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Ecology & Evolutionary Biology
Spring 1-1-2014
The Effects of Wind on Foraging Strategies of Atta
cephalotes Leaf-Cutter Ants
Michael John Rodriguez
University of Colorado Boulder, [email protected]
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THE EFFECTS OF WIND ON FORAGING SRATEGIES OF ATTA CEPHALOTES LEAFCUTTER ANTS
By MICHAEL JOHN RODRIGUEZ
B.S., Southeastern Louisiana University, 2011
A thesis submitted to the
Faculty of the Graduate School of the
University of Colorado in partial fulfillment
of the requirement for the degree of
Master of Science
Department of Ecology and Evolutionary Biology
2014
This thesis entitled:
The effects of wind on foraging strategies of Atta cephalotes leaf-cutter ants
written by Michael John Rodriguez
has been approved for the Department Ecology and Evolutionary Biology
Dr. Michael Breed
_____ Dr. Rebecca Safran
Date
The final copy of this thesis has been examined by the signatories, and we
Find that both the content and the form meet acceptable presentation standards
Of scholarly work in the above mentioned discipline.
iii
Rodriguez, Michael John (M.S., Department of Ecology and Evolutionary Biology)
The effects of wind on foraging strategies of Atta cephalotes leaf-cutter ants
Thesis directed by Professor Dr. Michael Breed
Abstract: Successful foragers alter their behavior in response to variation in local conditions,
resulting in reduction of foraging costs and maximization of resource gain. In eusocial colonies,
individuals may adjust their own efforts to maximize the productivity of the colony as a whole.
Maximization of colony productivity can be achieved through sub-maximal individual
performance. Attine leaf-cutter ant foragers often cut leaf fragments shorter than the hind legs
could allow, suggesting other factors contribute to load size determination. Several studies have
shown reasons why leaf-cutter ants cut smaller loads than they could maximally carry. The
effects of wind speed on leaf-cutter load size selection were examined in this study and showed
conditions in which leaf-cutter foragers change their behavior to cut larger loads than normal. In
response to wind treatments, foragers cut larger leaf loads and fewer minima workers hitchhiked
on those leaves. This study highlights behavioral plasticity of leaf-cutter foragers in response to
local conditions on the foraging trail, and it adds to our knowledge of resource allocation in
central-place foraging systems.
Key words: behavioral flexibility, ethology, foraging, load size selection, parasitism, social
insects
iv
Acknowledgements
Special thanks for funding from the Organization for Tropical Studies, the University of
Colorado, Boulder Department of Ecology and Evolutionary Biology, Colorado Diversity
Initiative, and Petridish.org contributors including: Sandra Blair, Michael Bonner, Kevin
Westmoreland, Jasmine Hegman, Nicole Gorden, James Waters, Jason Steiner, Samuel J. Ciurca,
Jr., James Jorasch, Gaurav Vaidya, Jaime Pawelek, Daniel Ewald, Kwame Hagan, Nicholas
Barbieri, Bob Peake, Kenneth Trease, Kelly Stewart, Mustafa, Susan Fay, and Alan F.
Rodriguez. Thank you to the staff and researchers of La Selva and the participants and
instructors of OTS Tropical Biology course 2012-1. Thanks to my adviser, Dr. Michael Breed,
and lab mates for guidance and reviews. Thank you to Dr. Catherine and Mac Macgregor.
v
CONTENTS
Introduction...............................................................................................1
Leaf-cutter ant background.................................................................2
Foraging efficiency ......................................................................... 3-7
Hitchhiker ants ..............................................................................7
Purpose of the study ............................................................................8
Methods ............................................................................................... 9-13
Results.. ............................................................................................. 13-19
Discussion ......................................................................................... 20-24
Conclusion .................................................................................. 24-25
References ......................................................................................... 26-30
vi
FIGURES
Figure
1.
Leaf fragment area between wind treatments ...............................................14
2.
Leaf fragment area and forager head width................................................. 15
3.
Forager head width between wind treatments ..............................................15
4.
Interaction of forager head width and leaf fragment area between wind
treatments................................................................................................16
5.
Hitchhiker numbers between wind treatments ..............................................17
6.
Foraging trail traffic density and leaf fragment mass ..................................18
7.
Leaf fragment area between leaf type ...........................................................19
8.
Forager head width between leaf type ..........................................................19
1
Introduction
Successful foragers alter their behavior in response to a shifting external environment
(Charnov 1976). This results in reduction of foraging costs and maximization of resource gain if
local conditions vary. In eusocial colonies, individuals specializing in certain tasks may adjust
their own efforts to maximize the productivity of the colony as a whole (Burd 1996a; Constant et
al. 2012). Theory predicts that individuals adjust their foraging efforts to achieve optimal
resource input into the nest (Charnov 1976; Wetterer 1989; Burd 1996a; Burd and Howard
2008). Interactions among nestmates and external cues allow individuals to alter their behavioral
effort, especially as different biotic (parasitism, predation, nest-mate interactions) and abiotic
conditions (rain, wind, temperature) vary (Hölldobler and Wilson 1990; Feener and Moss 1990;
Gordon 2002; Angilletta et al. 2008; Elizalde and Folgarait 2012). Behavioral variability within
a colony and behavioral flexibility displayed by individuals may contribute to the evolutionary
success of colony phenotypes and to the ecological success of the eusocial Hymenoptera (Wilson
1971; Constant et al. 2012). My results from studies of foraging in a leaf-cutter ant, Atta
cephalotes, add to our understanding of the complex interplay between costs and benefits in
central place foraging systems and how individual behavior and recruitment behavior of leafcutter ants is plastic in response to abiotic and biotic external conditions, such as wind (Rudolph
and Loudon1986), traffic on the foraging trail (Farji-Brener et al. 2011), or the presence of very
small workers, called minima, riding on a carried load (Feener and Brown 1992; Orr et al. 1995;
Porter et al. 1995).
Leaf-cutting ants
2
A small percentage of ant species have polymorphic workers (Wetterer 1994), and within
the fungus growing ants, family Formicidae, subfamily Myrmicinae, tribe Attini, only some
species have workers with different size castes. Workers of the monomorphic Attini forage for
insect carcasses, waste, and other detritus that do not require further processing. The
polymorphic Attini are specialist foragers on vegetable matter (seeds, flowers, and leaves). This
plant material needs special treatment to convert to a suitable substrate for fungal gardens grown
by the ants and used as food. Handling of plant material in preparation for use in fungal
gardening includes fragmentation, chewing, and regurgitation onto the fungal garden (Wilson
1980a, b).
Leaf-cutting ants in the genera Atta and Acromyrmex have highly polymorphic workers,
resulting in a high division of labor with workers specializing on tasks appropriate for their size
(morphological polyethism) (Wilson 1980a, b). In Atta cephalotes leaf-cutter ants, the species
addressed in this study, the largest workers can be 200 times the size of the smallest workers
(Weber 1972). The large, major, workers and intermediate, media, workers act as soldiers and
foragers, made effective by their large bodies and mandibular muscles. The smaller, or minima,
workers take care of the brood and garden and maintain the trails (Hughes and Goulson 2001).
Inside the nest, minima gardeners fragment the forage into a pulp that they feed to
basiodiomycetes fungi which are cultured as the primary food source for their developing larvae.
To a lesser extent adults also feed on the fungi (Weber 1972; Quinlan & Cherrett 1979;
Benckiser 2011). The fungal gardens are analogous to human agriculture (Benckiser 2011).
Minima workers are primarily fungal caretakers but have a secondary role as defenders of
adult ants against parasitic phorid flies (Phoridae: Pseudoacteon sp.). Minima workers hitchhike
rides aboard leaf fragments carried back by larger workers (Wilson 1980a, b; Feener and Moss
3
1990; Vieira-Neto et al. 2006) and fend off these flies. Foragers can travel for hours over long
distances on dedicated and manicured trails, recorded to span 300 m from the nest entrance, with
a mean distance of 50 m (Lewis et al. 1974; Wetterer 1990). Foragers travelling back to the nest
carrying loads are more vulnerable to parasitoid attack than unladen workers, and hitchhiking
ants offer defense, rearing up on hind legs to grab the fly or to block oviposition (Feener and
Moss 1990; Vieira-Neto et al. 2006). Considering the long travel times of foragers and their
vulnerability while carrying loads, hitchhikers offer a valuable defense from parasitoid enemies.
In addition to defense, hitchhikers sometimes work to remove trichomes on the leaf fragment,
decrease parasitic fungal load, and retain sap leaking from the leaf fragment as it is carried
(Vieira-Neto et al. 2006; Kitayama et al. 2012).
Foraging Efficiency
In eusocial species, behaviors have evolved that maximize colony productivity over
individual productivity (Burd 1996a). Optimal colony productivity can often be achieved
through sub-maximal individual performance. Nuñez (1982) showed that Apis mellifera
honeybees carry a less than maximal nectar load for faster recruitment of other workers to new
resources. In a competitive environment with limited resources, scramble competition drives the
location of, recruitment to, and monopolization of resources as quickly as possible (Hölldobler
1976; Brännström and Sumpter 2005). By spending only a moment to sample the nectar source
and flying with a minimal load, the honeybee recruits nest-mates to the resource faster. SchmidHempel et al. (1985) found that A. mellifera workers often return from a non-depleted nectar
resource to their nest with half-filled crops, increasing flight efficiency at the expense of
maximum nectar transport rate. Similarly, Jeanne (1999) showed that Polybia occidentalis
4
wasps bring back less nest construction material than they can maximally carry, increasing
material handling efficiency at the nest and flying efficiency so that they can make more trips per
unit time. Taylor (1977) demonstrated that Cataglyphis desert ants carry intermediate sized
loads to decrease travel time and sun exposure. Burkhardt (1998) reported Pheidole ant workers
from larger colonies spending less time drinking from a resource and more time recruiting than
ants from smaller colonies. In each of these cases workers achieve maximum transport rate as a
colony by balancing the costs that load mass creates for travel velocity.
Considering the energy required and the dangers associated with leaving the nest, centralplace foraging theory predicts that leafcutter foragers should select loads that maximize resource
delivery rate to the nest, (e.g. loads should be larger farther away from the central nest to
compensate for longer travel times) (Wetterer 1989; Roces 1990b). As predicted by theory,
Roces (1990) found that Acromyrmex lundi leaf-cutter ants cut larger fragments the further they
are from the nest, maximizing profitability. Cherrett (1972) found that smaller foragers cutting
from a fruit resource give up cutting when faced with very tough surfaces, allowing them to
switch to more time-efficient resources. Wetterer (1994) proposed that smaller workers disturb
and displace larger workers at more tender surfaces ensuring that loads are cut by the smallest
sized workers needed to accomplish the task. Counterintuitively, in leaf-cutter systems, the
average loads carried by workers are below the size necessary to achieve maximal leaf tissue
delivery rates (Burd 1996b, 2000, 2001).
Foraging leaf-cutter workers control the size of the leaf fragment they carry through their
cutting behavior. Observers originally thought that the size of the leaf load was dictated by the
size of the individual ant; early studies found a correlation between load mass and ant mass (Lutz
1929; Cherrett 1972; Rudolph and Loudon 1986; Waller 1986; Wetterer 1990). Lutz (1929)
5
proposed that leaf-cutter foragers pivot on their hind legs while cutting, establishing a fixed
cutting arc determined by the length of the hind legs.
However, individuals often cut fragments shorter than the hind legs could allow,
suggesting other factors contribute to determining load size (Roces and Nuñez 1993; Roces and
Hölldobler 1994; Burd and Howard 2005a,b; Dussutour et al. 2009a,b; Farji-Brener et al. 2011).
Comparing worker body length to the radius of the leaf fragment it carried, Rudolph and Loudon
(1986) found a weak correlation between fragment size and rear leg length, indicating that
foragers often cut fragments smaller than their hind legs could allow. Also, foragers cutting
denser leaves (the ratio of fragment area to volume) often cut smaller leaf fragments than
foragers cutting less dense leaves, suggesting a behavioral mechanism whereby foragers might
cut smaller loads than their body size would permit. Recent research demonstrates that
patrilineal lineages within colonies vary significantly in foraging behavior and this can affect the
size of the fragment cut, the time to cut it, and the transport velocity indicating genetic
mechanisms altering cutting behavior (Constant et al. 2012).
Shape and size may be of great importance when selecting a load because of
maneuverability. Dussutour et al. (2009b) found that placing an obstacle over the foraging trail
affected the shape of leaves cut in a foraging arena. The foragers cut shorter (smaller) leaf
fragments to fit back under the obstacle on their way back to the nest, showing individual
behavioral plasticity in load size selection. Also, perhaps to compensate for the decreased
biomass transport rate because of smaller fragments, more workers were recruited when the
obstacle was present compared to when the foraging path was clear. Farji-Brener et al. (2011)
found that traffic congestion on the foraging trail resulted in large foragers cutting lighter loads
6
to avoid slowing nestmates behind them like a semi-truck on a highway (the Truck Driver
Effect).
Previous studies on leaf-cutter ants establish that collection of larger fragments is more
efficient in terms of biomass transported per unit of perimeter cut, but heavier loads decrease
walking speed thereby increasing transport time to the colony (Rissing 1984; Rudolph and
Loudon 1986; Burd 1996a; personal observation). Maximal leaf transport rate occurs at the
point where the load gets large enough to slow walking speed of laden ants enough to offset the
biomass transport rate to the nest (Rudolph and Loudon 1986). The costs associated with larger
loads slowing velocity are more pronounced at farther distances, and the ability to inform nest
mates of a quality resource may affect load size in the early stages of foraging because of the
relationship between load size and travel velocity.
Researchers have developed models to predict maximal biomass transport rate to the
colony (Burd 1996a; Burd 2000; Burd and Howard 2005). The rest of this section discusses
three models of biomass delivery in Atta cephalotes leaf-cutter systems. The first two models
examine the foraging round trip outside the nest entrance, and the first model specifically focuses
on traffic congestion on leaf cutting surfaces. The third model takes previous models into
account and adds components of leaf processing time once inside the nest to determine optimal
parameters maximal resource input rate.
Maximizing the load size for individual workers may result in sub-optimal colony-wide
resource input because of queue time effects (waiting) in dense traffic situations (Burd 1996a).
There is a limited amount of surface area on a cutting surface (leaf), and leaf-cutter ant colonies
may benefit from sub-optimal individual performance when congestion is high. Foragers cutting
smaller leaf fragments experience a shorter cutting time. By cutting a smaller load than any
7
individual can maximally carry, server availability (cutting sites) is increased and more recruited
individuals are able to access that resource per unit time, resulting in greater resource acquisition.
Cutting sites are vacated quickly and the colony receives greater biomass transfer rate. However,
Burd (1996a) admits that the model may not fit because in natural canopies, it is unknown if the
density of workers reaches a high enough threshold to cause server queues and likely that
workers spread out on individual leaves and within a canopy.
Burd (1996a) composed a second model for maximal biomass collection and transport
back to the nest which removes any queue effects and takes into account colony size, ant mass,
leaf density, cutting time as a function of ant size, and ant velocity as a function of ant and load
mass. Burd (1996a) also took into account the physical space on a leaf that could be occupied
for different distributions of ant size classes and set the parameters to maximize cutting speed.
Lastly, the model accounted for the distance from the nest to include outbound travel time,
cutting time, and return travel time. Burd (1996a) compared this maximal biomass transfer
model to Atta columbica ants naturally foraging on Barro Colorado Island, Panama and found
that foragers cut loads below the size that would allow for maximal biomass transfer to the
colony, implying more complex rules exist for foraging than obtaining the largest load possible.
Burd and Howard (2005b) presented a new model for leaf tissue delivery to and inside
the nest after cutting and discovered optimality in the model when fragments were predicted to
be intermediate in size. The model took several factors into account such as the number of laden
foragers, the distance from the nest to the resource, the outbound speed of ants, the inbound
speed as a function of load size (leaf fragment area), the transfer time through the nest as a
function of load size, the capacity of fugal garden chambers, and the size and nutritional state of
8
the colony. Empirical data have not confirmed the model, but their finding points to potential
effects of processing leaf fragments inside the nest on load size selection.
Hitchhiking minima
The presence or absence of hitchhiking leaf-cutter minima workers may also affect load
size selection. These minima workers are found on the foraging trail and often ride back to the
nest (“hitchhike”) on a leaf fragment carried by a larger worker. Griffiths and Hughes (2010)
found evidence that minima hitchhikers act in a leaf cleansing role, observing hitchhikers riding
longer on contaminant-treated loads and fewer fungal contaminants after hitchhikers had access
to a load. However, another important theory is that hitchhiking behavior primarily evolved in
defense against parasitoid phorid flies which lay eggs in the ant body (Hölldobler and Wilson
1990; Feener and Moss 1990; Orr 1992). The load carrier holding the leaf fragment in its
mandibles cannot defend itself from harassing parasitoids and benefits from the protection
provided by the hitchhiker. Feener and Moss (1990) conclude that the role of hitchhikers is to
defend ant workers from phorid flies and that the presence of the flies can result in an increase in
hitchhiking behavior by the minima caste of ants (see also Braganca et al. 1998). It stands to
reason that the absence of the flies (which may not be able to fly in windy conditions) could
result in a decrease in hitchhiking behavior.
Hypotheses
The focus of this study is the abiotic factor of wind. Wind and rain are common
occurrences in the tropics and have consequences for ants foraging in tree canopies, potentially
limiting the area and mass (respectively) of loads foragers cut and transport (Rudolph and
9
Loudon 1986). Attines carry loads several times their own body size and run a risk of falling
large distances from trees to the ground or of losing their balance when walking on the ground
(Moll et al. 2010), but foragers should cut the maximal load that still permits stability while
walking. To maximize resource input rate to the nest in windy conditions, foragers could cut
smaller loads to maintain a stable walking course and minimize energy expenditure against wind
resistance. I tested the hypothesis that variation in wind speed is correlated with the size of leaf
fragments carried or the size of foragers recruited to the foraging site.
During initial observations, I noticed a marked absence of hitchhikers on leaf loads in
windy conditions, so I also examined the effects of wind on the prevalence of hitchhikers riding
on leaf fragments. The second goal of this study was to determine if hitchhiker density decreases
in windy conditions.
Materials and Methods
I conducted this study at La Selva Biological Station, Heredia Province, Costa Rica in
June and July 2012 and January 2014. La Selva Biological station is located in the Northeastern
lowlands of Costa Rica in premontane wet forest and disturbed lands, receiving an average of 4
m rainfall per year. The focal colonies in this study were well established and large colonies
with heavy foraging patterns on leaf sources. The focal colonies foraged nocturnally, and I ran
trials between 1400 and 2000 h each night on three A. cephalotes leaf-cutter nests in a short grass
clearing, each separated by at least 50 m. Peak foraging occurred around 1730 h each night.
A. cephalotes is a good model for load size selection because individuals usually carry
the load that they cut and must carry that burden back to the nest (Hubbell et al. 1980). The
round trip journey to a resource can last for several hours in A. cephalotes (Lewis et al. 1974),
10
and mature colonies contain millions of individuals (Weber 1972, Hölldobler and Wilson 1990)
with thousands out foraging at any given time (Fowler and Saes 1986), therefore it is unlikely I
sampled the same individual more than once in the same night. Prior observers document A.
cephalotes workers passing leaf fragments from one individual to another (task partitioning)
(Hubbell et al. 1980), but I found no evidence for leaf transfer in my observations and set
experimental methodology to avoid this problem.
A. cephalotes colonies may harvest leaves from the same tree for weeks (Burd 2000), and
I used only vegetation sources that the colonies were actively foraging (Myrtaceae: Psidium
friedrichstalianum and Hamelia patens). Leaf-cutter colonies can forage from multiple trees at
once, so I controlled for potential differences in intraspecific leaf density by collecting treatment
leaves from the same tree (Cherrett 1972; Rudolph and Loudon 1986). To control for any
individual differences in leaf density between leaves from the same tree, I chose leaves at the
same height and approximate age by focusing on young and tender leaves with similar light
green coloration, however, other studies concluded that A. cephalotes do not cut smaller
fragments from denser leaves regardless of body size (Wetterer 1990, 1994). Leaves with higher
fungal contaminant loads are found lower in the canopy, and Atta prefer low fungal load leaves
(Griffiths and Hughes 2010). I collected all treatment leaves from about 5 m from the ground in
the canopy, which is the height at which leaf-cutter foragers began foraging in a study with A.
colombica (Griffiths and Hughes 2010). Sampling leaves higher in the canopy assumes low
fungal loads on the treatment leaves used in this study which controls for possible effects of
fungal contaminants on hitchhiker or forager behavior.
For each trial, I collected a branch from a focal tree to pull off leaves as they were needed
and avoid desiccation before forager cutting. I pinned three of the collected leaves together on
11
each side of the trail 1.5 m from the nest entrance. By placing leaves on the trail edge, I avoided
introducing any obstacles directly onto the foraging trail that could alter foraging behavior
(Dussutour 2009b).
I fixed wind treatments perpendicular to the foraging trail with a desk fan situated 1.5 m
away from the nest entrance. Using a Kestrel 1000 anemometer to calibrate wind speed, I
recorded data at wind speeds of 0, 1.3, and 2.0 m/s. A 30 min acclimation period with the fan
running allowed the ants to adjust to the treatment and helped avoid effects of plastic load size
selection in the initial recruitment phase to the resource (Roces and Nuñez 1993; Roces and
Hölldobler 1994; Bollazzi and Roces 2011). A scarf prevented disturbance of the ants with my
breath.
Using forceps, I collected leaf fragments the ants harvested from the leaf piles. I only
collected leaf fragments from foragers I saw finish their last cut to ensure that the leaf loads were
from the leaf pile I provided and not from another foraging source or cut by another individual
(task partitioning). Additionally, I did not collect fragments from ants climbing down tree trunks
to eliminate any potential for task partitioning. The shape of the fragment cut can determine
cutting time (e.g. a circular interior cut or a semicircular edge cut) (Wetterer 1990), so I collected
both but not cuts that included leaf mid-veins, which may be heavier and more difficult to cut.
When treatment leaves were 75% depleted, I replaced them with previously uncut leaves of
similar size pulled from the sample branch. It is likely that my removal of leaf loads from
foragers or foragers themselves had little to no effect on recruitment in this study. Burd (2000)
removed leaf-cutter ants and their loads for the first 2 h of trials and found no effect on normal
traffic conditions; the researchers concluded the absence of laden ants had no effect on
recruitment.
12
After collecting freshly-cut leaf fragments from foragers, I placed the leaf fragments into
a plastic bag for later measurement. I collected 2012 samples in 30 min increments to avoid the
loss of mass from desiccation, which can be considerable. In 2014, I placed each sample in a
separate 1.5 mL Eppendorf tube along with the ant carrying it and recorded the time for each
sample. Image J software (v.1.45.s) calculated the surface area for each leaf fragment to the
nearest 10-4 cm2 and ant morphometrics to the nearest 10-3 cm (head width, pronotal width, and
metathoracic leg length (Rasband 1997-2011). I used head width as the best variable to represent
ant size as it best correlated with fragment size, and measured as the widest length when viewed
dorsally (Wilson 1980a, b). Metathoracic leg length was poorly correlated with head width, as
many workers were missing entire segments of tarsi on the rear legs. Each time I collected a leaf
fragment, I tallied the number of hitchhikers holding on during that 30 min interval, then divided
that count by the number of leaves collected during the interval to get the average number of
hitchhikers per leaf fragment in each interval (for 2012), or I recorded the number of hitchhikers
riding on each leaf fragment (for 2014). If an ant dropped a leaf fragment after cutting, I did not
record that sample. To record traffic density, I took pictures of the foraging trail and a meter
tape with a digital camera and later recorded the number of ants per cm2. After every third
interval (in 2012), I weighed the leaf fragments to the nearest 10-4 g for each time interval and
photographed them. The weight allowed me to obtain the average mass of each fragment per
time period. In 2014, I photographed each leaf fragment and the dry weight of the ant that
carried it to the nearest 10-4 g. I recalibrated the scale after every five measurements. I did not
weigh leaf fragments because of variability caused by desiccation at different time lengths.
13
I analyzed the data using R statistical software program (R ver. 2.15.1). To examine
whether load size changes in response to forager size, wind speed, or type of leaf harvested (leaf
toughness/density), I used a linear model comparison approach modeling leaf fragment size on
forager head width, wind treatment, leaf type, and their interactions. To examine if larger ants
recruit to windy sites or tougher leaves, I used a linear model comparison approach modeling
head width by wind treatment, leaf type, and their interactions. To check for normality in the
hitchhiker data, I performed a Shapiro-Wilk normality test (W = 0.87, P = 9.9e-05). Taking into
account the non-normality of the data, I conducted a non-parametric Kruskal-Wallis rank sum
test on the average number of hitchhikers per time interval modeled by wind treatment to
examine effects of wind on hitchhiker prevalence. To test whether load selection behavior
changes in relation to traffic congestion on the foraging trail, I conducted a Pearson’s ProductMoment Correlation examining the degree of linear association between the log of traffic density
on the foraging trail and leaf fragment mean weight per time interval.
Results
In examining whether foragers cut different sized leaf fragment loads in windy conditions
I found evidence that leaf-cutter ants cut larger leaf fragments as wind speed increased (F1,513 =
6.67, P = 0.01) (Fig 1). This was contrary to my original predictions that foragers would
minimize resistance and cut smaller loads. Leaf fragments were significantly larger in the 2.0
m/s wind treatment than with no wind (Tukey HSD test, Padj = 0.03). In the treatment with no
wind, I collected 236 leaf fragments with a surface area of 1.40 ± 0.03 cm2 (mean ± SE) from
ants foraging on the leaf pile. In the 1.3 m/s wind treatment, I collected 189 leaf fragments with
14
a surface area of 1.47 ± 0.036 cm2 (mean ± SE). In the 2.0 m/s wind treatment, I collected 90
leaf fragments with a surface area of 1.56 ± 0.073 cm2 (mean ± SE).
Fig 1 Bar plot showing mean leaf fragment area across wind treatments of 0, 1.3, and 2.0 m/s
(n=236, n=189, n=90 leaf fragments, respectively) for 2012 data. Different lower case letters
represent significantly different pairwise comparisons
I did not find significant evidence for a simple effect that larger workers cut larger leaves
(F1.132 = 1.73, P = 0.20) (Fig 2), and I found no evidence for the simple effect that larger workers
recruit to windy sites (F1, 137 = -0.03, P = 0.85) (Fig 3). There was a significant interaction
between head width and wind treatment predicting fragment size (F1, 132 = 6.45, P = 0.012) (Fig
4). There is a stronger relationship between forager size and leaf fragment size in windy
conditions compared to no wind conditions (control). Larger ants cut larger leaves, but more so
when wind is present.
15
Y = 0.76 + 2.7X
Fig 2 Regression plot with lne of best fit showing the relationship between forager head width
and fragment area (n = 140 ants and fragments)
Fig 3 Box plot showing that wind treatment does not affect the size of the foragers cutting at that
site (n = 70 no wind, n = 70 with wind). Boxes contain the interquartile data, whiskers indicate
maximum and minimum values, and dots represent extreme values
16
Fig 4 Regression plot with lines of best fit showing the interaction between forager head width
and leaf fragment size cut in wind and no wind treatments. Black dots and line indicate wind
treatments and gray dots and line indicate no wind treatments
Fewer hitchhikers rode on the leaf fragments as wind speed increased (X2 = 14.9, df = 2,
P = 0.0006) (Fig 5). A Wilcoxon rank-sum pairwise comparison test with Holm adjusted pvalues revealed that there were fewer hitchhikers present in the 1.3 m/s wind treatment compared
with no wind treatments (Padj = 0.03), and there were fewer hitchhikers present in the 2.0 m/s
wind treatment compared with no wind treatments (Padj = 0.0009). In each treatment, I counted
the number of hitchhikers on collected leaf fragments for each 30 min interval. With no wind,
1.70 ± 0.25 (mean ± SE) ants hitchhiked per leaf fragment over 17 intervals. In the 1.3 m/s
treatment 0.84 ± 0.22 (mean ± SE) hitchhikers were found per leaf fragment over 15 intervals,
and in the 2.0 m/s treatment, 0.46 ± 0.23 (mean ± SE) ants hitchhiked per leaf fragment over 15
intervals.
17
Fig 5 Box plot indicating median number of hitchhikers per fragment across time intervals and
wind treatments of 0, 1.3, and 2.0 m/s (n=17, n=15, n=15 time intervals, respectively) for 2012
data. Boxes contain the interquartile data, whiskers indicate maximum and minimum values, and
dots represent extreme values. Different lower case letters represent significantly different
pairwise comparisons
When I tested for a behavioral response to differences in traffic congestion in this study,
there was no evidence for a correlation between traffic density on the foraging trail and leaf
fragment weight (F1,15 = -1.68, P = 0.21) (Fig 6). Similarly, examining for evidence of change in
leaf fragment size due to congestion on the foraging trail, there was no correlation between
traffic density and leaf fragment size (F1,15 = -0.04, P = 0.84).
18
Fig 6 Scatter plot of log traffic density on the foraging trail with mean weight per leaf fragment
per time interval (test of the Truck Driver Effect) (n=18)
Differences in leaf density/toughness between the two forage tree species in this study
did not affect the size of the leaf fragment cut (F1,132 = -0.06, P = 0.80) (Fig 7) but did effect the
size of the workers that recruited to the cutting surface (F1,136 = -6.18, P = 0.01) (Fig 8). There
was no difference between the size of leaf fragments cut when 2012 and 2014 sampling seasons
were compared (F1, 653 = 0.06, P = 0.80).
19
Fig 7 Box plot showing that leaf density/toughness did not affect the size of the fragment cut (n
= 73 for cas, n = 65 for coralillo). Cas tree leaves are more dense and tough than coralillo tree
leaves. Boxes contain the interquartile data, whiskers indicate maximum and minimum
interquartile values, and dots represent extreme values
Fig 8 Box plot showing that leaf density/toughness did affect the size of the ant recruited to cut
(n = 73 for cas, n = 65 for coralillo). Boxes contain the interquartile data, whiskers indicate
maximum and minimum interquartile values, and dots represent extreme values
20
Discussion
I explored how local conditions on the foraging trail affect behavior in A. cephalotes leafcutter workers. Leaf-cutter ants alter behavior as local conditions vary. A. cephalotes leaf-cutter
ant foragers and hitchhikers exhibit behavioral plasticity in response to wind conditions on the
foraging trail. Contrary to my original prediction that foragers would cut smaller fragments in
wind, I found that foragers cut larger area leaf loads in wind than without wind, controlling for
ant size. The second finding of this study is that few minima hitchhike on leaf fragment loads
carried by foragers in windy conditions. Lastly, I expected A. cephalotes foragers to cut smaller
leaves as traffic density increased throughout the foraging cycle. In contrast with previous
studies, I did not detect that leaf fragment mass or size is affected as traffic density on the
foraging trail increases.
Much evidence exists for instances in which leaf-cutter ants cut smaller loads than
maximally possible, yet I found an instance where leaf-cutter foragers cut loads larger than
normal. A possible explanation for larger leaf fragment size in windy conditions is that foragers
may offset the added mass of hitchhikers when there is less wind by cutting smaller loads.
Phorid flies locate their hosts using receptors sensitive to ant volatile pheromones (Feener et al.
1996), and wind likely prevents parasitic phorid flies from locating hosts by displacing volatile
pheromone signals in the air. In the absence of parasitoid enemies foragers are free to cut larger
loads because vulnerability to parasitism is not a factor, hitchhikers are not needed for defense,
and foragers anticipate the non-recruitment and added mass of hitchhikers and subsequently cut a
larger load. Foragers would need to change the load size selection prior to potential hitchhiker
recruitment. Or, foragers could directly cue in to the absence of parasitoid phorid flies in windy
conditions. The presence or absence of parasitoids near the foraging trail can have a substantial
21
impact on daily foraging activity. One ovipositing female phorid fly can alter the behavior of
hundreds of ant workers if they are aware of her presence (Feener and Brown 1992; Orr et al.
1995; Porter et al. 1995).
The link between wind and rain may offer another explanation for larger load sizes cut by
foragers in wind. Leaf-cutter ants drop their loads at the onset of rain abandoning them on the
trail to quickly run back to the nest for cover (Rudolph and Loudon 1986, personal observations).
Wind may offer a warning to foragers that their trip will soon be cancelled because of bad
weather. It is possible that in order to maximize their final effort until the rain stops, ants may
cut one last large load when they sense wind, which is usually a precursor to rain (Lewis et al.
1974). Foragers may attempt to maximize their resource delivery for the last load of a foraging
cycle by cutting the largest load they can to offset the cost of idly waiting in the nest for adverse
conditions to cease. Future studies should examine individual foragers throughout a foraging
cycle and track load size selection to see if foragers cut the larger fragments for their last trip of a
foraging cycle.
Evidence in this study showed a stronger relationship between forager size and leaf
fragment size in windy conditions compared to no wind conditions (control), and larger ants cut
larger leaves, but more so in wind. It may be that size matching of a carrier to its load is less
variable in windy conditions than when no wind is present to maintain stability.
The decrease in hitchhikers riding on loads carried by foragers in windy conditions was
obvious by casual observation. Windy conditions may dampen or completely obscure signals
needed to recruit hitchhikers to leaf fragment loads. Hitchhiking minima of A. cephalotes are
likely attracted to leaf laden workers through stridulation that transfers through the ant’s head
into the substrate (Roces and Hölldobler 1995). Foragers tend to mill around on the cutting
22
surface, antennating sisters engaged in cutting and searching for a suitable place to begin cutting
their own fragment (personal observation). Minima workers milling around on a leaf are
possibly searching for a fragment to board. The fewer number of hitchhikers found on leaf loads
in wind treatments may result from the “noise” caused by the leaf fragment shaking in the wind,
obscuring the vibratory hitchhiker recruitment signal. Therefore, hitchhikers may not be
receiving the stimulus needed to board a freshly cut leaf fragment. It is intriguing that some
wind would render the primary function of hitchhikers useless resulting in a waste of effort and
energy travelling to and from a resource.
I conducted this study over two sampling efforts, and the sampling methods differed
between the two differed in some important aspects. There was no difference in leaf fragment
areas comparing 2012 and 2014 sampling seasons, but extreme values in 2012 for the larger
fragments cut in wind treatments may be an artifact of unmeasured variables. In 2014, I
calibrated wind speed using the same fan from the 2012 study based upon previous settings
including distance and angle from the trail, compared to anemometer calibration of wind speed
in 2012. In 2012, I displaced carriers from their loads without removing them from the foraging
trail, while in 2014 I collected carriers and their loads without returning them to the foraging
trail. Either sampling method could have an effect on nestmate interactions including recruiting,
but the method used in 2014 allowed me to obtain needed data on forager size and load
matching.
Maximum biomass transport rate may result more from the shape of the forage than the
mass or density in leaf-cutter systems. Forage load size and shape affects the collector’s cutting
effort, the transporter’s walking effort and ability to fit inside the nest entrance and chambers,
and the minima gardener’s processing effort required to mince, regurgitate and inoculate the
23
fungal garden. Rudolph and Loudon (1986) and other researchers found that ant mass is more
correlated with leaf fragment mass than area, but it is likely that fragments are selected for area
as well as mass because of constraints caused by maneuverability. Moll et al. (2010) showed
that the shape of a fragment, not its mass, has more of an effect on running speed in Atta
vollenweiden grass cutter ants. Longer grass fragments were more metabolically costly to
transport (as a measure of CO2 production) and slowed the carriers, and heavier loads did not
slow workers but still held a higher metabolic cost. Atta cephalotes carry round or semicircular
leaf fragments, not long grass blades, but Moll et al. (2010) point to the importance of size and
shape in load size selection in the Attini.
Farji-Brener et al. (2011) found that highly laden ants walk slowly and decrease the
walking speed of nest-mates behind them, similar to a large truck moving slowly on a highway
(the Truck Driver Effect). At high traffic densities, the proportion of A. cephalotes ants carrying
heavy loads decreases (Farji-Brener et al. 2011). Ants that would normally carry a heavy load
choose a lighter load to avoid slowing down nest-mates. Farji-Brener et al. (2011) showed that
traffic density mechanisms result in A. cephalotes workers adjusting foraging behavior to
regulate tissue transfer to the nest. I found no evidence for the Truck Driver Effect in this study.
Central-place foragers balance costs and benefits in the context of their local environment
on the foraging trail and plant surfaces to maximize resource allocation to the colony. If we
consider the nest interior as an added component of local environment, load size selection
becomes more complicated. Burd and Howard (2005b) found a strong main effect for garden
chamber size in their model with smaller chambers producing a negative feedback cue on
foraging. They felt that smaller chambers are more likely to exist naturally because smaller
chambers have a higher surface area to volume ratio and are better ventilated for CO2 removal
24
than larger chambers. They postulate that smaller leaf fragments might be transported to more
distal garden chambers, and that larger fragments are deposited closer to the nest entrance, so it
may be that substrate need in different chambers may have an effect on load size, as well.
Perhaps larger proximal chambers are left empty for events when foragers cut larger loads than
normal, such as wind. Future work could empirically examine for evidence of differential filling
in different sized garden chambers under varied experimental conditions and probe for feedback
effects of chamber capacities on forager load size selection.
Conclusion
It is clear that leaf-cutter ants regulate their foraging effort based upon foraging context,
and this study adds to our knowledge of resource allocation in central-place foraging systems. It
is unclear why foragers cut larger than average leaf loads in wind, and future studies should
examine flight potential of phorid flies and hitchhiker behavior in the presence and absence of
parasitoids. More work needs to be done on the ability of phorid flies to effectively fly, locate,
and oviposit eggs in windy conditions. Information of this type could be used to enhance
biocontrol release efforts of phorid flies in the United States to combat the invasive Solenopsis
fire ant infestation by timing parasitoid release during non-windy times of the year (Calcott et al
2011). In the Neotropics, leaf-cutter ant pests remove more vegetation than any other animal
group (Cherrett 1986; Hölldobler and Wilson 1990). Research into effects of wind on phorid
success and leaf-cutter vigilance may aid in biocontrol of leaf-cutter ant agricultural pests
throughout the Neotropics.
Insights into traffic patterns, load delivery, and wind resistance in ants may help
engineers and city planners determine ways to structure dense communities maximizing
25
efficiency (Burd 2002). For example, when leaf-cutter foragers on the trail are at a 50:50 laden
to unladen ratio, traffic flows more smoothly (Burd et al. 2002). We use dedicated lanes in our
highway system, but we should look to evolutionary solutions already present in the world to
help inform our decisions that shape our future.
26
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