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Seasonal Foraging by Forest Mice Enhances Loss of Weed Seeds from Crop–Field Edges
Sarah A. Abercrombie, Jacob L. Berl, Elizabeth A. Flaherty, and Robert K. Swihart

Northeastern Naturalist,Volume 24, Special Issue 8 (2017): 5–17

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Northeastern Naturalist 5 S.A. Abercrombie, J.L. Berl, E.A. Flaherty, and R.K. Swihart 2017 Vol. 24, Special Issue 8 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 Northeastern Naturalist S.A. Abercrombie, J.L. Berl, E.A. Flaherty, and R.K. Swihart 2017 6 Vol. 24, Special Issue 8 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 Northeastern Naturalist 7 S.A. Abercrombie, J.L. Berl, E.A. Flaherty, and R.K. Swihart 2017 Vol. 24, Special Issue 8 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 Northeastern Naturalist S.A. Abercrombie, J.L. Berl, E.A. Flaherty, and R.K. Swihart 2017 8 Vol. 24, Special Issue 8 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. Northeastern Naturalist 9 S.A. Abercrombie, J.L. Berl, E.A. Flaherty, and R.K. Swihart 2017 Vol. 24, Special Issue 8 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. Northeastern Naturalist S.A. Abercrombie, J.L. Berl, E.A. Flaherty, and R.K. Swihart 2017 10 Vol. 24, Special Issue 8 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 Northeastern Naturalist 11 S.A. Abercrombie, J.L. Berl, E.A. Flaherty, and R.K. Swihart 2017 Vol. 24, Special Issue 8 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. Northeastern Naturalist S.A. Abercrombie, J.L. Berl, E.A. Flaherty, and R.K. Swihart 2017 12 Vol. 24, Special Issue 8 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 . Northeastern Naturalist 13 S.A. Abercrombie, J.L. Berl, E.A. Flaherty, and R.K. Swihart 2017 Vol. 24, Special Issue 8 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 Northeastern Naturalist S.A. Abercrombie, J.L. Berl, E.A. Flaherty, and R.K. Swihart 2017 14 Vol. 24, Special Issue 8 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 Northeastern Naturalist 15 S.A. Abercrombie, J.L. Berl, E.A. Flaherty, and R.K. Swihart 2017 Vol. 24, Special Issue 8 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). 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