Germination of One-Seed Juniper Seeds Distributed by Different Frugivore Groups

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Abstract

One-seed juniper (Juniperus monosperma [Englem.] Sarg.) encroachment into grassland habitats is facilitated by a diverse group of frugivores. To test seed germination after gut passage, we collected pellets or scats containing mature seeds from four frugivore groups: passerine (perching) birds, lagomorphs (hares and rabbits), mesocarnivores (coyotes and foxes), and porcupines. For comparison of germination success, we also evaluated seeds from intact, nondigested one-seed juniper cones. We conducted germination trials under three different scenarios: 1) imbibed bare seeds (a measure of potential germination); 2) seeds still encased within a frugivore deposited pellet or scat matrix or still in a nondigested cone; and 3) matrix-free seeds that had gone through the matrix germination trials and then were freed from the matrix (a simulation of seeds that become dislodged from scats or pellets). In the bare seed trials, germination was highest (70.8% ± 7.4%) for seeds digested by mesocarnivores and was 63.9% ± 5.7% for porcupines, which was higher (P < 0.05) than germination of seeds from bird pellets (33.3% ± 7.7%). Germination of seeds from all frugivores, including lagomorphs (51.4% ± 7.2%), was higher (P < 0.05) than for seeds encased in cones (9.7% ± 3.2%). The germination percentage of seeds still encased in frugivore pellets or scats was highest for birds (40.1 ± 4.2) and was significantly lower (P < 0.05) for other frugivores. Seeds freed from all frugivore deposition matrices showed a second pulse of germination activity, especially seeds from lagomorph pellets. Germination success differences can influence the nature of one-seed juniper woodland infill and encroachment into bordering grasslands, which can lead to loss of soil health, lower grass biomass production, and a diminishment of habitat quality for grassland-dependent wildlife species.

Introduction

Encroachment of woody species into grasslands is a common worldwide occurrence (Archer et al. 2017). While the drivers of woody species encroachment are complex (Romme et al., 2009, Stevens et al., 2016, Archer et al., 2017), in western North America juniper encroachment is generally thought to be associated with improper grazing by domestic livestock (Allred et al. 2012), reduced fire frequency (Van Auken, 2009, Ratajczak et al., 2016), and climate change (Volder et al. 2012). Encroachment by juniper into grassland and shrubland habitats is accompanied by a number of undesirable conditions including reduced understory herbaceous cover and an increase in bare soil (Jacobs and Gatewood, 1999, Miller et al., 2000, Schott and Pieper, 1985); decreased soil water availability to surrounding plants (Roundy et al., 2014a, Zou et al., 2014); reduction of grassland bird nesting habitat quality (Coppedge et al., 2001, Coppedge, 2004, Knick et al., 2014); and overall diminished habitat quality for domestic livestock and some grassland wildlife species (Horncastle et al., 2005, Bender et al., 2007, Coates et al., 2017). However, juniper woodlands do provide nesting habitat for many bird species (Francis et al. 2011), and reduction of juniper woodlands has variable impacts on wildlife depending on functional group (Bombaci and Pejchar 2016).

There has been considerable emphasis on the ecological (Miller et al., 2008, Roundy et al., 2014b, Young et al., 2015) and economic and logistical implications (Aldrich et al., 2005, Miller et al., 2014) of treatments to remove encroaching juniper species, but less research focus on how juniper seed is distributed (Dimitri and Longland 2017) and germinates on the landscape (Escribano-Ávila et al. 2013). Understanding germination potentials of seeds in frugivore pellets and scats is important to predicting encroachment patterns, as reports of germination of Juniperus spp. seeds that have passed through various frugivores vary (Johnsen, 1962, Salomonson, 1978, Rumeu et al., 2011, Escribano-Ávila et al., 2013). Frugivores can be responsible for the primary dispersal of Juniperus spp. seeds (García et al., 2010, García-Cervigón et al., 2017), although secondary seed movement (diplochory) by scatter-hoarding rodents can also play a major role in seed dispersal of some juniper species (Longland and Dimitri 2016). The pattern of seed dispersal of Juniperus spp. on the landscape can be linked to seed deposition patterns of primary frugivores and secondary dispersers (Fedriani and Wiegand, 2014, Escribano-Ávila et al., 2015, Dimitri et al., 2017). It is also likely that the role frugivores and diplochores (secondary seed consumers) play in seed dispersal is variable; for example, Dimitri et al. (2017) found little evidence of frugivores dispersing the relatively dry, leathery cones of Utah juniper (J. osteosperma) while White et al. (1999) found that cones from J. osteosperma dominated the diet of the gray fox (Urocyon cinereoargenteus) for much of the year. Further, different frugivore groups consume fruits and cones of woodland species at different levels (Horncastle et al., 2004, Escribano-Ávila et al., 2014) and the class of frugivore ingesting the seed can influence germination success and possibly seedling survival (Herrera, 1989, Perea et al., 2013).

To assess the potential role of frugivory in seed dispersal and woody plant encroachment, we investigated the germination of frugivore-digested one-seed juniper seeds. Specifically, we tested germination of 1) bare seeds (bare seed trials); 2) seeds encased in the pellets and scats of frugivores (matrix trials); and 3) bare seeds after they had gone ungerminated through the matrix trials (matrix-free trials). We hypothesized that there would be differential germination between seeds that had passed through the guts of different frugivores. We also hypothesized that the germination percentage of seeds encased in frugivore pellets would be lower than seeds that had been removed from pellets or scats (matrix free), due to a potential physical barrier limiting germination, but that germination within or out of the fecal matrix would remain dependent on the frugivore group.

Section snippets

Study Area

We collected seeds from random plots in two one-seed juniper woodland study areas in central New Mexico. The first study area was located in the Cibola National Forest, ≈13 km southwest of the town of Corona, and was approximately 85 km2 in size. The second study area was located in the New Mexico State University Corona Range and Livestock Research Center, ≈11 km east of Corona, and was 110 km2 in size. The sites were 25 km apart. They had a similar range in topography and elevation (from 1

Results

The mean germination of seeds per trial in the bare seed imbibed experiment was highest for mesocarnivores (70.8% ± 7.4%) (mean ± standard error), followed by porcupines (63.9% ± 5.7%), lagomorphs (51.4% ± 7.2%), and birds (33.3 ± 7.7 %), and lowest in nondigested cones (9.7% ± 3.2%). In the matrix-encased experiment, the germination of seeds per trial was highest for birds (40.1% ± 4.2%), followed by mesocarnivores (16.5% ± 3.4%) and lagomorphs (9.4% ± 4.2%), and was lowest for porcupines

Discussion

The factors that determine the effects of frugivory (endozoochory) on germination are complex and specific to the frugivore and seed. They include disinhibition (removal of fleshy pericarp tissue), imbibition (water uptake through the seed coat), presence and denaturing of seed coat germination inhibitors, residency time in the frugivore, possible physical damage by ingestion and mastication by the frugivore, and selectivity by the frugivore for seed size (Soltani et al. 2018). We found

Management Implications

During the past century, there has been a worldwide trend of woody species encroachment into grassland habitats (Sala and Maestre 2014), resulting in changes to grassland habitats and their attendant ecosystem services including livestock forage availability and production, carbon sequestration relations, fire frequencies, soil relations, hydrological potentials, and the constituents of plant and animal species assemblages, as well as species richness (Archer et al. 2017). Germination success

Acknowledgments

Housing for technicians was provided by the New Mexico State University (NMSU) 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 thank technicians Elizabeth M. Butler, Mariela Estrada, Alyssa I. Fish, Jonathan L. Mark, and Andrew P. Stricklan for field work and Dr. Soum Sanogo at NMSU for the use of

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