DOI: 10.5061/dryad.k6djh9wbk
title: Small mammal granivory as a biotic filter for tree establishment beyond elevation range boundaries

description: Trees often experience migration lags in their response to rapidly
 changing climate. Preferential granivory by nocturnal small mammals has
 the potential to create lags by reducing germination success beyond range
 edges. To determine how granivory may limit establishment of trees beyond
 their range margins, we conducted a seed choice experiment which offered
 seeds of five regionally dominant tree species to small mammals within
 distinct forest communities across a 400m elevational gradient on four
 mountains in the northeastern United States. Multinomial logistic mixed
 effects models were used to (a) quantify seed preference of each species
 across the elevational gradient and (b) assess relationships between seed
 preference and abiotic variables. A separate seed dispersal experiment was
 used to compare the probability of seed consumption versus seed caching.
 The low-elevation temperate tree species Fagus grandifolia and Acer
 saccharum had an equally high probability of granivory within and beyond
 their range margins (~40% and ~20%, respectively). Generally, seed
 preference was positively correlated with seed mass and nutrient content
 regardless of elevation. Our seed dispersal experiment revealed that seeds
 were 3× more likely to be consumed than cached, suggesting that small
 mammals can potentially decrease germination success. Overall, temperate
 tree species with either high seed mass or nutritional value may
 experience substantial granivory beyond their range margin, partially
 explaining the observed lag between tree dispersal and climate change.
 Thus, granivory is vital to consider when modeling future tree species
 distributions under various climate change scenarios.
description: <strong>Seed Selection Experiment</strong>
 Seeds of five regionally dominant tree species were offered in a
 cafeteria-style experiment in the fall of 2020 (mid-September through
 mid-October), coinciding with the timing of natural seed release and
 dispersal of our focal tree species (Burns and Honkala, 1990). The focal
 tree species included American beech (<em>Fagus</em>
 <em>grandifoila</em>), sugar maple (<em>Acer</em>
 <em>saccharum</em>), yellow birch (<em>Betula</em>
 <em>alleghaniensis</em>), balsam fir
 (<em>Abies</em> <em>balsamea</em>), and red spruce
 (<em>Picea</em> <em>rubens</em>). All seeds were
 purchased from either Sheffield’s Seed Company (Locke, NY) or F.W.
 Schumacher Seed Company (Sandwich, MA). Seed species were offered in equal
 amounts by mass (3 g per station) in order to standardize across species
 with various seed sizes (Boone & Mortelliti, 2019). Seeds were
 offered to mammals as they would naturally be found post-dispersal on the
 forest floor (conifer seeds removed from cones and sugar maple wings
 attached). At each seed selection station, five Petri
 dishes (6 cm diameter) were affixed to one wooden plank with Velcro strips
 (see Figure 2). The planks were fixed to the ground with two metal lawn
 stakes to ensure stability. We opted not to enclose each station with a
 wire cage. While a cage would fully ensure exclusion of any non-target
 species (i.e., birds, large mammals), it also has the potential to
 discourage visitation by target species (Mortelliti, personal
 communication). We believed non-target visitation to seed stations would
 be low given the dense understory of the sites. In each Petri dish, seeds
 of one species were placed. Species were randomly assigned to a dish at
 each site. All stations were checked daily for damage, cleaned of debris,
 and removed after four nights. Seeds were not replaced after each daily
 check. At noon on the last day of deployment, any remaining seeds were
 collected in order to compare the final mass of seeds remaining for each
 species. Stations were then moved and redeployed on each of the remaining
 mountains for a total of 60 deployed stations at 12 distinct sites
 (elevations) across 16 total days. Small mammal seed
 choice was determined using infrared game cameras (see SI for examples of
 videos). At each station, a Stealth Cam G45NG Pro camera was attached to a
 tree within 1 m of the dishes. The camera was angled down between 45 and
 60 degrees to provide a full view of the station. All cameras were set up
 to record 30 s videos at 1080 HP, and with a 5 s trigger delay between
 videos when triggered using a near-field setting. In addition to seed
 choice and mammal species identification and behavior, the cameras were
 also used to record temperature, time, and the presence of rain at the
 time of each seed selection event. Sample videos were taken in the field
 prior to full deployment in order to ensure camera alignment with seed
 stations.  <strong>Seed Dispersal
 Experiment</strong> In each of the 12 sites, 3
 seed dispersal stations were established to track dispersal distances of
 seeds and their ultimate fate (consumption vs. caching). Only American
 beech seeds (beechnuts) were used in this experiment as retrieval tags
 could not be fixed to the smaller seed species. In order to track beechnut
 dispersal, a length (1 inch) of yellow yarn was attached to the side of
 each seed using solvent-free glue, as detailed by Kempter et al. (2018).
 At each seed dispersal station, 30 beechnuts were placed on a small wooden
 platform secured to the ground with lawn stakes. The seeds were left
 uncaged as in the seed selection experiment. An infrared camera was
 affixed to a nearby tree within 1 m of the station to allow for small
 mammal identification and quantification of behaviors at the time of seed
 removal. After three nights, a 2-hour, gridded systematic search up to 30
 meters away from the station was conducted for the tagged beechnuts. When
 one was found, we recorded distance away from the station, whether it was
 consumed or not, and the substrate in which the seed was found (either
 found on the surface of the forest floor, buried under the litter mat, or
 found on a tree). Across all sites, mean recovery rate for tagged
 beechnuts was 76%. <strong>Data Collection and
 Processing</strong> All 30-second field videos
 were processed to determine seed preferences by the resident small mammal
 community. Seed choice events were defined as the discrete times a small
 mammal handled a seed in any way. For each observed seed choice event ,we
 recorded time of day, the small mammal species, the seed species chosen,
 the number of seeds consumed per event, seed availability (the number of
 seeds remaining visible in the video) for all seed species, temperature,
 whether it was raining or not, illumination level, and handling time for
 the seed species during the event. The high quality of the video taken
 allowed us to count the number of seeds that were taken or consumed during
 each event. Running counts of remaining seed number at each station
 allowed for easy calculation of seed availability for each seed species.
 This number was divided by the total number of starting seeds to provide
 seed availability as a proportion. Time, rain, and temperature were taken
 directly from the video and camera metadata. As most seed predation events
 occurred during the night, illumination was characterized by the moon
 phase at the time of the event (new, crescent, quarter, gibbous, full, and
 a category for daytime light when events occurred during daylight hours).
 Local weather reports and the time and day of the seed predation event
 were used to determine the moon phase during each event. Seed handling
 time was measured with a stopwatch and was defined as the time between
 when a seed was first picked up and when it was fully consumed or dropped.
 Events where the endpoint could not be determined because the video ended
 before it occurred, or the mammal carried the seed outside the video frame
 were not used for handling time calculations. (see
 manuscript for more details)