2012 NORTHEASTERN NATURALIST 19(1):43–48
The Influence of Nearest Seed Neighbors on Seed Removal
in Deciduous Forests
Jaclyn L. Schnurr*,1, Richard S. Ostfeld2, and Charles D. Canham2
Abstract - In the temperate deciduous forests of the northeastern United States, the
majority of the dominant tree species disperse their seeds during the fall, causing a
heterogeneous mixture of seeds to be present at a specific location at one time. Because
these seeds vary in size and palatability to small mammals, some seed species,
such as Quercus acorns, may alter the risk of removal of neighboring, less preferred
species. The presence of a neighboring seed could attract seed predators, elevating the
risk that a neighboring seed will be removed (apparent competition), or it could divert
the attention of seed predators away from a neighboring seed (apparent mutualism).
We evaluated the effects of nearest seed neighbors on the survival of 5 different tree
species. Using logistic regression we determined whether the species or abundance of
nearest neighbors caused changes in the risk of removal. Contrary to our expectations,
we did not find any affect of neighboring seed species on the removal rates of other
seeds, indicating that risk of removal of naturally occurring seeds, separated by at
least 10 cm, is independent.
Introduction
The temperate deciduous forests of the northeastern United States are
comprised of a heterogeneous mixture of canopy tree species, many of which
disperse seeds during the fall of each year. This diversity causes spatial and
temporal variation in the abundance and distribution of seed types present at
a particular location on the forest floor (Ribbens et al. 1994, Schnurr et al.
2002). From the perspective of the tree species, it may be a favorable strategy
to disperse seeds when others are as well, to potentially satiate any seed predators
in the area (Koenig et al. 1994, Lalonde and Roitberg 1992, Shibata et
al. 1998, Silvertown 1980). However, tree species produce seeds that are not
nutritionally equivalent to the suite of seed predators found in these forests
(J.L. Schnurr, unpubl. data). Therefore, seed predators may have preferences
for certain seed types over others, which may increase, or decrease, the risk of
removal of neighboring seeds.
When survival of a specific seed type is influenced by the identity of its
neighbors and mediated by the preference of its predator, then short-term apparent
competition or apparent mutualism may be occurring (Holt and Kotler 1987;
Veech 2000, 2001). Apparent competition is an indirect effect that occurs when
species-specific seed survival decreases due to the identity of the neighboring
1Wells College, 170 Main St., Aurora, NY 13026. 2Cary Institute of Ecosystem Studies,
2801 Sharon Turnpike; PO Box AB, Millbrook, NY 12545. *Corresponding author -
jschnurr@wells.edu.
44 Northeastern Naturalist Vol. 19, No. 1
seed, while apparent mutualism occurs when species-specific seed survival increases
due to the other seed being preferred by the predator (Veech 2000). Veech
(2000) found support for apparent competition among seeds of desert annuals,
especially with those species that were preferred by their seed predators (see also
Caccia et al. 2006). However, in another desert system, Garb et al. (2000) found
support for short-term apparent competition that only occurred in patches with
highly variable initial seed densities.
Much research has been conducted on the effects of seed predation on survival
of tree seeds in temperate deciduous forests (Schnurr et al. 2002, 2004), and
many of these studies have indicated that acorns are a preferred food of the small
mammals commonly found in these forests (Elkinton et al. 1996; McCracken et
al. 1999; Ostfeld et. al 1996; Schnurr et al. 2002, 2004; Wolff 1996). Since seed
rain is heterogeneous, seed species are mixed on the forest floor, such that the
proximity of a fallen seed to an acorn may cause apparent competition or apparent
mutualism to occur. Although a common method of measuring seed removal
is to use a quadrat with seed species of varying identities found next to each
other (e.g., Schnurr et al. 2002, 2004), there has been no research addressing the
influences these seeds may have on each other. If apparent competition, or apparent
mutualism, is occurring, measuring these processes would help predict seed
survival and seedling recruitment in these communities.
In this study, we asked: Does the identity of the nearest seed neighbor influence
the chance of a particular seed being removed? We tested the hypothesis that
proximity to one or more seeds of any species has an effect on the risk of removal
of other seed species. We expected to find that only the proximity to Quercus rubra
L. (Northern Red Oak) acorns would influence survival of the other seeds.
Methods
This study was conducted at the 2500-ha privately owned Great Mountain
Forest (GMF), in Litchfield County, CT (41°57'N, 73°15'W). The major tree
species there are Fagus grandifolia Ehrh. (American Beech), Tsuga canadensis
(L.) Carr. (Eastern Hemlock), Acer saccharum Marsh. (Sugar Maple), Acer
rubrum L. (Red Maple), Pinus strobus L. (White Pine), Red Oak, Prunus serotina
Ehrh. (Black Cherry), and Fraxinus americana L. (White Ash), and the
major small-mammal seed predators in this area are Peromyscus maniculatus
(Wagner) (Deer Mouse), P. leucopus (Rafinesque) (White-footed Mouse),
Myodes gapperi (Vigors) (Red-backed Vole), and Tamias striatus (L.) (Eastern
Chipmunk).
During the fall of 1994, we established fifty-two 1- x 1-m quadrats at 2 mixedcanopy
sites that were separated by approximately 2 km. Within each quadrat,
we randomly placed 1 seed (technically fruit propagules containing the seed) of
5 different species every 10 cm on a grid—which gave us varying sample sizes
for the number and identities of neighbors for each seed. The species used were
Red Oak (average seed weight 2.6 g), Black Cherry (36.4 mg dry wt), Sugar
2012 J.L. Schnurr, R.S. Ostfeld, and C.D. Canham 45
Maple (27.4 mg), White Ash (≈16 mg), and Red Maple (9.3 mg). The propagules
were placed directly on the ground and marked with a wooden coffee stirrer. We
returned after 1 week and recorded their fate.
The numbers of neighbors within 10 cm of the focal seed and their identities
were calculated in every quadrat (maximum possible n = 8). We used
logistic regression to determine if seed status (live, dead) was influenced by
the numbers and species of nearest neighbors. If a seed was missing it was
considered “dead”.
Figure 1. The influence of Red Oak acorns on the average survival of A) Red Maple
seeds, B) Sugar Maple seeds, C) White Ash seeds, D) Black Cherry seeds, and E) Red
Oak acorns. Error bars are one standard error.
46 Northeastern Naturalist Vol. 19, No. 1
Results
Independent of the identity of the neighboring seed, Red Oak acorns were
most likely to be removed, but there was no significant effect of proximity and
density of acorns on the removal of any other seed species (Table 1, Fig. 1). Sugar
Maple seeds were the only species that showed a significantly higher removal
rate with conspecific neighbors (Table 1). There were no patterns of seed survival
based on numbers and identities of neighboring species (Table 1), and seed removal
rates were constant for each species, independent of the numbers and the
identities of a seed’s neighbors (Fig. 1).
Discussion
Our results do not support our hypothesis: risk of seed removal was independent
of the identity of neighboring seeds at a local scale. Red Oak acorns were
consistently found and removed, supporting the general research consensus that
Quercus is a preferred food of small-mammal seed predators in temperate forests
(Elkinton et al. 1996; McCracken et al. 1999; Ostfeld et. al 1996; Schnurr
et al. 2002, 2004; Wolff 1996). However, it appears that animals remove acorns
as they discover them and do not concentrate their foraging in the areas where
acorn density is higher. A confounding effect may occur due to the species of
small mammals that are removing the seed. Although the major seed predators
at GMF (White-footed Mice, Deer Mice, Red-backed Voles, and Eastern
Chipmunks) are all considered generalists, it is possible that these different
mammal species were differentially removing certain species of our seeds.
Schnurr et al. (2002) found that Peromyscus species preferred Red Oak acorns,
while Red-backed Voles appeared to prefer Red Maple samaras. If these species
are foraging independently within our quadrats, it may appear that there is
Table 1. Results of the logistic regression of seed survival (live, dead) of the focal seed species (Red
Oak, Black Cherry, Sugar Maple, White Ash, or Red Maple) found with conspecific or interspecific
neighbors. Significant P-value shown in bold.
Focal With neighbors of
seed species Red Oak Black Cherry Sugar Maple White Ash Red Maple
Red Oak t = 0.174, t = 1.003, t = -1.318, t = -0.682, t = -0.35,
P = 0.862 P = 0.316 P = 0.188 P = 0.495 P = 0.726
Black Cherry t = -1.246, t = 0.035, t = 0.211, t = -0.111, t = 1.648,
P = 0.213 P = 0.726 P = 0.833 P = 0.912 P = 0.099
Sugar Maple t = -1.028, t = 0.826, t = 2.704, t = -0.567, t = -1.242,
P = 0.304 P = 0.409 P = 0.007 P = 0.571 P = 0.214
White Ash t = 0.699, t = -1.661, t = 0.437, T = -0.763, t = 0.45,
P = 0.484 P = 0.097 P = 0.662 P = 0.446 P = 0.653
Red Maple t = 0.626, t = 1.897, t = -1.726, t = -1.366, t = -1.326,
P = 0.532 P = 0.058 P = 0.084 P = 0.172 P = 0.185
2012 J.L. Schnurr, R.S. Ostfeld, and C.D. Canham 47
no effect of neighboring seeds on focal seed removal, while the real effect may
be caused by the mammal species removing the seeds: White-footed and Deer
Mice may be preferentially removing acorns while ignoring maple seeds, while
Red-backed Voles might be removing maple seeds. However, these differing
foraging strategies do not affect the eventual survival and germination of seeds.
Much current research is focused on understanding the importance of indirect
effects in the maintenance of temperate forests (Ostfeld and Keesing 2000,
Ostfeld et al. 1996). This study demonstrates that the patterns and processes associated
with seedling recruitment can be understood through seed dispersal and
survival alone since seed survival is independent of neighboring seeds, at least
simplifying one aspect of community dynamics.
Acknowledgments
The authors wish to acknowledge the field help of Erika Latty and Sue Bookhout. The
manuscript benefited by comments from Brian Hough and two anonymous reviewers.
Literature Cited
Caccia, F.D., E.J. Chaneton, and T. Kitzberger. 2006. Trophic and non-trophic pathways
mediate apparent competition through post-dispersal seed predation in a Patagonian
mixed forest. Oikos 113:469–480.
Elkinton, J.S., W.M. Healey, J.P. Buonaccorsi, G.H. Boettner, A.M. Hazzard, H.R. Smith
and A.M. Liebold. 1996. Interactions among Gypsy Moths, White-footed Mice, and
acorns. Ecology 77:2332–2342.
Garb, J., B.P. Kotler, and J.S. Brown. 2000. Foraging and community consequences of
seed size for coexisting Negev Desert granivores. Oikos 88:291–300.
Holt, R.D., and B.P. Kotler. 1987. Short-term apparent competition. American Naturalist
130:412–430.
Koenig, W.D., R.L. Mumme, W.J. Carmen, and M.T. Stanback. 1994. Acorn production
by oaks in central coastal California: Variation within and among years. Ecology
75:99–109.
Lalonde, R.G., and B.D. Roitberg. 1992. On the evolution of masting behavior in trees:
Predation or weather? American Naturalist 139:1293–1304.
McCracken, K.E., J.W. Witham, and M.L. Hinter, Jr. 1999. Relationships between seed
fall of three species and Peromyscus leucopus and Clethrionomys gapperi during 10
years in an oak-pine forest. Journal of Mammalogy 80:1288–1296.
Ostfeld, R.S., and F. Keesing. 2000. Pulsed resources and community dynamics of consumers
in terrestrial ecosystems. Trends in Ecology and Evolution 15:232–237.
Ostfeld, R.S., C.G. Jones, and J.O. Wolff. 1996. Of mice and mast: Ecological connections
in eastern deciduous forests. BioScience 46:323–330.
Ribbens, E., J.A. Silander, Jr., and S.W. Pacala. 1994. Recruitment in forests: Calibrating
models to predict patterns of tree seedling dispersal. Ecology 75:1794–1804.
Schnurr, J.L., R.S. Ostfeld, and C.D. Canham. 2002. Direct and indirect effects of masting
on rodent populations and tree seed survival. Oikos 96(3):402–410.
Schnurr, J.L., C.D. Canham, R.S. Ostfeld, and R.S. Inouye. 2004. Neighborhood analyses
of small-mammal abundance and activity: Impacts on tree seed predation and seedling
establishment. Ecology 85(3):741–755.
48 Northeastern Naturalist Vol. 19, No. 1
Shibata, M., H. Tanaka, and T. Nakashizuka. 1998. Causes and consequences of mast seed
production among four co-occurring Carpinus species in Japan. Ecology 79:54–64.
Silvertown, J.W. 1980. The evolutionary ecology of mast seeding in trees. Biological
Journal of the Linnean Society 14:235–250.
Veech, J.A. 2000. Predator-mediated interactions among the seeds of desert plants. Oecologia
124:402–407.
Veech, J.A. 2001. The foraging behavior of granivorous rodents and short-term apparent
competition among seeds. Behavioral ecology 12:467–474.
Wolff, J.O. 1996. Population fluctuations of mast-eating rodents are correlated with the
production of acorns. Journal of Mammalogy 77:850–856.