AND J.A. MACMAHON. 1992. Harvester ant for- ship in L. papilliferum may be affected by aging and shrub-steppe seeds: interactions of seed Owyhee harvester ants. Overall, our results resources and seed use. Ecology 73:1768–1779. suggest that slick spots supporting large num- FISHER, H., L. ESLICK, AND M. SEYFRIED. 1996. Edaphic bers of L. papilliferum in a given year may be factors that characterize the distribution of Lepidium papilliferum. Idaho Bureau of Land Management buffered from the effects of seed predation by Technical Bulletin No. 96-6, Boise ID. harvester ants, whereas those with relatively GORDON, D.M. 1991. Behavioral flexibility and the forag- few plants may suffer high levels of seed loss. ing ecology of seed-eating ants. American Natu- Lepidium papilliferum populations that con- ralist 138:379–411. HOBBS, R.J. 1985. Harvester ant foraging and plant spe- sistently support only small numbers of plants, cies distribution in annual grassland. Oecologia 67: of which there are many (Miller and Kinter 519–523. 2018), are likely to be particularly vulnerable HÖLLDOBLER, B., AND E.O. WILSON. 1990. The ants. to the detrimental effects of seed predation, 1st edition. Harvard University Press, Cambridge. given the longevity of ant colonies and the HOLMGREN, N.H., P.K. HOLMGREN, AND A. CRONQUIST. 2005. Intermountain flora, vascular plants of the preference exhibited by these ants for L. papil- Intermountain West, U.S.A. Volume 2, Part B, Sub- liferum seeds. class Dilleniidae. New York Botanical Garden Press, Bronx, NY. HOWELL, B.D., AND I.C. ROBERTSON. 2015. Reclaiming ACKNOWLEDGMENTS lost territory: the response of Owyhee harvester ants to forager intrusions by neighboring colonies. Jour- Funding for this project was provided by nal of Insect Behavior 28:722–731. the Idaho Army National Guard (IDARNG) INOUYE, R.S., G.S. BYERS, AND J.H. BROWN. 1980. Effects and Boise State University. We thank Charles of predation and competition on survivorship, fecun- Baun (IDARNG) for his interest and support dity, and community structure of desert annuals. Ecology 61:1344–1351. of the project; David Wisniewski, Triton JANZEN, D.H. 1971. Seed predation by animals. Annual Rimkus, Samantha Kirkendall, Tristan Froerer, Review of Ecology and Systematics 2:465–492. BROWN AND ROBERTSON ♦ SLICKSPOT PEPPERGRASS SEED PREDATION 491

JEFFRIES, M.I. 2016. An investigation of herbivory and PORTER, S.D., AND C.D. JORGENSEN. 1988. Longevity of seed predation on slickspot peppergrass. Master’s harvester ant colonies in southern Idaho. Journal of thesis, Boise State University, Boise, ID. 94 pp. Range Management 41:104–107. JOHNSON, R.A. 2000. Seed-harvester ants (Hymenoptera: R DEVELOPMENT CORE TEAM. 2013. R: a language and Formicidae) of North America: an overview of ecol- environment for statistical computing. R Foundation ogy and biogeography. Sociobiology 36:89–122. for Statistical Computing, Vienna, Austria. http:// JORGENSEN, C.D., AND S.D. PORTER. 1982. Foraging behav- www.R-project.org ior of Pogonomyrmex owyheei in southeast Idaho. REICHMAN, O.J. 1979. Desert granivore foraging and its Environmental Entomology 11:381–384. impact on seed densities and distributions. Ecol- KAY, A. 2004. The relative availabilities of complementary ogy 60:1085–1092. resources affect the feeding preferences of ant RISSING, S.W. 1989. Long-term regulation of the foraging colonies. Behavioral Ecology 15:63–70. response in a social insect colony (Hymenoptera: KELLY, D. 1994. The evolutionary ecology of mast seeding. Formicidae: Pogonomyrmex). Journal of Insect Behav- Trends in Ecology and Evolution 9:465–470. ior 2:255–259. KINTER, C.L., J.R. FULKERSON, J.J. MILLER, AND D.L. ROBERTSON, I.C., AND W. G. R OBERTSON. 2020. Colony CLAY. 2013. Draft habitat integrity and population dynamics and plant community associations of the monitoring of Lepidium papilliferum (slickspot pep- harvester ant, Pogonomyrmex salinus (Hymenoptera: pergrass): 2012. Idaho Natural Heritage Program, Formicidae) in sagebrush-steppe habitat. Environ- Idaho Department of Fish and Game, Boise, ID. mental Entomology 49:983–992. MACKAY, W.P. 1981. A comparison of the nest phenologies ROBERTSON, I.C., AND D. KLEMASH. 2003. Insect-medi- of three species of Pogonomyrmex harvester ants ated pollination in slickspot peppergrass, Lepidium (Hymenoptera: Formicidae). Psyche 88:25–74. papilliferum L. (Brassicaceae), and its implications MACMAHON, J.A., J.F. MULL, AND T.O. C RIST. 2000. Har- for population viability. Western North American vester ants (Pogonomyrmex spp.): their community Naturalist 63:265–268. and ecosystem influences. Annual Review of Ecol- SCHMASOW, M.S. 2015. Diet selection by the Owyhee har- ogy and Systematics 31:265–291. vester ant (Pogonomyrmex salinus) in southwestern MANCUSO, M., AND R.K. MOSELEY. 1998. An ecological Idaho. Master’s thesis, Boise State University, Boise, integrity index to assess and monitor Lepidium papil - ID. liferum (slickspot peppergrass) habitat in southwest- SCHMASOW, M.S., AND I.C. ROBERTSON. 2016. Selective ern Idaho. Idaho Department of Fish and Game, foraging by Pogonomyrmex salinus (Hymenoptera: Boise, ID. Formicidae) in semiarid grassland: implications for a MEYER, S.E., D. QUINNEY, AND J. WEAVER. 2005. A life rare plant. Environmental Entomology 45:952–960. history study of the Snake River plains endemic STEPHENS, D.W., J.S. BROWN, AND R.C. YDENBERG. 2007. Lepidium papilliferum (Brassicaceae). Western North Foraging behavior and ecology. University of Chicago American Naturalist 65:11–23. Press, Chicago, IL. MILLER, J.J., AND C.L. KINTER. 2018. Field assessment of TABER, S.W. 1998. The world of harvester ants. 1st edition. Lepidium papilliferum (slickspot peppergrass) ele- Texas A&M University Press, College Station, TX. ment occurrences: Snake River Plain and adjacent TSCHINKEL, W.R. 1999. Sociometry and sociogenesis of foothills. Report prepared for Idaho Natural Heri- colony-level attributes of the Florida harvester ants tage Program, Idaho Department of Fish and Game, (Hymenoptera: Formicidae). Annals of the Entomo- Boise, ID. logical Society of America 92:80–89. MIRETTI, M.F., J. LOPEZ DE CASENAVE, AND R.G. POL. UNITED STATES FISH AND WILDLIFE SERVICE. 2016. Endan- 2019. Stereotyped seed preferences of the harvester gered and threatened wildlife and plants; threatened ant Pogonomyrmex mendozanus in the central Monte status for Lepidium papilliferum (slickspot pepper- Desert. Arthropod-Plant Interactions 13:771–778. grass) throughout its range; Final Rule. Federal Reg- MOSELEY, R.K. 1994. Report on the conservation status of ister 81(159):55058–55084. Lepidium papilliferum. Idaho Department of Fish WENNINGER, A., T.N. KIM, B.J. SPIESMAN, AND C. GRAT- and Game, Boise, ID. TON. 2016. Contrasting foraging patterns: testing O’DOWD, D.J., AND A.M. GILL. 1984. Predator satiation resource-concentration and dilution effects with pol- and site alteration following fire: mass reproduction linators and seed predators. Insects 7(2): Art. 23. of alpine ash (Eucalyptus delegatensis) in southeast- 11 pp. https://doi.org/10.3390/insects7020023 ern Australia. Ecology 65:1052–1066. WHITE, J.P., AND I.C. ROBERTSON. 2009. Intense seed pre- PIRK, G.I., AND J. LOPEZ DE CASENAVE. 2006. Diet and dation by harvester ants on a rare mustard. Eco- seed removal rates by the harvester ants Pogono- science 16:508–513. myrmex rastratus and Pogonomyrmex pronotalis in the WHITFORD, W.G., AND G. ETTERSHANK. 1975. Factors central Monte Desert, Argentina. Insect Sociaux 53: affecting foraging activity in Chihuahuan desert har- 119–125. vester ants. Environmental Entomology 4:689–696. PIRK, G.I., J. LOPEZ DE CASENAVE, R.G. POL, L. MARONE, AND F.A. MILESI. 2009. Influence of temporal fluctua- Received 3 December 2019 tions in seed abundance on the diet of harvester ants Revised 16 April 2020 (Pogonomyrmex spp.) in the central Monte Desert, Accepted 8 May 2020 Argentina. Austral Ecology 34:908–919. Published online 31 December 2020 Copyright of Western North American Naturalist is the property of Monte L. 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