# Full Text: ArgentineAnt

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RESEARCH ARTICLE
Foraging behavior and locomotion of the
invasive Argentine ant from winter
aggregations
Benjamin P. Burford1*, Gail Lee2, Daniel A. Friedman2, Esme´ Brachmann3☯,
Rebia Khan2☯, Dylan J. MacArthur-Waltz2☯, Aidan D. McCarty2☯, Deborah M. Gordon2
1 Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, California, United
States of America, 2 Department of Biology, Stanford University, Stanford, California, United States of
America, 3 College of Letters & Science, University of California Berkeley, Berkeley, California, United States
of America
☯These authors contributed equally to this work.
* bburford@stanford.edu
Abstract
The collective behavior of ant colonies, and locomotion of individuals within a colony, both
respond to changing conditions. The invasive Argentine ant (Linepithema humile) thrives in
Mediterranean climates with hot, dry summers and colder, wet winters. However, its forag-
ing behavior and locomotion has rarely been studied in the winter. We examined how the
foraging behavior of three distinct L. humile colonies was related to environmental condi-
tions and the locomotion of workers during winter in northern California. We found that colo-
nies foraged most between 10 and 15˚C, regardless of the maximum daily temperature.
Worker walking speed was positively associated with temperature (range 6–24˚C) and neg-
atively associated with humidity (range 25–93%RH). All colonies foraged during all day and
night hours in a predictable daily cycle, with a correlation between the rate of incoming and
outgoing foragers. Foraging activity was unrelated to the activity of a competing native ant
species, Prenolepis imparis, which was present in low abundance, and ceased only during
heavy rain when ants left foraging trails and aggregated in small sheltered areas on trees.
Introduction
The invasive Argentine ant, Linepithema humile, is established in Mediterranean climates
worldwide, where it is unicolonial and seasonally polydomous. Within a colony, workers,
queens, and brood are distributed among multiple nests linked by a trail network that expands
and contracts seasonally. During the polydomous summer phase, many workers can quickly
recruit to nutritional resources directly from the colony’s vast trail network [1], and then use
the network to distribute resources among multiple nests [2]. Colonies condense during win-
ter in Mediterranean climates, to aggregate in a single nest with very few foraging trails [3–5].
Winter conditions, including precipitation, cool temperatures, and decreased sunlight, reduce
resource availability relative to summer conditions [6, 7]. However, most studies of the
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OPEN ACCESS
Citation: Burford BP, Lee G, Friedman DA,
Brachmann E, Khan R, MacArthur-Waltz DJ, et al.
(2018) Foraging behavior and locomotion of the
invasive Argentine ant from winter aggregations.
PLoS ONE 13(8): e0202117. https://doi.org/
10.1371/journal.pone.0202117
Editor: James A. R. Marshall, University of
Sheffield, UNITED KINGDOM
Received: February 17, 2018
Accepted: July 27, 2018
Published: August 9, 2018
Copyright: © 2018 Burford et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: The dataset recorded
and analyzed during the current study is included
as supporting information.
Funding: The authors received no specific funding
for this work.
Competing interests: The authors have declared
that no competing interests exist.

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influence of environmental conditions on foraging behavior and locomotion in the invaded
range have been made in warm, dry summer conditions. Here we consider the behavior of L.
humile in winter conditions in northern California to further examine how it competes with
native species in invaded habitats.
Linepithema humile forage collectively, a process that in many ant species is regulated by
interactions among individuals [8]. As poikilotherms, the speed at which ants are able to move
and interact increases with ambient temperature [9–11]. Foraging behavior is also adjusted in
association with temperature [12–18], and this relation depends on biotic factors such as food
availability, habitat structure, and interactions with other species [15, 16, 19–21]. Linepithema
humile are active under a wide range of conditions, but the highest sustained rates of foraging
recorded in the invasive range occur during summer, when temperatures range between 10
and 35˚C [22–26]. Foraging by L. humile during this season declines outside the optimal tem-
perature range [22–26], which may allow some native ant species to persist in invaded habitats
[26–28]. In addition, locomotion rate in L. humile declines with temperature [11], so that
cooler conditions reduce the thermal envelope for foraging [29]. Although starvation and cool
temperatures do not reduce resource discovery by L. humile colonies examined in laboratory
settings [30], the narrow mid-winter temperature requirement (7–14˚C) that appears neces-
sary for this species to become established in a given habitat [31–33] suggests that foraging is
restricted by temperature.
Winter daily patterns of foraging and locomotion are known from only a single study in
southern California [22, 34]. In northern California, the native winter ant, Prenolepis imparis,
is one of the few native ant species remaining in urban environments where Argentine ants are
present [35]. It is active mainly in the winter [36], competes with L. humile for food resources
[37, 38], and has a chemical defense effective against L. humile [39]. To examine the behavior
of L. humile under wintertime conditions, and in the presence of P. imparis, we recorded the
rate and speed at which ants travelled on foraging trails of three winter aggregations in north-
ern California (Fig 1A) for three 24-hour periods, and concurrently measured ambient tem-
perature, relative humidity, light level, and the abundance of P. imparis. Our results 1) show
evidence for a winter circadian rhythm, 2) describe a shelter-seeking behavior in response to
heavy rain, 3) indicate that low numbers of a competing ant species do not deter foraging by L.
humile, and 4) demonstrate that locomotion and foraging activity differ in relation to tempera-
ture and humidity.
Results
Colony foraging behavior
All three L. humile winter aggregations maintained consistent bidirectional foraging trails on
Quercus agrifolia (Coast live oak) trees, with maximum sustained foraging rates ranging from
0.29–0.95 ants s-1 and forager walking speeds from 1.85–2.46 cm s-1. In all observations, forag-
ers traveling up trees rarely had full abdomens, while most traveling down did; this suggests
that ants were harvesting honeydew from scale insects observed in canopy foliage [7, 22, 40,
41]. The rate of ants travelling in both directions on trails was low in the early morning, rapidly
increased until early or late afternoon, and then gradually returned to the low early morning
level (Fig 2). During all hours of the 24-hour cycle of foraging, each colony maintained an
approximately equal rate of ants leaving and returning to the nest (Fig 3). The foraging rate up
trees was positively correlated with the foraging rate down trees at a lag of 1 hour, and to a
lesser extent, up to a lag of 3 hours (partial correlation coefficients from autoregressive
models > 0.5; Fig 4). Thus, the rate of outgoing foragers exhibited the highest association with
the rate of foragers returning to the nest the hour of or the hour before. Foraging trails
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dissolved only during heavy rain, when foragers aggregated in sheltered areas on tree trunks
near the trail instead of returning to the nest. These small aggregations were isolated from each
other by water on the tree. When the rain stopped, foragers moved between sheltered areas
and, once the trunk dried further, the foraging trail was reformed.
Environmental conditions, walking speed, and foraging
Ambient temperature, which ranged between 6.3 and 24˚C, was strongly associated with tree
surface temperature (linear regression, p < 0.003). Ant walking speed was positively related to
ambient temperature (quadratic mixed effect model, p < 0.003; Fig 5A); an increase of 1˚C
corresponded to an average (± 1SD) increase of 0.1 (± 0.03) cm s-1 in walking speed. Colony
foraging rate showed a negative parabolic relationship with ambient temperature (quadratic
Fig 1. The study area and observational methods at each Linepithema humile colony. In the study area (a) on Stanford main
campus, numbers represent locations of nests, grey lines paved paths, and shaded circles canopy cover. We consider colonies 2 and
3 to be distinct colonies in spite of their spatial proximity because we never saw trails connecting the two trees. In the observational
methods at each tree (b), points represent entrances to the nest (dark shaded area); dashed lines the bidirectional foraging trail; the
light shaded area the trunk area where Prenolepis imparis were counted; dark horizontal arrow the line where L. humile foraging
rate was recorded; and the 10.0 cm line parallel to the trail the line where L. humile walking speed was measured.
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mixed effect model, p = 0.003; Fig 5B). Foraging activity was highest for 5–6 hours at tempera-
tures from 10–15˚C in the evening (Fig 2). These thermal conditions also occurred for about 1
hour during the morning without a surge in colony foraging effort. Walking speed was not sig-
nificantly related to humidity, but showed a mildly negative association (Fig 5A); an increase
of 1% RH corresponded to an average (± 1SD) decrease of 0.013 (± 0.012) cm s-1 in walking
speed. Accounting for covariation between temperature and humidity showed that walking
speed had a significant association with humidity and a smaller coefficient, while the associa-
tion with temperature remained significant and also had a smaller coefficient (Fig 5). Colony
foraging rate showed a negative parabolic association with humidity (quadratic mixed effects
model, p < 0.003; Fig 5B); when accounting for covariation of predictors, both temperature
and humidity remained significant in their association with foraging rate, and coefficients
became marginally smaller (Fig 5). Light level showed a significant neutral association with
walking speed and foraging rate (quadratic mixed effects models, p < 0.003 in both cases; Fig
Fig 2. Walking speed and foraging rate in relation to temperature and humidity. Average normalized (0–1 scale) hourly foraging rate (black lines) and walking speed
(red lines) ± 1SD are plotted against linearly-interpolated average hourly temperature (˚C; a and b) and humidity (%RH; c and d) on the coolest (a and c) and warmest
(b and d) observations. Temperature and humidity data are missing from 10:00–12:00 on the warmest observation (shaded in grey) due to a temporary failure of power
supply in the sensor.
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5A and 5B). Neither walking speed nor foraging rate were associated with the abundance of P.
imparis (ranged from 0–5), which was seen often at Colony 2, less at Colony 1, and never at
Colony 3. When temperatures were lowest (observation 1), foraging activity was positively cor-
related with walking speed within 4 hours (partial correlation coefficients from autoregressive
models > 0.5). When temperatures were highest (observation 2), foraging rate was correlated
with walking speed within 8 hours.
Fig 3. The temporal pattern of Linepithema humile colony foraging activity in the rate of returning and outgoing foragers. Line color represents time since
observation start: during observations 1 and 2, hour 1 and 27 are equal to 05:00 on day 1 and 07:00 on day 2 (PST), respectively. The third observation occurred from
hour 2 to 18, or 06:00 to 23:00 on the same day. Grey lines represent a slope of 1.
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Discussion
We found that L. humile colonies foraged from winter aggregations during all day and night
hours. Other work has shown moderate levels of wintertime foraging by L. humile in northern
California [23] and North Carolina, USA [41]. Our observations suggest that tree structure
could facilitate continuous L. humile foraging, as in [21, 41], perhaps by offering dry microen-
vironments in bark cracks or on the underside of branches that protect forgers from rain. For-
aging activity of the L. humile colonies increased from an early morning low until a peak in the
afternoon, and then gradually declined until the following morning (Figs 2 and 3). A similar
pattern of circadian oscillations in winter foraging by L. humile was found during a 24-hour
Fig 4. The correlation between returning and outgoing Linepithema humile foragers. Bars represent partial correlation coefficients between normalized (0–1 scale)
hourly foraging rate down and up trees when the foraging rate up is shifted -12 to 12 hours. Partial correlation coefficients were greatest with a lag of 0–1 hours between
rates down and rates up (shaded in grey).
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Fig 5. Analysis of the association of environmental factors with log transformed Linepithema humile (a) walking speed and (b) foraging rate. Points represent
coefficients (± SE) of the x2 term from quadratic mixed effects models, and are color-coded by predictor: red = temperature, blue = humidity, grey = light level, and
black = P. imparis abundance. Error bars in (a) are present, but small. A Bonferroni correction reduces alpha to 0.013, and asterisks () on the x-axis labels represent
significant associations. Corrections for covariance between temperature and humidity resulted in the following coefficients (all p < 0.013): walking speed-temperature
(0.62), walking speed-humidity (-0.38), foraging rate-temperature (-2.60), and foraging rate-humidity (-3.36). Insets in both (a) and (b) are visualizations of the
quadratic equations (based on slopes and intercepts) relating each dependent and independent variable from the mixed effects models.
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period at four trees in a southern California citrus grove [22], and the alignment with our find-
ings may suggest a relatively conserved daily activity cycle in winter.
Argentine ant recruitment, in response to trail pheromone, is primarily known from exper-
iments investigating exploratory behavior [42, 43]. In our study, colonies were not exploring a
new habitat, but instead apparently harvesting the honeydew of scale insects, a relatively per-
sistent resource [7, 22, 40, 41]. All colonies maintained a ratio of about one to one of foragers
traveling up to foragers traveling down a tree (Fig 3), and rates of outgoing foragers were also
correlated with rates returning to the nest within the previous hour (Fig 4). Recent work indi-
cates that the volume of L. humile foragers on bidirectional trails is altered in response to
changing resource abundance and quality [44]. We hypothesize that, as in other species (e.g.
the harvester ant Pogonomyrmex barbatus) [45], returning foragers may stimulate outgoing
foragers to leave the nest.
Linepithema humile foraging trails dissolve when trail pheromone concentrations are
reduced to levels that are undetectable by workers [46]. During intense rainstorms, L. humile
left foraging trails and aggregated in sheltered locations on the trees–perhaps because chemical
trails were obscured when rain water saturated the tree trunks. Similar behavior during rain
has also been observed in the leaf-cutting ant Atta cephalotes, when workers abandon the for-
aging trail in search of dry locations on nearby trees [47, 48]. Behavior similar to shelter-seek-
ing on foraging trails may be involved in the formation of winter aggregations. In choosing
aggregation sites, colonies react to pervasive wet and cold conditions, on a larger spatial and
temporal scale, by condensing many nests and a large trail network to one or two sheltered
nest sites [3, 24].
The temporal partitioning of nutritional resources within ant communities is influenced by
competition [15], and this can limit the distribution of L. humile [35]. Prenolepis imparis for-
ages on both trees and the ground in large numbers during winter in northern California [39].
However, we observed this native species only at very low levels on the trees where L. humile
colonies were aggregated. Although P. imparis possesses a chemical defense that can harm L.
humile aggressors [39], and can reduce habitat colonization by L. humile [38], it appears that
these small numbers of P. imparis ants did not deter L. humile foraging (Fig 5B).
Forager walking speed was positively associated with temperature and showed a negative
trend with respect to humidity (Fig 5A), as is common in colonial poikilotherms [9–11]. Dur-
ing the low wintertime temperatures we observed, the average rate at which walking speed
increased with temperature (0.10 cm s-1˚C-1) was half that reported in L. humile under higher
summer temperatures (0.20 cm s-1˚C-1 at 25.2–33.8˚C) [10]. Peaks in walking speed preceded
peaks in foraging activity, with the time elapsed between maximum daily speed and foraging
rate longer during warmer conditions than cooler conditions (Fig 2). While walking speed
exhibited a mild positive parabolic relationship with temperature, foraging rate exhibited a
strong negative parabolic relationship with temperature (Fig 5A and 5B). Thus, foraging activ-
ity and locomotion rate differed in their relation to temperature.
Linepithema humile is most likely to occur where mean daily temperatures in mid-winter
range between 7 and 14˚C [31]. We found that in winter, colonies appeared to prefer to forage
most from 10–15˚C, even though the maximum daily temperatures ranged from 17.7 to
24.05˚C (Fig 2). This contrasts with the high rates of L. humile foraging at higher temperatures
during the summer polydomous phase [22–25]. However, our results do not show whether the
surge in foraging effort from 10–15˚C reflects temperature preference, as these thermal condi-
tions briefly occurred in morning hours with no spike in foraging effort. It may be that forag-
ing rate is related to a circadian rhythm that happens to align with a narrow temperature
range. Although it is likely that a variety of factors are at play, the 10–15˚C thermal window
may have provided an improved opportunity, metabolic [11–14, 29] or environmental [44,
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49], for L. humile colonies to forage on hemipteran honeydew during a time of reduced
resource availability [6, 7].
Methods and materials
Study area
The study was conducted in a 5.15-acre cultivated woodland bordered by footpaths, buildings,
and a parking lot on Stanford University’s main campus, CA, USA (37˚25’47"N by 122˚
10’14"W) (Fig 1A). This woodland is mostly composed of Quercus agrifolia (Coast live oak),
with Sequoia sempervirens (Coast redwood), Olea sp. (Olive), and Quercus douglasii (Blue oak)
in the overstory. Several Aesculus californica (California buckeye), Rhamnus sp. (Buckthorn),
and Ceanothus thyrsiflorus (Blueblossom ceanothus) grow under the main canopy. The under-
story is dominated by non-native annual European grasses, and includes scattered pedestrian
paths, leaf litter, and wood chips. There was moderate foot, bicycle, and service vehicle traffic
throughout the study, but no direct impact of human activity on the trees the ants were using.
In January 2016, we identified three winter aggregations of L. humile colonies (Fig 1A). Col-
onies 2 and 3 were approximately 20 m apart and Colony 1 was about 100 m away from 2 and
3. Although trails can extend up to 43 m from a winter aggregation [1], in observations from
January to April 2016, we never observed trails linking any of the three aggregations, so we
considered the 3 aggregations to be separate colonies [2, 50]. Each colony’s aggregation nest
was at the base of a Q. agrifolia tree exposed to southern light. All three colonies had estab-
lished a bidirectional foraging trail leading from the nest, up along the trunk, and into the tree
canopy.
Environmental conditions
To monitor environmental conditions during our behavioral observations, we arranged and
affixed a DHT22 temperature and humidity sensor, CdS photoresistor, Arduino UNO proces-
sor, SD card, and 9V alkaline battery inside a transparent, cylindrical plastic tube using hot
glue, hung 2 m off the ground underneath a southeast-facing branch in tree 2 (Fig 1A). We
recorded ambient temperature (˚C), relative humidity (0–100%), and light level every 5 sec-
onds for the duration of all observation periods. We also measured the surface temperature of
tree trunks where foraging trails were located during the second observation (05:00 on 2/22–
07:00 on 2/23) to compare with air temperature recorded by the data logger (Ryobi ZRIR001
Non-Contact Infrared Thermometer, Solar Wide Industrial Ltd., Hong Kong). We recorded
the number of P. imparis, the only other ant species we found in the study area, in a specific
region of all tree trunks (trunk area, Fig 1B) at the beginning of all observations.
Colony behavior
The foraging trails of the three L. humile colonies were simultaneously monitored in three sets
of observations in winter 2016. Observation 1 was made from 05:00 PST on 2/1–07:00 on 2/2
(27 h); observation 2 from 05:00 on 2/22–07:00 on 2/23 (27 h); and observation 3 from 06:00–
23:00 on 3/14 (17 h). To minimize disturbance, observations at night were made using the red
light setting on Fred LED Headlamps (Princeton Tec1, USA). At each colony, a line was
marked perpendicular to the foraging trail and tree trunk 1.0 m up the trunk from the main
nest entrance to measure foraging rate. Just below this rate line, we marked a second 10.0 cm
line, the speed line, parallel to the foraging trail (Fig 1B). We made behavioral measurements
at the rate and speed lines each hour at each aggregation. All foraging trail locations, and thus
rate and speed lines, remained consistent throughout the study. Foraging was estimated by
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counting the number of L. humile ants that passed the rate line travelling to and from nests for
16 sequential 30 s intervals during each observation. Ant walking speed was measured by
recording the time it took 1–10 individual foragers headed both directions to travel the length
of the speed line.
Statistical analysis
All analyses were conducted in R [51] or MATLAB [52], were two-tailed, and met assumptions
unless otherwise noted. Measurements of physical variables taken every 5 seconds were averaged
for each aggregation’s hourly observation period. To evaluate how well ambient temperature
predicted tree surface temperature, we used linear regressions for each tree with ambient and
surface temperature on 2/22–2/23 as the independent and dependent variables, respectively. We
found for each observation period the mean of the foraging rate (number of foragers s-1) and for-
ager speed (cm s-1) counts in both directions.
To capture general trends of association despite differences among colonies, hourly for-
aging rates and speeds were normalized on a 0–1 scale within colonies and days. The highest
foraging rate and speed for a given colony on a given day would be 1, and the lowest rate
and speed 0. The abiotic conditions under which the highest foraging rates and forager
speeds occurred were investigated by averaging the normalized (0–1 scale) foraging rate
and forager speed of all colonies on the coldest and warmest observations (1 and 2, respec-
tively). We then plotted these values (± 1SD) against linearly interpolated temperature and
humidity data (Fig 2).
To illustrate the temporal pattern of foraging activity, we plotted the mean foraging rate in
each direction over time (Fig 3). We examined the correlation between foraging rate up and
down the trees by calculating shifts in the timing of association. The partial correlation coeffi-
cients between normalized (0–1 scale) hourly colony foraging rates in both directions were cal-
culated for each colony using autoregressive models, with values above 0.5 or below -0.5
considered to be significant positive and negative correlation, respectively. Correlation of
these two variables was examined at shifts of -12 to 12 hours. If outgoing foragers tended to
leave the nest shortly after returning foragers entered the nest, partial correlation coefficients
between foraging rates up and down would be significantly positive with no or little time shift
(Fig 4).
To examine how environmental parameters were related to L. humile foraging rate and for-
ager walking speed up trees, which were non-independent measures, we performed both linear
and quadratic mixed effects analyses with foraging rate or walking speed as dependent vari-
ables and ambient temperature, relative humidity, light level, and P. imparis abundance as
independent variables. Environmental predictors were the fixed effects, and to account for var-
iation among colonies and trees, by-colony and by-day intercepts and slopes for the influence
of environmental predictors on speed and foraging were random effects. Prior to running the
models, both independent and dependent variables were log-transformed so that all data
would be on a similar scale, thus enhancing the signal of non-dominant data. We performed
one linear and one quadratic mixed effects analysis for each dependent variable as a function
of all independent variables. For both pairs of linear and quadratic models, we used ANOVA
to perform a likelihood ratio test (Chi-square) to determine if the quadratic model had explan-
atory value over the linear model (alpha = 0.05). If the reduction in residual sum of squares
was statistically significant, we reported results from the quadratic model. In both cases, the
quadratic models were used. After model selection, we identified outlying data points based on
quantile-quantile plots of the residuals. If outliers were present (points well beyond 95% CIs),
we ran models with and without these data. Finding similar direction and significance of
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effects to models with outliers included, we report only model results with these data removed
(3 and 6 data points were removed from the foraging rate and forager speed model, respec-
tively). P-values for each predictor were determined using likelihood ratio tests to compare the
model with each effect against the model without it. Coefficients (± SE) and p-values for each
predictor-response comparison from mixed effects analyses are identified based on predictor
and significance (a Bonferroni correction reduces alpha to 0.013) (Fig 5). Two independent
variables, temperature and humidity, exhibited a relatively high degree of correlation (0.83)
and thus may have led to type II error. We re-ran both analyses with temperature or humidity
omitted from the fixed effects to assess the potential for inaccuracy in the respective coeffi-
cients and p-values (Fig 5).
To determine if foraging rate was associated with walking speed, and if this association
depended on temperature, we compared the correlation between foraging rate and walking
speed up trees on the coldest and warmest observations (1 and 2, respectively). The partial cor-
relation coefficients between normalized (0–1 scale) hourly foraging rate and walking speed
were calculated for each colony using autoregressive models, as described above. If colonies
foraged most when workers were travelling most rapidly, partial correlation coefficients would
be significantly positive with little or no time shift.
Supporting information
S1 Data. The dataset recorded and analyzed during the current study.
(CSV)
Acknowledgments
The authors are especially grateful to two anonymous reviewers, Philip Lester, and Rachel
Crane for valuable feedback that improved the manuscript. We also thank Taylor Powell for
assisting with data collection.
Author Contributions
Conceptualization: Benjamin P. Burford, Gail Lee, Daniel A. Friedman, Deborah M. Gordon.
Data curation: Benjamin P. Burford, Gail Lee, Esme´ Brachmann, Rebia Khan, Dylan J. Mac-
Arthur-Waltz, Aidan D. McCarty.
Formal analysis: Benjamin P. Burford, Gail Lee, Daniel A. Friedman, Esme´ Brachmann,
Rebia Khan, Dylan J. MacArthur-Waltz, Aidan D. McCarty.
Investigation: Benjamin P. Burford, Gail Lee, Daniel A. Friedman.
Methodology: Benjamin P. Burford, Gail Lee, Daniel A. Friedman, Deborah M. Gordon.
Resources: Deborah M. Gordon.
Supervision: Deborah M. Gordon.
Validation: Benjamin P. Burford.
Visualization: Benjamin P. Burford, Gail Lee, Daniel A. Friedman, Esme´ Brachmann, Rebia
Khan, Dylan J. MacArthur-Waltz, Aidan D. McCarty.
Writing – original draft: Benjamin P. Burford, Daniel A. Friedman, Deborah M. Gordon.
Writing – review & editing: Benjamin P. Burford, Gail Lee, Daniel A. Friedman, Esme´ Brach-
mann, Rebia Khan, Dylan J. MacArthur-Waltz, Aidan D. McCarty, Deborah M. Gordon.
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*Extraction method: pymupdf*