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Seasonal Foraging by Forest Mice Enhances Loss of Weed
Seeds from Crop–Field Edges
Sarah A. Abercrombie1, Jacob L. Berl1,2,*, Elizabeth A. Flaherty1, and
Robert K. Swihart1
Abstract - Native seed predators, such as mice (Peromyscus spp.) and ground beetles (Carabidae),
consume weed seeds and waste grain within agricultural fields and thus provide a
potentially important service to farmers. Most previous investigations of agricultural seed
predation services have focused on within-field factors that affect rates of seed removal and
consumption by field-resident seed predators. However, seasonal migrants from adjacent
non-crop habitats may also contribute to removal of weed seed, particularly along field
edges. We investigated whether rates of weed seed removal within fields increased during
summer crop growth when Peromyscus leucopus noveboracensis (White-Footed Mouse),
a ubiquitous forest-dwelling rodent in the eastern US, seasonally migrates into crop fields
from adjacent forested woodlots. We used exclosure experiments to quantify the relative
number of Setaria faberi (Giant Foxtail) seeds removed from seed trays by vertebrate and
invertebrate seed predators within 4 corn fields in central Indiana during 4 different stages of
crop growth (emergence [May], vegetative [July], reproductive [August], post-harvest [November]).
Seed-removal experiments were coupled with live trapping of rodents and pitfall
sampling of invertebrates to identify seed predators. Vertebrates (mice) contributed nearly
twice as much (~50%) to seed removal compared to invertebrates (~25%), irrespective of
season. Rates of invertebrate consumption differed among seasons but were not affected by
distance from forest–field edge. Rates of seed removal by mice significantly interacted with
season and distance from field edge, with higher rates of seed loss near forest–field edges
during July and August even though mouse abundance showed no strong association with
distance. Increased seed loss near (within 90 m) forest–field edges was presumably due to
consumption by seasonally field-resident White-footed Mice, which constituted the majority
(>70%) of mouse captures near field edges. Peromyscus maniculatus bairdii (Prairie
Deer Mouse) is a year-round resident in crop fields and most likely contributed to seed loss
nearer field interiors, where they comprised >90% of the rodents caught. Although non-crop
habitats are often overlooked as a source of seed predation services, our results indicate that
forest-dwelling White-footed Mice likely supplement rates of in-field predation on weed
seed. Future investigations of seed-predation services should consider the role of resident
and seasonally opportunistic seed predators in regulation of weed populations in crop fields.
Introduction
Identifying and evaluating multifunctional farmland management strategies
is important to reduce environmental impacts of pesticide use in high-input agricultural
systems. Recently, management to conserve farmland biodiversity has
1Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN
47907. 2Current address - Enforcement Bureau, Idaho Department of Fish and Game, Idaho
Falls, ID 83401. *Corresponding author - jacob.berl@idfg.idaho.gov.
Manuscript Editor: Michael Cramer
Natural History of Agricultural Landscapes
2017 Northeastern Naturalist 24(Special Issue 8):5–17
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focused on the facilitation of ecosystem services provided by natural invertebrate
and vertebrate communities, such as pollination and biological pest control
(Power 2010, Tscharntke et al. 2012). Consumption of weed seeds (hereafter,
weed-seed predation) is an ecosystem service provided by invertebrate and vertebrate
seed predators in many agricultural systems (Westerman et al. 2003).
Farmers go to great expense (herbicide) and effort (tillage) to reduce the negative
effects of weeds (Gibson et al. 2006). Seed predators can substantially reduce
(>50% removal; Westerman et al. 2003) post-dispersal weed-seed populations
in crop fields and reduce weed growth in following years (Blubaugh and Kaplan
2016, Davis et al. 2013, Zhang et al. 1997). Consequently, farmers can benefit
from natural weed-seed predation services and potentially reduce herbicide costs
by adjusting weed management strategies to account for natural seed removal (Liebman
and Gallandt 1997).
Most previous investigations of agricultural weed seed predation services have
focused on within-field factors affecting seed consumption. Factors such as tillage
regime, crop type, microhabitat, and seed preference are known to affect rates of
seed removal and consumption by field-resident invertebrate and vertebrate seed
predators (Cromar et al. 1999, Petit et al. 2014, Trichard et al. 2014, Westerman
et al. 2003). However, in many agricultural landscapes, seed predators likely use
crop fields only seasonally when within-field conditions (e.g., vegetation structure
provided by crop growth) promote use of these habitats. Unfortunately, little is
known about how populations of seed predators from non-crop habitats supplement
within-field rates of consumption.
In fragmented agricultural landscapes of the central and eastern United States,
many row-crop fields are bordered by or adjacent to forested non-crop habitat. The
2 dominant vertebrate seed predators in eastern corn belt landscapes, Peromyscus
maniculatus bairdii (Hoy and Kennicott) (Prairie Deer Mouse) and Peromyscus leucopus
noveboracensis (Fischer) (White-footed Mouse), differ in habitat preferences
but are seasonally sympatric in row-crop habitat (Kalmer et al. 1998). Prairie Deer
Mice typically select open habitats and are year-round residents in crop fields
(Clark and Young 1986, Wecker 1963, Whitaker 1966), whereas the White-footed
Mouse is predominantly a forest-dwelling species that selects habitat with dense
vegetative cover (Nupp and Swihart 1998). However, White-footed Mice are generalists
(Swihart et al. 2006) and show flexibility in habitat use, particularly when
food availability is high (Cummings and Vessey 1994, Morris and Davidson 2000).
It is unknown how seasonal differences in space use by Prairie Deer Mice and
White-footed Mice may influence weed seed predation in crop field s.
We hypothesized that invertebrate and vertebrate seed predators would differentially
contribute to seed removal in row-crop habitats. We also hypothesized
that White-footed Mice would migrate into fields from adjacent non-crop habitats
(e.g., herbaceous buffers or forested woodlots) and contribute to within-field loss
of weed seed. To gather evidence related to these hypotheses, we used seed predation
experiments to (1) compare the relative number of weed seeds removed by
vertebrates and invertebrates within row-crop agriculture and (2) investigate how
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seasonal differences in crop growth (emergence, vegetative, reproductive, and
post-harvest crop stages) and distance from non-crop habitat (forested woodlots)
affected seed removal rates. We predicted that (1) the relative contribution of invertebrates
and vertebrates to seed removal would vary as a function of season and
distance from forest–field edge due to differences in seasonal activity and space
use by seed predators, and (2) seasonal movements and opportunistic foraging by
White-footed Mice would increase seed removal rates near field edges during summer
crop growth.
Field-Site Description
Our study occurred on 4 privately owned crop fields in Tippecanoe County, IN.
The study area was characterized by flat topography and land use dominated by
agriculture (>70%) interspersed by remnant forest fragments (Gehring and Swihart
2003). Our study sites consisted of 4 conventionally farmed (annual tillage and
agrochemical [fertilizer and pesticide] applications) corn fields that were adjacent
to forested woodlots. Forested woodlots were 5–40 ha in size with overstories
dominated by Quercus spp. (oak), Carya spp. (hickory), Prunus serotina Ehrh.
(Black Cherry), and Acer spp. (maple). Rapid-assessment vegetation surveys we
conducted in the field indicated understory vegetation was predominantly Lonicera
maackii (Rupr.) Herder (Amur honeysuckle), Toxicodendron radicans (L.) Kuntze
(Poison Ivy), and Rosa multiflora Thunb. (Mulitflora Rose). Vegetation structure
was typically denser at woodlot edges, but species composition was similar to interiors
as has been documented in other forest fragments in this region (Anderson et
al. 2003).
Methods
Research design
Seed removal experiments. We quantified weed-seed predation by measuring
seed removal from experimental trays presented within each crop field. Seed trays
consisted of inverted plastic petri dishes, with seeds adhered using double-sided
carpet tape. We placed 50 Setaria faberi R.A.W. Herm. (Giant Foxtail) seeds on
each tray, and covered remaining tape with fine-grain sand to eliminate the chance
of accidentally capturing seed predators. Giant Foxtail is a common agricultural
weed in the eastern United States whose seed is consumed by both vertebrates
and invertebrates (Ward et al. 2014, White et al. 2007). We placed inverted seed
trays within fields such that seeds were flush with the soil surface and used vertebrate
exclosure (caged) and uncovered (open) seed trays to quantify relative seed
removal by vertebrate and invertebrate seed predators. Caged trays had a 10 cm
× 10 cm hardware cloth cage (1.27-cm mesh) placed over them to exclude vertebrates
from removing seeds, while open trays remained uncovered and available
to all seed predators. Additionally, we used 5 control trays per grid per sampling
period to account for seed loss due to wind or rain. Control trays were mounted
35 cm aboveground on top of a platform ringed with carpet tape that restricted
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consumption by vertebrate and invertebrate seed predators but remained subject to
seed loss by wind and rain. Seed trays remained in fields for 4 consecutive nights,
after which we counted the number of seeds remaining on trays.
We placed trays in fields during 4 trial periods (and corresponding stages of corn
growth): 21–25 May (emergence), 2–6 July (vegetative), 13–17 August (reproductive),
and 14–18 November 2015 (post-harvest). We arranged the trays on a grid
of consisting of 5 transects (A–E) running perpendicular to the forested woodlot
edge, with 20 m between each transect (Fig. 1). The first seed tray position was
10 m from the forest–field edge, with each subsequent position separated by 20-m
intervals and extending 190 m into field interiors. At each position, we placed a
single vertebrate exclosure tray within ~1 m of an open tray .
Sampling of seed predators. Shortly after (< 2 weeks) each seed-presentation
trial, we sampled for seed predators to identify vertebrate and invertebrate seed
predators within our study system. We used capture–mark–recapture via live
trapping with Sherman traps (H.B. Sherman Traps Inc. Tallahassee, FL) to determine
the species of vertebrate seed predators (i.e., rodents) present within seedremoval
grids. We rarely saw any sign of potential avian seed predators in or near
our grids during the course of this study, and therefore assumed that all vertebrate
seed consumption was by mammals likely to be caught in Sherman traps. We followed
the guidelines for use of wild mammal species as directed by the American
Society of Mammalogists (Sikes et al. 2011) and Purdue Animal Care and Use
Figure 1. Arrangement of experimental seed tray sampling grids within each of 4 corn fields
in Tippecanoe County, IN.
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Committee (PACUC). We placed a single Sherman live-trap at each seed tray
position along transects A–D. Traps were baited with black oil sunflower seeds
and checked for 2 consecutive trap nights. Once caught, inidividual rodents were
marked with metal ear tags (Kent Scientific Corp., Torrington, CT). We identified
captured vertebrates to species (i.e., White-footed Mice or Prairie Deer Mice)
using tail length and hind-foot length morphometric characteristics (Berl 2017,
Kalmer et al. 1998).
We sampled invertebrates within seed tray grids using pitfall traps consisting
of 1-quart plastic cups buried flush with the soil surface and covered with a plastic
plate that allowed access by ground-dwelling invertebrates. We placed 20 pitfall
traps per field during each sampling event (arranged on transects B and D). Pitfalls
remained in fields for 4 nights, after which we identified and classified all invertebrates
to their taxonomic family. Dominant invertebrate seed predators (species of
interest) included ground beetles (Carabidae) and crickets (Gry llidae).
Data analysis
We analyzed the number of Giant Foxtail seeds removed out of 50 after a 4-day
trial, with loss attributed to invertebrate or vertebrate consumption after accounting
for seed loss from wind or rain on control trays. We used the following formulas to
calculate the number of seeds removed over the course of each 4-day trial (following
Westerman et al. 2003):
(1) Invertebrate removal = NE - [(NC - RC) + RE]
(2) Vertebrate removal = NO - [[(NC - RC) + RE] - RO],
where R is the number seeds remaining on trays, N is initial number of seeds presented,
C indicates control trays, E indicates exclosure trays, and O indicates open
trays. We set seed removal to 0 in situations where seed loss from control trays (C)
equaled or exceeded seed removal from experimental trays (O or E).
We used negative binomial regression, implemented through program R (R
Core Development Team 2016), to investigate the effect of seed predator (invertebrate
or vertebrate), season (May [emergence], July [vegetative], August
[reproductive], November [post-harvest]), and distance from forest–field edge on
rate of seed removal. We specified a negative binomial error distribution instead
of a Poisson distribution due to zero inflation in counts of seed removal. Because
rates of seed removal significantly differed between seed predators (see Results),
we ran separate models for vertebrates and invertebrates to test the effects of covariates
on seed removal. For each seed-predator group we tested for additive and
interactive effects of season and distance from forest–field edge on rate of seed
removal. We used logistic regression to calculate the probability of mouse species
given capture (binary response; White-footed Mice or Prairie Deer Mice) as
a function of distance from forest–field edge. We used linear regression to test
whether mouse abundance (minimum number known alive) differed among seasons
or varied in relation to distance from forest–field edge. Significance was set
at α = 0.05 for all statistical tests.
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Results
Analysis of the effects of seed-predator type (vertebrate or invertebrate) on
seed removal indicated that vertebrates removed significantly more seeds than
invertebrates irrespective of season and distance from forest–field edge (Table 1).
Collectively, vertebrates (51.22% seed removal) accounted for removal of an average
of 2.8 times more seeds than invertebrates (18.26% seed rem oval).
Table 1. Parameter estimates from negative binomial regression of the number of Setaria faberi (Giant
Foxtail) seeds removed from experimental seed trays as a function of seed predator type (vertebrates
and invertebrates). Invertebrates were set as the intercept in the model.
Estimate SE t P
Intercept 2.212 0.041 54.21 less than 0.001
Vertebrates 1.031 0.057 18.03 less than 0.001
Figure 2. Predicted number of Setaria faberi (Giant Foxtail) seeds removed by (A) invertebrate
and (B) vertebrate seed predators in relation to season and distance from forest–field
edge. Error bars represent 95% confidence intervals. Maximum number of seeds that could
be removed = 50.
Table 2. Parameter estimates from negative binomial regression of the number of Setaria faberi (Giant
Foxtail) seeds removed by vertebrates as a function of seasonal stage of crop development (emergence
was used as the intercept), distance from forest–field edge, and their interaction.
Estimate SE t P
Intercept 1.401 0.125 11.174 less than 0.001
Vegetative 2.361 0.172 13.678 less than 0.001
Reproductive 2.096 0.172 12.134 less than 0.001
Post-harvest 2.053 0.172 11.88 less than 0.001
Distance 0.184 0.019 9.287 less than 0.001
Vegetative x distance -0.239 0.027 -8.684 less than 0.001
Reproductive x distance -0.200 0.027 -7.274 less than 0.001
Post-harvest x distance -0.212 0.027 -7.676 less than 0.001
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Vertebrate seed predation
Seed removal by vertebrates differed significantly among seasonal stages of
crop development and as a function of distance from forest–field edge (Table 2).
There was also a significant interaction between season and distance on seed removal,
such that seed removal by vertebrates increased near (less than 100 m) forest–field
edges during vegetative, reproductive, and post-harvest stages relative to spring
emergence (Fig. 2B). Average seed removal by vertebrates 10 m from forest–field
edges was minimal (~10%) during spring emergence but increased dramatically (by
60–80%) during the growing season and immediately post-harvest. In the interior
of fields, seed removal by vertebrates remained relatively constant (~45%) with
minimal seasonal variation (Fig. 2B).
White-footed Mice and Prairie Deer Mice were the only species of vertebrate
seed predators captured during our live-trap sampling. The proportion of Whitefooted
Mice and Prairie Deer Mice captured varied greatly as a function of distance
from forest–field edge (Fig. 3). The probability of a captured mouse being a Whitefooted
Mouse was greater less than 70 m from forest–field edges, whereas the likelihood
of a capture being a Prairie Deer Mouse was almost a certainty >125 m from edges
(Fig. 3). Mouse abundance varied as a function of season, distance from forest–
field edge, and their interactive effects. Mice were generally more abundant in crop
fields during summer crop growth than during spring emergence or post-harvest
(Table 3) and overall showed only a weak positive trend in relation to distance from
forest–field edge (Fig. 4).
Figure 3. Predicted probability of species identity, given captures of Peromyscus leucopus
(White-footed Mice) or Peromyscus maniculatus (Prairie Deermice) in relation to distance
from woodlot–field edge. Error bars represent 95% confidence inte rvals.
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Invertebrate seed predation
Ground beetles constituted the majority (58.9%) of invertebrate sampled. Pterostichus
spp. were the most commonly captured ground beetles (85.5%), followed by
Poecilus spp. (7.0%), Chlaenius spp. (3.4%), Harpalus spp. (3.0%), and Scarites
spp. (0.1%). Granivorous field crickets comprised 8.4% of invertebrates captured.
Other, non-seed-eating invertebrates captured included millipedes (Myriapoda;
24.2%), spiders (Arachnida; 6.3%), and centipedes (Chilopoda; 2.2%). Captures
of invertebrate seed predators (ground beetles and crickets) varied among seasons
and declined sharply following crop harvest in the fall (Fig. 5). Distance from forest–
field edge did not significantly affect seed removal by invertebrates (Table 4).
Rates of invertebrate seed removal varied significantly by season and were higher
Table 3. Parameter estimates from generalized linear model evaluating variation in vertebrate seed
predator (Peromyscus spp.) abundance (minimum number known alive) as a function of crop stage
(emergence was used as the intercept), distance from forest–field edg e, and their interaction.
Estimate SE t P
Intercept 0.346 0.113 3.054 0.002
Vegetative 0.005 0.001 5.164 less than 0.001
Reproductive 0.986 0.160 6.163 less than 0.001
Post-harvest 0.908 0.160 5.671 less than 0.001
Distance 0.209 0.160 1.307 0.191
Vegetative x distance -0.004 0.001 -2.658 0.007
Reproductive x distance -0.003 0.001 -1.965 0.495
Post-harvest x distance -0.004 0.001 -2.697 0.007
Figure 4. Mean abundance (minimum number known alive) of vertebrate seed predators
(Peromyscus spp.) in relation to season and distance from forest–field edge .
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during periods of crop growth (vegetative and reproductive stages; 31.5%) than
during emergence and post-harvest periods (7.8%; Fig. 2A). Additionally, there was
no interaction between season and distance from forest–field edg e.
Discussion
Understanding predation on weed seeds has applied importance because capitalizing
on ecosystem services can help improve the ecological integrity of agricultural
landscapes through reductions in agro-chemical use. We found that over a 4-day
Figure 5. Seasonal variation in median captures of invertebrate seed predators (Carabidae
and Gryllidae).
Table 4. Parameter estimates from negative binomial regression of the number of Setaria faberi (Giant
Foxtail) seeds removed by invertebrates as a function of crop stage (emergence was used as the
intercept) and distance from forest–field edge.
Estimate SE t P
Intercept 1.033 0.231 4.466 less than 0.001
Vegetative 1.155 0.320 3.601 less than 0.001
Reproductive 0.846 0.321 2.631 0.008
Post-harvest 0.292 0.325 0.945 0.368
Distance 0.057 0.037 1.551 0.121
Vegetative x distance 0.039 0.051 0.758 0.448
Reproductive x distance 0.047 0.051 0.917 0.359
Post-harvest x distance -0.015 0.052 -0.305 0.760
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period vertebrate and invertebrate seed predators removed a majority (on average,
~75%) of weed seeds presented on experimental seed trays in conventionally farmed
corn fields. This level of seed removal is comparable to weed-seed predation studies
in other cropping systems, including hayfields in the Netherlands (72%; Westerman
et al. 2003), upland wheat fields in Japan (42%; Ichihara et al. 2011), and corn or
soybean fields in Iowa (~57% and ~65%; Heggenstaller et al. 2006). Across both
groups, the highest amount of removal occurred during the summer crop growth,
which corresponds to the beginning stage of increased weed-seed rain (Blubaugh
and Kaplan 2016). Invertebrates in our study generally removed fewer weed seeds
than vertebrates, with removal rates by invertebrates substantially higher during
summer crop growth (vegetative and reproductive stages) than during spring crop
emergence or after fall harvest. Although our study found that vertebrates were
the dominant seed predator in conventionally farmed corn fields, other studies
have shown invertebrates to be the major seed predators in crop environments (e.g.
Blubaugh and Kaplan 2016). Multiple environmental (e.g., season) and biological
(e.g., seed preference) factors can affect the abundance and relative seed-consumption
rates of invertebrate and vertebrate seed predators (Cromar et al. 1999, Orrock
et al. 2003, Shearin et al. 2007). Our study was not designed to holistically address
the numerous factors contributing to species-specific variation in seed predation in
crop fields; nonetheless, our results suggest that omnivorous mice are more effective
predators of Giant Foxtail seeds throughout the crop-production cycle compared to
invertebrates. Strong seasonal variation in invertebrate seed removal was expected
because of seasonal variation in invertebrate activity patterns (Holland and Luff
2000, Westerman et al. 2003, Wilson et al. 1999). Whereas invertebrates are typically
dormant or inactive during the non-growing season, omnivorous mice are active
year-round and likely consume weed seed throughout the annual cycle. Therefore,
seasonal variation in activity patterns likely explains the temporal differences in removal
rate between vertebrate and invertebrate seed predators (Daedlow et al. 2012,
Lövei and Sunderland 1996).
Most previous studies of predation on weed seeds have solely considered factors
that affect seed removal rates by field-resident predators (e.g., tillage regime,
within-field vegetation, and microhabitat; Cromar et al. 1999, Jacob et al. 2006)
with little focus on seed predation by migrant or transient species. Our findings
suggest that forest mice migrating seasonally into crop fields from nearby noncrop
habitats (forested woodlots) can enhance seed predation along field edges.
The environmental benefits of remnant non-crop habitats (e.g., soil retention) in
fragmented agricultural landscapes are well documented (Altieri 1999, 2002). Our
results show that seed predators migrating from non-crop habitats can positively
impact within-field seed loss, particularly along crop field edges (Cardina et al.
1997, Menalled et al. 2000). The White-footed Mouse is considered a generalist
species, and individuals likely migrate from woodlots into adjacent crop fields in
search of food or other resources (Kalmer et al. 1998).
Cross-habitat resource subsidies, or the movement of nutrients or services from
one habitat type to another, are a common ecological phenomenon (e.g., Harding
et al. 2015, Schneider et al. 2011). In fragmented farmland ecosystems, our results
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suggest that non-crop habitats may augment seed predation services within crop
fields through seasonal migration or “spillover” by seed predators from non-crop
habitats. This finding potentially highlights additional ecosystem service benefits
provided by non-crop habitats in fragmented agro-ecosystems. Future investigations
of natural seed-predation services should therefore consider the role of
resident and seasonally opportunistic seed predators in regulation of weed populations
in crop fields (Menalled et al. 2000).
Farmers may be able to implement management strategies to reduce weed
growth by capitalizing on natural seed predation. Timing of seed consumption
can dictate the impact that seed predators have on weed population dynamics
(Westerman et al. 2003). As previously stated, we documented increased seed
removal by vertebrates during summer and fall, coinciding with periods of weed
seed rain (Blubaugh and Kaplan 2016). As such, high rates of predation on weed
seeds during this period can result in fewer seeds entering the seed bank and reduce
seed densities to levels sufficient to lower weed emergence in subsequent
years (Bohan et al. 2011, Blubaugh and Kaplan 2016, Chauhan et al. 2012, Lövei
and Sunderland 1996, White et al. 2007). Capitalizing on seed-predation services
can potentially reduce herbicide applications and thus reduce environmental
impacts of high-intensity agriculture (Bond and Grundy 2001, Rosegrant and
Livernash 1996).
Acknowledgments
This study was supported by Purdue College of Agriculture, Purdue Department of
Forestry and Natural Resources, the Indiana Academy of Sciences, and the USDA North
Central Sustainable Agriculture Research and Education Grant Program. We thank the
numerous volunteers who assisted with lab and fieldwork, C. Blubaugh for contributing
insight and materials, and P. Zollner, C. Day, and L. D’Acunto for reviewing earlier versions
of the manuscript.
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