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Article

Dispersal Patterns of One-Seed Juniper Seeds Contained in Mammal Scats and Bird Pellets

by
Dave Stricklan
1,*,
Andrés F. Cibils
1,
Pradip Saud
2,
Robert L. Steiner
3,
Matthew M. McIntosh
1,
Amy C. Ganguli
1,
Douglas S. Cram
4 and
Akasha M. Faist
5
1
Department of Animal and Range Sciences, New Mexico State University, Las Cruces, NM 88003, USA
2
Arkansas Forest Resources Center, College of Forestry, Agriculture, and Natural Resources, University of Arkansas at Monticello, Monticello, AR 71656, USA
3
Department of Applied Statistics & International Business, New Mexico State University, Las Cruces, NM 88003, USA
4
Department of Extension Animal Sciences and Natural Resources, New Mexico State University, Las Cruces, NM 88003, USA
5
Department of Ecosystem and Conservation Sciences, University of Montana, Missoula, MT 59812, USA
*
Author to whom correspondence should be addressed.
Forests 2022, 13(10), 1693; https://doi.org/10.3390/f13101693
Submission received: 24 July 2022 / Revised: 28 September 2022 / Accepted: 10 October 2022 / Published: 14 October 2022
(This article belongs to the Section Forest Ecology and Management)
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Abstract

:
We conducted a two-year study in New Mexico, USA, to determine the role of birds, lagomorphs, mesocarnivores, and porcupines in one-seed juniper (J. monosperma (Englem.) Sarg.) seed dispersal. We established random plots: (1) around cone-bearing juniper trees in the woodland; (2) around non-cone-bearing juniper trees in the woodland; (3) in woodland/grassland transition zones; and in (4) grassland habitats near juniper woodlands. We estimated seed density and tallied the number of plots with seeds deposited by each disperser group. Birds deposited the highest number of seeds/ha under the canopy of cone-bearing trees. Mesocarnivores were responsible for the highest average seed deposition in all other habitats. In juniper cone-bearing tree habitats, birds deposited seeds in 100% of plots under-canopy and 93% of plots outside-canopy. Seeds deposited by lagomorphs were observed in plots across all sampled habitats. Overall, seed deposition was greatest around cone-bearing juniper trees, followed by non-cone-bearing juniper trees, woodland-grassland transition zones, and grassland habitats. Birds deposited seeds primarily under cone-bearing tree perch sites. Lagomorphs deposited seeds widely in relatively high numbers across all habitats and are likely responsible for the greatest number of one-seed juniper seeds deposited on the soil surface at our research site.

1. Introduction

Globally, the rate of woody species encroachment and recolonization into savanna and grassland habitats is accelerating [1,2,3], with many of the underlying causes connected to land use patterns [3,4,5,6], yet specific understanding of this process often remains incomplete and underappreciated. One-seed juniper (J. monosperma) is the dominant woody plant on millions of hectares of mid-elevation rangelands in New Mexico, Arizona, Colorado, and parts of western Texas, USA [7]. One-seed and other juniper species encroach into and recolonize nearby grassland and savanna habitats [8,9,10]. In general, juniper woodland recolonization results in reduced understory biomass production [11,12,13], reduction of soil water availability to other plants [14], and loss of grassland bird habitat [15,16] and sagebrush habitats [17].
Drivers of woody species encroachment and recolonization are complex [1,18] but are generally thought to be primarily associated with factors linked to past and present herbivory regimes by livestock [1,6], with associated reduced fire frequencies [6], and with atmospheric CO2 and ambient temperature increases [19]. However, there is evidence that grazing is not always a driver of woody species encroachment and habitat recolonization [20]. Once juniper seeds have been zoochorously delivered to a site and germinate, competition for water and light primarily control survival and growth [21]. The putative role of seed placement by dispersers on the eventual footprint of Juniperus spp. woodland stands is well-recognized [22,23]. Several studies have successfully documented Juniperus spp. seed dispersal by animals that ingest the berry-resembling cones and subsequently deposit viable seeds on the landscape (frugivory), [24,25,26]; or transport and dispersal of seeds that have been previously deposited on the landscape by animals (diplochory) [27,28].
The primary mechanism for the beyond-canopy movement of juniper seeds is dispersal by vertebrate animals [29,30,31]. Frugivores can ingest the outer fleshy pericarp of the juniper cone (commonly called a berry), which contains the seed(s). The seeds are exposed to acids in the animal’s digestive tract and later deposited in pellets or scats at varying distances from the parent tree, depending on the behavior of the animal seed disperser [32]. The full process of ingestion, transport, and deposition of a seed is referred to as endozoochory [33]. Zootransport and diplochory of juniper seeds by small mammals can also be a method of juniper seed transport [26,28]. The dispersal pattern of seeds is fundamental to the ultimate location of tree establishment in juniper woodlands [25,34]. This seed dispersal pattern and recolonization of woodland stands have been evaluated for Juniper spp. in relation to frugivorous birds [23,29,35], diplochory and zoo transport by small mammals [27,28] and complex animal seed dispersal assemblages [22,31,36].
Our overarching objective was to determine the role of different animal groups in dispersing one-seed juniper seeds in woodland and nearby grassland habitats. We hypothesized that in our study area: (1) birds were the primary dispersers of juniper seed; (2) that mesocarnivores would be the primary out-stand distributors of seed; and (3) that birds would be the most important seed distributors in all habitat categories. We were also interested in understanding if some seed movement was attributable to other potential dispersers such as bears, porcupines, or ungulates and if scatter hoarding and/or burial by small mammals was an important component of seed dispersal in our study area.

2. Materials and Methods

2.1. Study Area

Our study was conducted in one-seed juniper woodlands in central New Mexico, USA at the New Mexico State University Corona Range and Livestock Research Center (Corona Ranch) in Torrance and Lincoln counties, and at the Cibola National Forest, which is located approximately 25 km west of the Corona Ranch in Lincoln County. Elevation at the study sites ranges from 1735 to 2360 m. The climate is semiarid continental, characterized by warm summers and cold winters. Mean annual precipitation is 40 cm and the average maximum and minimum annual temperatures are 18.1 °C and 3.7 °C [37]. We conducted fieldwork from late December through the end of February in 2017 and 2018. The woodland overstory was dominated by one-seed juniper (J. monosperma) and two-needle pinyon pine (Pinus edulis). The understory within the woodlands was a mixed cool and warm season grass community including blue grama (Bouteloua gracilis) and spike dropseed (Sporobolus contractus). Prominent species in the grassland habitats adjacent to the woodlands were blue grama (Bouteloua gracilis), New Mexico feathergrass (Hesperostipa neomexicana), and buffalo grass (Bucholoe dactyloides) [38]. The transition zone between the woodlands and grasslands generally retained the grassland understory with interspersed juniper saplings.

2.2. Study Species

J. monosperma is a shrub or small tree that generally grows to 2–7 m, but very old individuals can approach 12 m. Mature individuals often have multiple stems and a rounded canopy. Plants are predominantly diaceous. Pollen is shed in late winter or early spring. Cones begin to mature in late fall and continue to ripen over the winter [7]. Seed cones are berry-like, soft, and pulpy with an ovoid shape 6–8 mm in size. Seeds are 4–5 mm long and generally occur singly in cones. J. monosperma is strongly dioicous and is distributed from central Arizona through New Mexico, southern Colorado, and into Oklahoma and Texas [7]. On portions of our study site, it was a codominant with pinyon pine (Pinus edulis). In much of New Mexico, including our study site, it aggressively recolonizes into grassland sites [7,9,25]. When snow cover reduces the availability of other food sources the pulpy cones provide a readily available food source to birds, small mammals, and mesocarnivores. The timing of seed dispersal and deposition of seeds on the landscape corresponds with a frugivory activity [38].

2.3. Study Design

We sampled the dispersal of animal-deposited one-seed juniper seeds within juniper woodlands and bordering grasslands habitats. To establish the location of seed collection plots we overlaid 100 m2 grid lines on aerial images of juniper woodland and nearby grassland habitats. We then randomly selected 100 m2 grid cells for each of four habitat categories: woodland directly around a cone-producing tree; woodland directly around a non-cone-producing tree; grassland areas near woodlands; and transition zone between grassland and woodlands. Inside the 100 m2 cells we established a random point to serve as a focal point for 25 m. radius sampling plots. The random focal point served as the center of the study plot in the grassland and transition zone categories. In woodland habitats, we selected the nearest mature juniper to the random focal point that fit the category of the plot (cone-producing tree or non-cone producing tree). We then used the selected juniper as the center of the 25 m. radius sample plot. Juniper seed production events can be erratic [39,40] and localized [41]. If a randomly selected 100 m2 cell for the cone-producing category did not contain a cone-producing tree we randomly selected another 100 m2 cell. Within the woodland there were cone-producing trees at various distances from the center of our non-cone producing tree plots. We accepted this as part of the natural variability within a woodland, except if any part of the canopy of a cone-producing tree was within the border (25 m radius) of a non-cone tree producing plot. In that instance, we selected another grid cell and established a non-cone producing tree plot in it. Because of the localized and concentrated nature of juniper cone production within the woodland, juniper cone trees and therefore our study plots within the woodlands had a clumped arrangement (Supplementary Materials, Figure S1).
At cone tree and non-cone tree plots, we categorized animal-deposited pellets and seeds within the 25 m transects as either under-canopy or beyond-canopy of the center point focal tree. In order to better understand seed dispersal in the immediate transition zone between mature juniper woodlands and open grasslands we added a fourth category during the second year of the study. We called this habitat the transition zone. Sites were considered to be juniper woodlands if they contained three or more mature juniper trees within a 50 m2 area surrounding the random location point, however, the density of juniper trees in the woodland was often considerably greater than this minimum criterion. If a one-seed juniper tree was three meters tall and had at least one trunk with a diameter at breast height (dbh) of 7 cm, we considered it to be mature because female trees of these dimensions could generally produce cones. Most mature one-seed junipers in the study area had larger dimensions than the minimum criteria. Sample plots that we classified as grassland were within 1.5 km of a mature female one-seed juniper but contained no mature juniper within one hundred meters of the plot center. We considered habitat transition zones to be areas with at least fifteen juniper saplings/100 m2 but without a mature juniper component.
In 2018, juniper cone production in our study area was rare, so relatively few cells throughout the entire study area were available to establish cone tree sample plots. We were concerned that concentrated sampling in the same woodland stands might compromise the independence of our sample plots, so we expanded the study area to portions of the nearby (approximately 25 km to the west), Gallinas Mountains in the Cibola National Forest. In the Gallinas Mountains, we included only woodlands where pinyon pine (Pinus edulis) but not ponderosa pine (Pinus ponderosa) occurred, to match the woodland characteristics on the NMSU Corona Ranch, where Ponderosa pine was not present. To assess the general pattern of seed dispersal in sample plots we compared the number of seeds deposited by dispersal groups in each habitat category.
Within plots in all habitats, we established four 1 × 25 m belt transects, at the center point of the plot and oriented them in the cardinal directions (Figure 1). We carefully searched these transects for pellets and scats. We collected all of the pellets and scats within the plot transects. We also carefully looked for evidence of buried or cached seeds while we took measurements and data at each sample plot. We only collected seeds that were associated with the pellet or scat matrix from an identifiable seed disperser group. A standard field guide was used for pellet and scat verification [42]. Pellets or scats were used to identify the seed disperser responsible for depositing the seed. Transition zone and grassland plots contained no center focal juniper tree, so all seeds were classified as outside the canopy. Because of the relatively low occurrence of mesocarnivore (see species included in this group below) scats in the belt transects, we searched the entire circular plot for scats. We collected the first mesocarnivore scat we encountered in the plot circle for seed density analysis and then made a tally of the other mesocarnivore scats located within the study plot. We used the average of seeds/scat from the first scats encountered in all plots as an estimate of the average number of seeds in other scats. When occasional snowstorms left the ground with a light snow cover, we discontinued searches until the snow had melted and pellets or scats were again readily detectable. Snow melt typically occurred within a few to 48 h. On a few occasions, we encountered one or several bare one-seed juniper seeds that appeared to have weathered out of a pellet or scat and were no longer encased in an identifiable deposition matrix. To be confident that a seed had been dispersed by a known disperser group, we required clear evidence of association with that group and did not include non-matrix identifiable seeds.
We combined seeds from pellets and scats into functional seed disperser animal groupings. We combined all bird species into a single seed disperser group. Likewise, we combined all seeds from mesocarnivore scats into a single mesocarnivore group and seeds from all lagomorphs into a single lagomorph category. The porcupine (Erethizon dorsatum) group had a single member. The most common species of bird that we observed during the study was the mountain bluebird (Sialia currucoides). We also observed western bluebirds (Sialia mexicana) and Cassin’s finches (Haemorhous cassinii) eating one-seed juniper cones. It is common to see other birds in one-seed juniper stands, but during the study years, we did not observe them in the study area. Coyotes (Canis latrans) and gray fox (Urocyon cinereoargenteus) were the primary mesocarnivores in the study area, although kit fox (Vulpes macrotis) were taken by trappers in the winter of 2018 from the grassland near our study area. Black-tailed jackrabbits (Lepus californicus) and desert cottontail (Sylvilagus audubonii) were the lagomorphs present in our study area. Elk (Cervus canadensis) and mule deer (Odocoileus hemionus) pellets were sometimes present in the sample plots but did not contain one-seed juniper seeds. We found one black bear (Ursus americanus) scat and numerous American badger (Taxidea taxus) scats in the sample plots, but none of them contained juniper seeds and therefore are not represented in the seed distributor data. Elsewhere in New Mexico, bear scats commonly contain one-seed juniper seeds [43]. Seed-containing matrix material was secured in resealable plastic bags and stored at ambient temperature for later evaluation in the lab.

2.4. Seed Counts

We estimated the number of seeds/ha deposited by each seed distributor group in each of the habitats sampled. In order to separate juniper seeds from pellet and scat matrix material we manually forced the pellet or scat matrix materials through a no. 10 (2.0 mm) mesh U.S.A. standard testing soil sieve, leaving the seeds on the screen mesh. We did not estimate seeds/pellets because bird pellets were fragile and did not always hold together as a single unit during collection or transport. Further, some transects had hundreds of pellets from birds, lagomorphs, or porcupines so we forced them through the soil sieve screen en masse (by distributor group), which precluded an estimate of seeds/individual pellets.
For grassland and transition zone plots we took the total number of seeds from each distributor group in each 1 × 25 m belt transect and divided by 25 to obtain the number of seeds/m2. We then multiplied the seeds/m2 value by 10,000 to obtain an estimate of the seeds/ha value per distributor group. We followed the same protocol with transects in cone tree and non-cone tree plots except we broke the 25 m transect into under-canopy and beyond-canopy categories. So for example, if the under-canopy section of the transect was 3.4 m long and the outside-canopy section of the transect was 21.6 m long we would divide the number of seeds collected under the canopy by 3.4 and the number of seeds collected beyond the canopy by 21.6 and then multiply each value by 10,000 to obtain the number of seeds/ha for under-canopy and beyond-canopy. Mesocarnivore scats were distributed less evenly across our study plots so in all habitat categories we counted the total number of scats within the full 25 m radius plot and then multiplied the number of scats by a standard factor of 150 seeds in cone tree habitats and 148 seeds in non-cone tree habitats, which were the averages of the first collected scats of all plots for those habitat categories. We then divided the total number of seeds from mesocarnivore scats for the entire plot by 1963, which is the number of square meters in a 25 m radius plot, and multiplied that number by 10,000 to determine the estimated number of mesocarnivore seeds in a hectare.

2.5. Statistical Analyses

We used R [44] for statistical analysis of the data except for the analysis of pellet/scat presence in study plots where we used PROC FREQ in SAS 9.4 (SAS Institute, Cary, NC, USA). To account for the large difference in seeds/ha deposited by specific seed disperser groups and for the high number of plots with a zero value, we applied a log transformation on the seed counts (log (seeds + 1)) per hectare. We used a two-way analysis of variance (ANOVA) to explore the patterns of seed dispersal by habitat classifications and seed disperser group as main effects. We conducted a posthoc Tukey HSD test on the mean difference in the log value of seeds between and across the habitat classifications and seed disperser groups. We used Chi-square tests and the Cochran–Mantel–Haenszel (CMH) statistic to analyze the frequency of plots with seed-containing pellet/scat presence and determine whether seed disperser groups were similarly represented within and across habitats. A probability value of 0.05 was used to determine statistical significance.

3. Results

The estimated total number of seeds/ha deposited by animal disperser groups was highest directly under the canopy of juniper cone-producing trees, where birds deposited the highest average number of seeds/ha (117,989 ± 19,387 SEM) followed by mesocarnivores (107,200 seeds/ha ± 65,977 SEM; Table 1). In habitats at increasing distance from a cone tree source, the overall total number of seeds/ha decreased greatly and shifted in dominance from bird to mesocarnivore-deposited (Table 1). Porcupines were minor contributors to the total number of animal-deposited seeds/ha. in all habitats.
The log value for the number of seeds/ha was significantly influenced (p < 0.05) by the interaction of the habitat classification and disperser group (Table 1; Supplementary Materials Table S1). There were significant differences in the mean number of seeds/ha (log-transformed) deposited in different habitat classifications except between juniper non-cone tree and transition zone habitats.
Seed disperser groups as a whole deposited significantly more seeds in juniper cone tree habitats than in juniper non-cone tree and transition zone habitats, which in turn had significantly more seed deposition than grassland habitats (Figure 2a). Lagomorphs deposited significantly more seeds/ha in all habitats combined than birds or mesocarnivores, which in turn deposited more seeds/ha than porcupines (Figure 2b).
Mesocarnivores, lagomorphs, and birds were primarily responsible for seed dispersal around cone trees. Lagomorphs and mesocarnivores were primarily responsible for seed dispersal in juniper woodlands around juniper non-cone trees. In the transition zone and in grasslands, lagomorphs were the principal seed-dispersing vectors (Figure 3).
Areas around juniper cone trees had the highest predicted mean log values of seeds/ha, followed by areas around juniper non-cone trees, then areas in the transition zone, and lastly grassland areas. Lagomorphs had the highest estimated mean log value for seeds/ha dispersed in all habitats (Figure 4). The presence of animal-deposited seeds in sample plots (both years combined except for the transition zone which was only included in 2018) was highest for lagomorphs in all habitats (grassland: 18%; transition zone: 50%; non-cone tree beyond-canopy: 64%) except in juniper cone tree beyond-canopy and under-canopy habitats. In beyond-canopy habitats, lagomorphs and birds deposited seeds in 93% of the plots. In cone tree under-canopy habitats lagomorphs and birds deposited seeds in 82% and 100% of study plots, respectively. Birds deposited seeds in 100% of the juniper cone tree under-canopy plots. Mesocarnivore and porcupine-deposited seeds were also present in all habitats but in a lower total number of plots compared to lagomorphs (Table 1).
The frequency of seed-containing pellets or scats in each habitat (juniper cone tree, juniper non-cone tree, and grassland) in 2017 (transition habitat not sampled), was significantly associated with the animal seed distributor group (p < 0.01; Table 2). More than 85% of juniper cone tree plots had bird, lagomorph, and mesocarnivore pellets/scats containing one-seed juniper seeds, but porcupine pellets were present in only a few plots of the various habitats (Table 2). The frequency of plots with lagomorph pellets tended to be highest in all habitats in 2017 (Table 2). In 2018, we found the same seed distributor group relationship, (p < 0.01) for juniper cone tree, juniper non-cone tree, and transition habitats, but not for grassland habitats (Table 2). The frequency of plots with lagomorph pellets containing one-seed juniper seeds tended to be highest in all habitats (except grasslands) again in 2018 (Table 2). We found a significant overall relationship between habitats and seed distributor group when both years were analyzed jointly using the CMH statistic (p < 0.01; Table 2). Small mammal activity resulting in burying or caching J. spp. seeds has been reported elsewhere [27,28] but was not detected in any of our study plots.

4. Discussion

Our hypothesis that birds were the primary dispersal vector of one-seed juniper seed in woodland, transition zone, and grassland habitats was not supported by the data. Lagomorphs and mesocarnivores moved more seeds, more often, in all habitats except directly around juniper cone-producing trees than did birds. Zoochory by avian frugivores is often emphasized as the primary driver of Juniperus spp. seed dispersal, especially in the North American literature [35,45]; although dispersal by other animals [26,29,43]; diplochory [27], and transport and burial by small mammals [28] are also known. In our study, the dispersal of one-seed juniper seeds by birds was primarily concentrated in areas around cone-producing trees. Bird pellets containing juniper seeds were heavily clustered beneath the canopy of cone-producing trees. Birds are known to deposit seeds below power lines and fence lines [46], but we often observed rabbit and porcupine pellets containing one-seed juniper seeds beneath putative bird perch sites such as walking stick cholla cactus (Cylindropuntia imbricata), wooden fence posts, and windmill scaffolding. In juniper woodlands not in close proximity to juniper cone trees, bird pellet numbers and presence was not a major contributor to seed deposition numbers and it is clear that birds were not the primary animal vector facilitating seed movement of one-seed juniper into transition and grassland habitats. Birds, lagomorphs, mesocarnivores, and porcupines all moved viable one-seed juniper seeds [47], but the amount and location of dispersal were strongly influenced by habitat and seed distributor group.
Our hypothesis that mesocarnivores were primarily responsible for out-stand seed dispersal was only partially supported by the data. We observed widespread seed dispersal across all habitats by lagomorphs as well. Mesocarnivores [31,48] and lagomorphs [49,50] are known juniper seed dispersers elsewhere and in our study area were responsible for the dispersal of the greatest number of seeds in all habitats except directly below the canopy of the cone-producing trees. Mesocarnivores did deposit seeds in a clumped pattern as we predicted. Lagomorphs moved seeds widely across habitats, especially into grass openings in woodlands. Lagomorphs and, to a lesser degree, mesocarnivores, appeared to be moving seeds within the juniper woodland including into stands where no seed-producing trees are currently present. Porcupines were also responsible for distributing seeds within the juniper woodland and into adjacent grasslands, but in much lower numbers and frequency (Table 1).
The presence of seedlings and saplings in grassland openings within the juniper woodland and in adjacent grasslands away from bird perch sites suggests that mesocarnivores and especially lagomorphs play a crucial role in woodland infill into grassland areas at our site. Lagomorphs deposit pellets in concentrated latrines in some areas [24], but in central New Mexico lagomorph seed-containing pellets were the most widely and evenly distributed of all the scat and pellet deposition matrices, as evidenced by the relatively high presence value of lagomorph pellets in sample plots in all habitat categories. The role of lagomorphs as juniper seed distributors is perhaps underestimated in some other juniper woodlands and adjacent grasslands. Lagomorph pellets contain a single to several seeds/pellet and are more uniformly spread across all the habitats in our study area, making it more likely that lagomorphs distribute seeds to microsites that facilitate successful germination and subsequent seedling establishment.
Porcupines dispersed seeds at specific locales in juniper woodlands, adjacent transition zones, and grasslands. In woodland settings, they deposited seed-containing pellets in piles under the canopy of the cone-producing one-seed juniper as well as under the canopy of two-needle pinyon pine (Pinus edulus), where they are known to roost and feed on the inner bark [51]. In juniper recolonization zone habitats or even deeper into grassland habitats, porcupines are also known to deposit pellets at the base of walking stick cholla [47]. They are also known to leave pellets in caves or rock outcrops in habitat that provides shelter [52,53]. There are several important waypoints on the pathway from seed production to the establishment and maintenance of juniper woodland, but the total number of seeds delivered per hectare should not be discounted and deserves further analysis, especially relating to the differential success rates of juniper seeds delivered by various animal distributors. Non-ingested cones that contain seeds fall to the soil surface directly under the canopy of cone-producing trees throughout the fruiting season [47]. The under-canopy area is also where the greatest number of seeds are deposited by animal seed distributors. However, the seed rain and heavy accumulation of seed deposition from animal seed distributors did not result in concentrations of saplings under the canopy of juniper non-cone trees, regardless of whether they were female trees (which could have produced seed in previous years) or male trees. Therefore, we chose to only include out-canopy values for seed numbers and presence for juniper cone tree plots. We did observe a pattern of attenuation of the number of animal-deposited seeds in habitats at an increasing distance from seed tree sources.
Pellet and scat matrices from different seed distributors have differential influences on the germination of seeds encased within them [47]. One-seed juniper seeds encased in a bird-deposited matrix had a higher average germination rate than seeds encased in various mammalian-deposited matrices, which were generally larger and denser. The concentration of seeds in an area likely increases intraspecific competition among potential seedlings [29,54] and therefore likely results in the lower seedling establishment per germinable seed. For example, red fox (Vulpes vulpes subsp. ichnusae) scats contained 73–86 J. phoenicea seeds [55] whereas mesocarnivore scats in our study contained 100–500 seeds. Bird [25] or lagomorph [50] pellets may contain one to several juniper seeds but bird pellets in our study area were often deposited in concentrations directly below perch sites, while lagomorph pellets were scattered singly or in small groups across the landscape. Seedlings originating from widely spaced pellets, containing only a few seeds presumably experience lower intra-specific competition than seedlings originating from pellets in congregations of dozens (porcupines) or many hundreds (birds), or in larger scats (mesocarnivores and bears), or in small mammal seed caches or rabbit latrine areas. The wider spacing of germinates originating from seeds in lagomorph pellets could favor seedling survival in our study area, but this hypothesis requires further investigation.

5. Conclusions

Our study suggests that in addition to commonly cited proximal causes of woody plant recolonization such as single-species livestock grazing and fire suppression [3] indirect impacts of land management on the ecology of seed dispersal vectors need to be considered. A more nuanced understanding of the interactions among climate, juniper cone crops, seed disperser population cycles, and agricultural uses of juniper-recolonized rangelands is needed to provide site-specific land management guidelines. At our research site in New Mexico, detailed knowledge about the ecology of lagomorph and mesocarnivore populations could be critical to managing rates of one-seed juniper encroachment into and recolonization of short grass prairie rangeland.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f13101693/s1, Figure S1: Study area with cone tree (pink diamonds), non-cone tree (purple diamonds), transition zone (teal diamonds), and open grassland plot (green diamonds) locations; Table S1: Mean significant difference of log seed counts based on post hoc test-TukeyHSD of an interaction model within habitat and seed disperser factors.

Author Contributions

Conceptualization, D.S., A.C.G. and A.F.C.; methodology, D.S., A.C.G., A.F.C. and A.M.F.; software, P.S.; formal analysis, P.S. and R.L.S.; investigation, D.S.; resources, D.S., A.C.G. and A.F.C.; data curation, D.S.; writing—original draft preparation, D.S.; writing—review and editing, D.S., A.F.C., A.C.G., A.M.F., D.S.C. and M.M.M.; visualization, M.M.M.; supervision, A.C.G. and A.F.C.; funding acquisition, A.C.G., D.S. and A.F.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was partially funded by the USDA National Institute of Food and Agriculture, Hatch project 1000985 (A. Cibils), the New Mexico State University Agricultural Experiment Station (A. Ganguli), The Range Improvement Task Force at New Mexico State University (D. Cram), Arkansas Forest Resource Center, University of Arkansas at Monticello (Saud), University of Montana, College of Forestry and Conservation (Faist).

Data Availability Statement

Data is available upon request to the first author.

Acknowledgments

Housing for technicians was provided by the New Mexico State University Corona Range and Livestock Research Center and the Southwest Center for Rangeland Sustainability. Superintendent Shad H. Cox and senior research assistant Richard L. Dunlap provided invaluable logistical support to the project during field work. We are indebted to many field technicians for field work, especially long-term technicians Elizabeth M. Butler, Alyssa I. Fish, Jonathan L. Mark, and Andrew P. Stricklan. We are grateful for helpful suggestions to improve the manuscript by two independent reviewers.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Archer, S.R.; Andersen, E.M.; Predick, K.I.; Schwinning, S.; Steidl, R.J.; Woods, S.R. Woody plant encroachment: Causes and consequences. In Rangeland Systems; Briske, D., Ed.; Springer: College Station, TX, USA, 2017; pp. 25–84. [Google Scholar]
  2. Stephens, G.J.; Johnston, D.B.; Jonas, J.L.; Paschke, M.W. Understory Responses to Mechanical Treatment of Pinyon-Juniper in Northwestern Colorado. Rangel. Ecol. Manag. 2016, 69, 351–359. [Google Scholar] [CrossRef] [Green Version]
  3. Wilcox, B.P.; Fuhlendorf, S.D.; Walker, J.W.; Twidwell, D.; Ben Wu, X.; E Goodman, L.; Treadwell, M.; Birt, A. Saving imperiled grassland biomes by recoupling fire and grazing: A case study from the Great Plains. Front. Ecol. Environ. 2021, 20, 179–186. [Google Scholar] [CrossRef]
  4. Berg, M.; Sorice, M.G.; Wilcox, B.P.; Angerer, J.P.; Rhodes, E.C.; Fox, W.E. Demographic Changes Drive Woody Plant Cover Trends—An Example from the Great Plains. Rangel. Ecol. Manag. 2015, 68, 315–321. [Google Scholar] [CrossRef]
  5. Briske, D.D.; A Joyce, L.; Polley, H.W.; Brown, J.R.; Wolter, K.; A Morgan, J.; A McCarl, B.; Bailey, D.W. Climate-change adaptation on rangelands: Linking regional exposure with diverse adaptive capacity. Front. Ecol. Environ. 2015, 13, 249–256. [Google Scholar] [CrossRef] [Green Version]
  6. Van Auken, O. Causes and consequences of woody plant encroachment into western North American grasslands. J. Environ. Manag. 2009, 90, 2931–2942. [Google Scholar] [CrossRef] [PubMed]
  7. Adams, R.P. Junipers of the World: The genus Juniperus, 4th ed.; Trafford Publishing: Bloomington, IN, USA, 2014. [Google Scholar]
  8. Johnsen, T.N. One-Seed Juniper Invasion of Northern Arizona Grasslands. Ecol. Monogr. 1962, 32, 187–207. [Google Scholar] [CrossRef]
  9. Pieper, R.D. Overstory-understory relations in pinyon-juniper woodlands in New Mexico. J. Range Manage. 1990, 43, 413–415. [Google Scholar] [CrossRef]
  10. Rosenstock, S.S.; Van Riper, C. Breeding Bird Responses to Juniper Woodland Expansion. Rangel. Ecol. Manag. 2001, 54, 226. [Google Scholar] [CrossRef] [Green Version]
  11. Jacobs, B.F.; Gatewood, R.G. Proceedings: Ecology and Management of Pinyon-Juniper Communities within the Interior West, Provo, UT, USA, 15–18 September 1997; Monsen, S.B., Stevens, R., Eds.; Proc. RMRS-P-9; Department of Agriculture, Forest Service, Rocky Mountain Research Station: Ogden, UT, USA, 1999.
  12. Miller, R.F.; Svejcar, T.J.; Rose, J.A. Impacts of Western Juniper on Plant Community Composition and Structure. Rangel. Ecol. Manag. 2000, 53, 574. [Google Scholar] [CrossRef]
  13. Schott, M.R.; Pieper, R.D. Influence of Canopy Characteristics of One-Seed Juniper on Understory Grasses. Rangel. Ecol. Manag. 1985, 38, 328. [Google Scholar] [CrossRef]
  14. Roundy, B.A.; Young, K.; Cline, N.; Hulet, A.; Miller, R.E.; Tausch, R.J.; Chambers, J.C.; Rau, B. Pinion-juniper reduction increases soil water availability of the resource growth pool. Rangel. Ecol. Manage. 2014, 67, 495–505. [Google Scholar] [CrossRef] [Green Version]
  15. Coppedge, B.R.; Engle, D.M.; Masters, R.E.; Gregory, M.S. Avian response to landscape change in fragmented southern great plains grasslands. Ecol. Applications. 2001, 11, 47–59. [Google Scholar] [CrossRef]
  16. Coppedge, B.R. Predicting juniper encroachment and CRP effects on avian community dynamics in southern nixed-grass prairie, USA. Biol. Conserv. 2004, 115, 431–441. [Google Scholar] [CrossRef]
  17. Coates, P.S.; Prochazka, B.G.; Ricca, M.A.; Gustafson, K.B.; Ziegler, P.; Casazza, M.L. Pinyon and juniper encroachment into sagebrush ecosystems impacts distribution and survival of greater sage-grouse. Rangel. Ecol. Manage. 2017, 70, 25–38. [Google Scholar] [CrossRef] [Green Version]
  18. Romme, W.; Allen, J.D.; Bailey, W.L.; Baker, B.T.; Bestelmeyer, P.M.; Brown, K.S.; Eisenhart, M.L.; Floyd-Hanna, D.W.; Huffman, B.F.; Jacobs, R.F.; et al. Historical and modern disturbance regimes, stand structure, and landscape dynamics in pinyon-juniper vegetation of the western United States. Rangel. Ecol. Manag. 2009, 62, 203–222. [Google Scholar] [CrossRef] [Green Version]
  19. Stevens, B.F.; Erasmus, N.; Archibald, S.; Bond, W.J. Woody encroachment of 70 years in savannahs: Overgrazing, global change or extinction aftershock? Philos. Trans. R Soc. Lond B Biol. Sci. 2016, 371, 20150437. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. Allred, B.W.; Fuhlendorf, S.D.; Smeins, F.E.; Taylor, C.A. Herbivore species and grazing intensity regulate community composition and an encroaching woody plant in semi-arid rangeland. Basic Appl. Ecology 2012, 13, 149–158. [Google Scholar] [CrossRef]
  21. Ganguli, A.C.; Engle, D.M.; Mayer, P.M.; Salo, L.F. Influence of resource availability on Juniperus virginiana expansion in a forest-prairie ecotone. Ecosphere 2016, 7, e01433. [Google Scholar] [CrossRef] [Green Version]
  22. Escribano-Avila, G.; Calviono-Cancela, M.; Pias, B.; Virgos, E.; Valladares, F.; Escudero, A. Diverse guilds provide complementary dispersal services in a woodland expansion process after land abandonment. J. Appl. Ecol. 2014, 51, 1701–1711. [Google Scholar] [CrossRef] [Green Version]
  23. Rumeu, B.; Elias, R.B.; Padilla, D.P. Differential seed dispersal systems of endemic junipers in two oceanic Macaronesian archipelagos: The influence of biogeographic and biological characteristics. Plant Ecology 2011, 212, 911–921. [Google Scholar] [CrossRef]
  24. Lezama-Delgado, E.; Sainos-Paredes, P.; López-Portillo, J.; Angeles, G.; Golubovc, J.; Martínez, A.J. Association of Juniperus deppeana (Cupressaceae: Pinales) seeds with Mexican cottontail rabbit (Sylvilagus cunicularius; Leporidae: Lagomorpha) latrines. J. Nat. Hist. 2016, 50, 2547–2555. [Google Scholar] [CrossRef]
  25. Salomonson, M.G. Adaptations for animal dispersal of one-seed juniper seeds. Oecologica 1978, 32, 333–339. [Google Scholar] [CrossRef] [PubMed]
  26. White, C.G.; Flinders, J.T.; Cates, R.G.; Blackwell, B.H.; Smith, H.D. Dietary use of Utah juniper berries by gray fox in eastern Utah. In Proceedings of the Ecology and Management of Pinyon-Juniper Communities within the Interior West: RMRS-P-9; Monson, S.B., Stevens, R., Eds.; Dept. of Agriculture, Forest Service, Rocky Mountain Research Station: Ogden, UT, USA, 1999. [Google Scholar]
  27. Longland, W.S.; Dimitri, L.A. Are western juniper seeds dispersed through diplochory? Northwest Sci. 2016, 90, 235–243. [Google Scholar] [CrossRef]
  28. Dimitri, L.A.; Longland, W.S. Distribution of western juniper seeds across an ecotone and implications for dispersal. West. North Amer. Nat. 2017, 77, 212–222. [Google Scholar] [CrossRef]
  29. Chavez-Ramirez, F.; Slack, R.D. Carnivore Fruit-Use and Seed Dispersal of Two Selected Plant Species of the Edwards Plateau, Texas. Southwest. Nat. 1993, 38, 141. [Google Scholar] [CrossRef]
  30. Escribano-Ávila, G.; Pías, B.; Sanz-Pérez, V.; Virgós, E.; Escudero, A.; Valladares, F. Spanish juniper gain expansion opportunities by counting on a functionally diverse dispersal assemblage community. Ecol. Evol. 2013, 3, 3751–3763. [Google Scholar] [CrossRef] [Green Version]
  31. García-Cervigón, A.I.; Velázquez, E.; Wiegand, T.; Escudero, A.; Olano, J.M. Colonization in Mediterranean old-fields: The role of dispersal and plant-plant interactions. J. Veg. Sci. 2016, 28, 627–638. [Google Scholar] [CrossRef]
  32. Jordano, P.; García, C.; Godoy, J.A.; García-Castaño, L.L. Differential contribution of frugivores to complex seed dispersal patterns. PNAS 2007, 104, 3278–3282. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Traveset, A.; Verdu, M. A meta-analysis of the effect of gut treatment on seed germination. In Seed Dispersal and Frugivory: Ecology, Evolution and Conservation; Silva, W.R., Galetti, M., Eds.; CAB International: New York, NY, USA, 2002; pp. 339–350. [Google Scholar]
  34. Strand, E.K.; Robinson, A.P.; Bunting, S.C. Spatial patterns on the sagebrush steppe/Western juniper ecotone. Plant Ecol. 2007, 190, 159–173. [Google Scholar] [CrossRef]
  35. Holthuijzen, A.M.; Sharik, T.L. The avian seed dispersal of eastern red cedar. Can. J. Bot. 1985, 63, 1508–1515. [Google Scholar] [CrossRef]
  36. Herrera, C.M. Frugivory and seed dispersal by carnivorous mammals, and associated fruit characteristics, in undisturbed Mediterranean habitats. Oikos 1989, 55, 250–262. [Google Scholar] [CrossRef] [Green Version]
  37. NOAA, West. Reg. Climate Center. Available online: https://wrcc.dri.edu/Climate/west_coop_summaries.php (accessed on 17 November 2018).
  38. Forbes, A.C.; Allred, K.W. A field guide to the flora of New Mexico State University’s Corona Range and Livestock Research Center. NMSU Ag. Expt. Stn. Res. Rep. 2001, 745, 61. [Google Scholar]
  39. Santos, T.; Tellería, J.L.; Virgós, E. Dispersal of Spanish juniper Juniperus thurifera by birds and mammals in a fragmented landscape. Ecography 1999, 22, 193–204. [Google Scholar] [CrossRef]
  40. Tellería, J.L.; Carrascal, L.M.; Santos, T. Species abundance and migratory status affects large-scale fruit tracking in thrushes (Turdus spp.). J. Ornithol. 2014, 155, 157–164. [Google Scholar] [CrossRef]
  41. Jordano, P. Geographical ecology and variation of plant-seed disperser interactions: Southern Spanish junipers and frugivorous thrushes. In Vegetatio 107/108, Frugivory and Seed Dispersal: Ecological and Evolutionary Aspects; Fleming, T.H., Estrada, A., Eds.; Kluwer Academic Publishers: Dordrecht, Belgium, 1993; pp. 85–104. [Google Scholar]
  42. Elbroch, M. Mammal Tracks & Sign: A Guide to North American Species, 1st ed.; Stackpole Books: Mechanicsburg, PA, USA, 2003; 780p. [Google Scholar]
  43. Costello, C.M.; Jones, D.E.; Inman, R.M.; Inman, K.H.; Thompson, B.C.; Quigley, H.B. Relationship of variable mast production to American black bear reproductive parameters in New Mexico. Ursus 2003, 14, 1–16. [Google Scholar]
  44. R Core Team. 2017. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available online: https://www.R-project.org/ (accessed on 12 February 2019).
  45. Salomonson, M.G.; Balda, R.P. Winter territoriality of Townsend’s Solitaires (Myadestes townsendi) in a pinon-juniper-ponderosa pine ecotone. Condor 1977, 79, 148–161. [Google Scholar] [CrossRef]
  46. Holthuijzen, A.M.; Sharik, T.L. The red cedar (Juniperus virginiana L.) seed shadow along a fenceline. Amer. Mid. Nat. 1985, 113, 200–202. [Google Scholar] [CrossRef]
  47. Stricklan, D.; Saud, P.; Cibils, A.F.; Steiner, R.L.; Cram, D.S.; Young, K.; Faist, A.M. Germination of one-seed juniper seeds distributed by different frugivore groups. Rangel. Ecol. Manage. 2020, 73, 433–440. [Google Scholar] [CrossRef]
  48. Schupp, E.W.; Gomez, J.M.; Jimenez, J.E.; Fuentes, M. Dispersal of Juniperus occidentalis (western juniper) seeds by frugivorous mammals on Juniper Mountain in southeastern Oregon. Great Basin Nat. 1997, 57, 74–78. [Google Scholar]
  49. Perea, R.; Delibes, M.; Polko, M.; Suárez-Esteban, A.; Fedriani, J.M. Context-dependent fruit–frugivore interactions: Partner identities and spatio-temporal variations. Oikos 2013, 122, 943–951. [Google Scholar] [CrossRef] [Green Version]
  50. Schupp, E.W.; Heaton, H.J.; Gomez, J.M. Lagomorphs and the dispersal of seeds into communities dominated by exotic annual weeds. Great Basin Nat. 1997, 57, 253–258. [Google Scholar]
  51. Ilse, L.M.; Hellgren, E.C. Demographic and behavioral characteristics of North American porcupines (Erethizon dorsatum) in Pinyon-Juniper Woodlands of Texas. Amer. Mid. Nat. 2001, 146, 329–338. [Google Scholar] [CrossRef]
  52. Stricklan, D.; Flinders, J.T.; Cates, R.G. Factors affecting selection of winter food and roosting resources by porcupines in Utah. 1995. Great Basin Nat. 1995, 55, 29–36. [Google Scholar]
  53. Sweitzer, R.E. Predation or starvation: Consequences of foraging decisions by porcupines (Erethizon dorsatum). J. Mamm. 1996, 77, 1068–1077. [Google Scholar] [CrossRef] [Green Version]
  54. Schupp, E.W. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 1993, 107/108, 15–29. [Google Scholar] [CrossRef]
  55. Farris, E.; Canopoli, L.; Cucca, E.; Landi, S.; Maccioni, A.; Filigheddu, R. Foxes provide a direct dispersal service to Phoenician junipers in Mediterranean costal environments: Ecological and evolutionary implications. Plant Ecol. Evol. 2017, 150, 117–128. [Google Scholar] [CrossRef]
Forests 13 01693 g001 550
Figure 1. Sample plot configuration showing four, one-meter-wide, 25-m-long transects located in the cardinal directions. Bird, lagomorph, mesocarnivore, and porcupine pellets and scats were collected within the transects. Location beneath the outside of the juniper canopy was noted for frugivore-deposited pellets or scats in woodland plots (cone tree and non-cone tree habitats). The entire sample plot was searched for mesocarnivore scats.
Figure 1. Sample plot configuration showing four, one-meter-wide, 25-m-long transects located in the cardinal directions. Bird, lagomorph, mesocarnivore, and porcupine pellets and scats were collected within the transects. Location beneath the outside of the juniper canopy was noted for frugivore-deposited pellets or scats in woodland plots (cone tree and non-cone tree habitats). The entire sample plot was searched for mesocarnivore scats.
Forests 13 01693 g001
Forests 13 01693 g002 550
Figure 2. Mean values and standard deviation of the mean (log-transformed) of seeds per hectare based on habitat classifications and seed disperser groups. Letters indicate significant differences (p ≤ 0.05) among groups.
Figure 2. Mean values and standard deviation of the mean (log-transformed) of seeds per hectare based on habitat classifications and seed disperser groups. Letters indicate significant differences (p ≤ 0.05) among groups.
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Forests 13 01693 g003 550
Figure 3. Distribution of juniper seed counts (log-transformed) per hectare based on habitat classifications and seed disperser groups in (a) 2017 and in (b) 2018.
Figure 3. Distribution of juniper seed counts (log-transformed) per hectare based on habitat classifications and seed disperser groups in (a) 2017 and in (b) 2018.
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Forests 13 01693 g004 550
Figure 4. Predicted mean log value of seed/ha deposited by seed disperser groups in four habitats based on two-way ANOVA model.
Figure 4. Predicted mean log value of seed/ha deposited by seed disperser groups in four habitats based on two-way ANOVA model.
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Table
Table 1. Mean and SEM, median, maximum seeds/ha, and percent of plots present for one-seed juniper seeds by seed disperser group (bird, lagomorph, mesocarnivore, and porcupine) in each habitat category for years 2017–2018 combined, except for transition zone which was sampled in 2018 only. When only one plot in a habitat category had seeds, the SEM is reported as not applicable.
Table 1. Mean and SEM, median, maximum seeds/ha, and percent of plots present for one-seed juniper seeds by seed disperser group (bird, lagomorph, mesocarnivore, and porcupine) in each habitat category for years 2017–2018 combined, except for transition zone which was sampled in 2018 only. When only one plot in a habitat category had seeds, the SEM is reported as not applicable.
HabitatMean & SEMMedianMaximum% Presence
Cone Trees (under canopy) n = 60
Bird117,989 ± 19,38771,474844,473100
Lagomorph36,146 ± 754313,851291,77482
Mesocarnivore107,200 ± 65,97703,922,53527
Porcupine861 ± 391019,93415
Cone Trees (beyond canopy) n = 60
Bird5338 ± 818319326,46493
Lagomorph10,839 ± 25432543119,06893
Mesocarnivore52,257 ± 10,03120,503375,77763
Porcupine52 ± 330181808
Non-Cone Tree (under canopy) n = 60
Bird896 ± 312011,62019
Lagomorph5641 ± 1044231238,71064
Mesocarnivore14,218 ± 85640415,12905
Porcupine3029 ± 30290181,73402
Non-Cone Tree (beyond canopy) n = 60
Bird154 ± 990579812
Lagomorph1983 ± 49769022,27787
Mesocarnivore10,054 ± 30050117,65425
Porcupine39 ± 240123405
Transition Zone n = 32 *
Bird128 ± 500110025
Lagomorph1260 ± 6055018,60050
Mesocarnivore1759 ± 947023,20019
Porcupine13 ± 12040009
Grassland Open Areas n = 60
Bird2 ± NA010002
Lagomorph90 ± 390200018
Mesocarnivore3325 ± 1836082,10008
Porcupine23 ± NA0140002
* Number of plots sampled in habitat categories was 28-32 each year.
Table
Table 2. Frequency of bird (B), lagomorph (L), mesocarnivore (M) and porcupine (P) scat/pellet presence in plots (n = 27 to 33) located in four habitat types at our research site. Chi-square was used to test the association between seed disperser and habitat type.
Table 2. Frequency of bird (B), lagomorph (L), mesocarnivore (M) and porcupine (P) scat/pellet presence in plots (n = 27 to 33) located in four habitat types at our research site. Chi-square was used to test the association between seed disperser and habitat type.
HabitatScat/Pellet Presence (% Plots)Frugivore Tests aGeneral Assoc. b
BLMPChi2pCMH Statisticp
2017
Cone trees92.688.985.27.462.7<0.01
Non-cone trees15.290.915.23.075.1<0.01
Open grassland0.026.70.90.021.5<0.01
2018
Cone trees90.996.945.59.170.8<0.01
Non-cone tree7.481.537.07.444.7<0.01
Transition zone c20.046.713.33.318.7<0.01
Open grassland3.310.010.03.32.10.54
Overall Frugivore by Habitat relationship d212.4<0.01
a Test of association for seed disperser presence/absence frequency controlling for habitat type and year; b Cochran–Mantel–Haenszel Test of General Association; c Transition zone was not sampled in 2017; d Overall test of association of frugivore presence/absence frequency.
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Stricklan, D.; Cibils, A.F.; Saud, P.; Steiner, R.L.; McIntosh, M.M.; Ganguli, A.C.; Cram, D.S.; Faist, A.M. Dispersal Patterns of One-Seed Juniper Seeds Contained in Mammal Scats and Bird Pellets. Forests 2022, 13, 1693. https://doi.org/10.3390/f13101693

AMA Style

Stricklan D, Cibils AF, Saud P, Steiner RL, McIntosh MM, Ganguli AC, Cram DS, Faist AM. Dispersal Patterns of One-Seed Juniper Seeds Contained in Mammal Scats and Bird Pellets. Forests. 2022; 13(10):1693. https://doi.org/10.3390/f13101693

Chicago/Turabian Style

Stricklan, Dave, Andrés F. Cibils, Pradip Saud, Robert L. Steiner, Matthew M. McIntosh, Amy C. Ganguli, Douglas S. Cram, and Akasha M. Faist. 2022. "Dispersal Patterns of One-Seed Juniper Seeds Contained in Mammal Scats and Bird Pellets" Forests 13, no. 10: 1693. https://doi.org/10.3390/f13101693

APA Style

Stricklan, D., Cibils, A. F., Saud, P., Steiner, R. L., McIntosh, M. M., Ganguli, A. C., Cram, D. S., & Faist, A. M. (2022). Dispersal Patterns of One-Seed Juniper Seeds Contained in Mammal Scats and Bird Pellets. Forests, 13(10), 1693. https://doi.org/10.3390/f13101693

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