Absence of Polar ity in Trail Pheromones and Use of Sun Compass Orientation In Leafcutter Ants Atta cephalotes 1 Marc A. Bli ss Department of Biology, Northeastern University, Boston, Massachusetts 02115 U.S.A ABSTRACT THE COMPLEX SOCIAL SYSTEM of leafcutter ants, Atta cephalotes (Formicidae) requires a high degree of organization and efficiency to ensure the survival of the colony. This suggests that communication between individual s is both common and intricate, especia lly during the complicat ed foraging process Chemical signaling is employed by returning, laden ants along foraging trails This study tested for the presence of polar properties within these trail pheromones to convey orientation cues to workers. Using manipulated foraging trail s of a single colony in San Luis, Costa Rica I observed individual ant behavior at different times of day Rather than finding a correlation between ant direction and pheromone direction, A.cephalotes demonstrated a compass like ability to navigate in vectors to their colony using the sun for navigation. These results indicate that a complicated navigation system in leafcutter ants, A. cephalotes has developed using light to determine relative positio n in space. RESUMEN EL COMPLEJO SISTEMA SOCIAL de las zompopas, Atta cephalotes (Formicidae) requiere un alto grado de organizacin y eficiencia para asegurar la sobrevivencia de la colonia. Esto sugiere que la comunicacin de individuos es comn e intrincado, especialmente durante el proceso de forrajeo. Seales qumicas son utilizadas por las hormigas a lo largo del sendero de forrajeo. Este estudio prueba la presencia de propiedades polares dentro de estos senderos de feromonas para transmitir pistas a las obreras. Usando senderos de forrajeo manipulados en una nica colonia de zompopas en San Luis, Costa Rica, observe el comportamiento de las hormigas a diferentes horas del da. En lugar de encontrar correlacin entre la direccin de la hormi ga y la direccin de la feromona, A. cephalotes muestra una habilidad similar a la brjula para navegar hacia la colonia, usando el sol para este fin. Estos resultados indican que existe un complicado sistema de navegacin en zompopas, A. cephalotes utili za la luz para determinar la posicin relativa en el espacio. INTRODUCTION WITH COLONIES NUMBERING MILLION S OF INDIVIDUALS leafcutter ants, Atta cephalotes (Formicidae) are the dominant herbivore of the Neotropics ( Fowler et al 1986 Hlldobler & Wilson 1990). C olony function of A. cephalotes has widely been studied by entomologists as they must rely on highly organized systems to ensure the efficiency and survival of the massive groups in which they live ( Farji Brener et al 2010) Division of labor, allocation of resources, and recruitment communication are examples of such systems. During foraging, ants may travel up to 300 m from the nes t, suggesting a need for a well developed means of navigation (Farji Brener et al 2010). In ant species, navigation mechanisms can exist in a number of different forms including p hysical cues ( head on antennation), spatial directional cues (tandem running) and chemical indicators ( Farji Brener 2010, Planque et al. 2010 ).
Having one single foraging column of both nest bound and food bound ants allows returning Atta foragers to lay trail pheromones as signals to the other ants on the path indicating food availability and quality (Roces 2002). These trail pheromones, composed of the molecules methyl 4 methyl pyrrole 2 carboxylate and 3 ethyl 2,5methylpyrazine are secreted from abdominal glands of the ants ( Hlldobler & Wilson 1990). The abdomens are then dragged along the trail surface in a nest bound direction, spreading chem ical cues to nearby nestmates. Ma ny of the properties of these pheromones are known to researchers, but others have been disputed. For instance, it has been postulated that A. cephalotes may be capable of alternating these chemicals to create polar indicators of dire ctionality along the f oraging trail (Viela et al. 1987). In many ant species trail pheromones are used solely for this type of orientation (Plaque et al. 2003), but other studies have indicated that the trail chemicals in A.cephalotes give no directional cues at all ( Viela et al 1987, We t terer et al 1992 ) and suggest that these pheromones are instead used in recruitment communication, the process by which social insects enlist the aid of nestmates to complete a task ( Jaffe 1979). If true, additional factors must be used for navigation of A. cephalotes during foraging. This field study investigated whether trail pheromones provide directional cues in foraging A. cephalotes ants. Based on the complex chemical signals required to orchestrate foraging in a complex social system I expect ed trail pheromones of A. cephalotes to exhibit polar properties indicating a nest bound direction and an anti n est direction. It may also be possible that abiotic cues influence ant orientation either in place of or in addition to chemical trails However, with abiotic conditions being inconsistent, this seemed unlikely. Relying on factors beyond the use of pheromonal signaling may be detrimental to colony efficiency. METHODS This study was conducted between October and November, 2010, in the premonta ne wet forest of Altos de San Luis, Puntaranas, Costa Rica The study site comprised a single Atta cephalotes nest, located in a secondary forest fragment at 1100 meters above sea level on the farm of Xinia Leitn Araya Investigation 1: Day Dayt ime trials were conducted betw een 07 30 and 12 40 on tw o neighboring foragi ng trails. Both of these trails were relatively flat as to reduce visual or spatial orientation cues from prominent topographical features Approximately 3 m from the nest entrance, a piece of paper measuring 33 cm x 21.6 cm, was placed lengthwise to collect trail pheromones Pieces of wood and leaf litter were placed along lengthwise edges to keep the paper in place and to discourage the ants from going around or treating the paper a s a trail obstruction Sufficient time was allotted for returning ants to establish a pheromone trail across the paper (2 hours at the start of a new trial or 30 mi nutes between sampling efforts). T he paper was then marked to indicate its initial orientation removed from the foraging trail, and transferred ~1 m to the side of its original position on the trail. Wooden blinders were added to the sides of the paper to reduce visual cu es for ant navi gation to ensure isolation of chemical cues in the trail pheromones. Nest bound, laden ants were individually sampled from trails. The ants, which comprised a single media subcaste were manipulated with forceps by leaf fragment s to avoid an alarm response Ants were transferred to the center of the pap er and placed perpendicular to the pheromone trail, It was presumed that navigation behavior of inbound, l aden ants was an attempt to reach the nest entrance. Upon reaching an edge of the paper the direction of the ant was
recorded both in terms of physical bearing (compass direction) and direction in relation to the pheromones (toward or away from nest) O rientation of the paper was reversed after the first 10 ants such that the pheromones were rotated 180 and 10 additional ants were observed. In total, 500 individuals were sampled and ants were never observed more than once. Investigation 2: Night Night trials made use of the same foraging trails and methodologies as the daytime investigation but were conducted between 1830 and 20 40 in the absence of sunlight. Again I sampled a total of 500 ind ividuals. RESULTS Investigation 1: Day The direction traveled by the nest bound ants varied significantly from the chemical direction of trail pheromones ( 2 = 62625.25 df = 1, P < 0.0 0 01) In fact, nearly as many individuals followed the pheromones in the expected nest bound chemical direction (N = 249) as those travelling chemically away from the nest (N = 2 51 ; Fig. 1 ). At first glance this data appears to illustrate a random distribution, however is more easily explained by analyzing navigation in terms of compass direction. There was a very strong relationship between ant direction and the physical direction of the nest ( 2 = 434.312, df = 1, P < 0.0001) Roughly 96 % of returning ants continued in the physical compass direction of the nest regardless of paper orientation (Fig. 2) This pattern held for each of the two foraging trails (Table 1). FIGURE 1. Percentage of ants that moved toward and away from nes t in relation to paper/pheromone orientation during day and night investigations. The number over each bar represents the number of individuals that traveled in each chemical direction, independent of physical compass direction. 249 270 251 230 0 20 40 60 80 100 Day Night Percent (%) Investigation To Nest Polarity Anti Nest Polarity
FIGURE 2: Percentage o f all ant responses in terms of physical direction for both day and night investigations. The number over each bar represents the number of individuals that traveled in each compass direction, independent of paper orientation. In total, 18 ants (3.6%; F ig. 2) travelled in directions away from the colony direction. Among that group, there was no trend in pheromonal direction ( 2 = 0.058, df = 1, P = 0.808). Only half of the individuals that moved physically away from the nest (9 ants) did so with pheromones in the reversed orientation, implying that the pattern was due to chance. Investigation 2: Night The behaviors observed in night investigation varied from those displayed during the day There remained a significant difference between paper/ pheromone orientation and actual ant behavior ( 2 = 52546.1, df = 1, P < 0.0001). Again, there appeared to be an even distribution between nest bound pheromone direction (54%) and anti nest pheromone direction (46%; Fig. 1). However, in this investigation equal occurrences of pheromone direction responses was not the result of a single compass direction preference, as it was in Investigation 1. During the night, the ants showed no clear preference fo r any direction ( 2 = 2.312, df = 1, P = 0.128 ; Fig. 2, Table 1 ). The number of individuals that travelled in a nest bound physical direction ( N = 267 or 53.4%) was only marginally higher than those that travelled physically away from the nest (N = 233 or 46.6%) On the first trail, 53.2% of ants navigated toward the nest, while 46.8% navigated in the opposite direction. Very similar proportions occurred on the second trail with 53.6% of sampled individuals navigating in the nest direction and 46.4% travelling westward, away from the colony. 482 267 18 233 0 20 40 60 80 100 Day Night Percent(%) Investigation To Nest Away From Nest
TABLE 1: Distribution of responses by Atta cephalotes individuals in relation to physical direction. This data is divided to show the relative number and percentage for each foraging trail. Foraging Trail 1 Foraging Trail 2 Investigation # to nest % to nest # away % away # to nest % to nest #away % away Day 252 96.7 8 3.3 230 95.8 10 4.2 Night 117 53.2 103 46.8 150 53.6 130 46.4 Additional Observations When removed from the foraging trail, ants rarely let go of leaf fragments in their mandibles. Upon transference to the paper, they often paused and circled several times before going in one direction However, in the event that a fragment was dropped, the resulting behavior was often spastic and rapid movement to an arbitrary side of the paper. The se alarm responses highlight the differences of slower, more deliberate paths of navigating foragers. In the absence of trail pheromones, such as on a clean sheet of paper, this circling, searching behavior is a much longer process and ant direction is see mingly random. DISCUSSION The results of these investigations provide several insights into the role of trail pheromones and the orientation and nest bound navigation of A. cephalotes Paper/pheromone orientation appeared to have no influence on ant nav igation, day or night, indicating that the trail chemicals contain no directional cues. During the day, the an ts demonstrated a clear ability to navigate in the direction of the nest independent of pheromone direction. This trend further supports the idea that trail pheromones are nonpolar and suggests that A. cephalotes relies on a separate cue for navigation. A lack of orientation cues in trail pheromones does not mean these chemicals are unimportant in foraging. They play an important role in col ony efficiency and recruitment. Other studies have shown that the abundance of t rail pheromone l aid down by a single ant is proportional to both the quality of the food source being collected and the speed of outbound recruited foragers ( Hlldobler & Wils on 1990, Roces 2002). This behavior i nitiates a positive feedback loop as recruits lay their own recruiting chemicals, again increasing foraging efficiency of the colony ( P lanque et al. 2010 ). T he ant s were able to navigate in the absence of chemical indicators and isolated from biological communication such as head on antennations or tandem running. This begs the question of what other cues the ants were using to orient themselves. Studies have shown that such factors as olfactory indicators (Wetterer et al. 1992) an d magnetic field cues (Banks & Srygley 2003) may be used by Atta species for navigation. However, due to the inconsistency of wind patterns, including days in this study where wind was part icularly strong, I do not believe that olfactory cues were being used for navigation. Likewise, the reduction in ants ability to field. In this study, the drastic change between the ants ability to navigate during the day and night indicates that they are using the sun to locate their nest. This ability, often referred to as
sun compass orientation has been demonstrated in a variety of insects, including other spec ies within Atta and of a related leafcutter genus, Acromyrmex ( Hlldobler & Wilson 1990). Directional patterns between the two foraging trails closely m irrored one another in each of the two investigations This result implies that the ants were not simply walking toward the s position, but rather, have developed a complex lea r ning mechanism for navigation. The ants are not relying on proprioceptive information garnered along the trail If that were the case with these ants, they would become easily disoriented after being lifted and removed from the trail Instead, A. cephalotes demonstrate the use of a geocentric navigation system, in which they derive their own position in space or that of the nest from any nearby position, including adja cent foraging trails (Banks & Srygley 2003). From an evolutionary standpoint, this learning behavior is even more impressive than the use of intricate chemical signaling. It demonstrates incredible neurological functioning. Rather than viewing ants as mind less drones of a superorganism, we must reconsider the value of an individual. ACKNOWLED GEMENTS I would like first and foremost, to express my appre ciation to Anjali Kumar for her patience and continued support, both academically and emotionally throughout the duration of this study. To Xinia Leit n Araya and family for welcoming me into their home and the use of their land Thank you to Moncho Calder n for helping me acquire necessary supplies, and to Ben jamin Hedin for his assistance in the field despite territorial ruminants and the possibility of pumas as well as his constant camaraderie over wild lemons and guavas. LITERATURE CITED Banks, Alexander, N. and R.B Srygley. 2003. Orientation by Magnetic Field in Leafcutter Ants, Atta colombica (Hymenoptera: Formicidae). Ethology. 109: 835 846. Farji Brener, Alejandro G., G. Barrantes, O. Laverde, K. Fierro Calder n, F. Bascop, and Adriana Lpez. 2007. Fallen Branches as Part of Leaf Cutting Ant Trails: Their Role in Resource Discovery and Leaf Transport Rates in Atta cephalotes. Biotropica. 39(2): 211 215 Farji Brener, A.G., S. Amador Vargas, F. Chinchilla, S. Escobar, S. Cabrera, M.I. Herrera, an d C. Sandoval. 2010. Information transfer in head on encounters between leaf cutting ant workers: food, trail condition or orientation cues? Animal Behavior 79: 343 349. Fowler, H., V. Pereira da Silva, L. Forti, and N. Saes. 1986. Population dynamics of leaf cutting ants: a brief review. In: Fire Ants and Leaf Cutting Ants: Biology and Management (Ed. by C. S. Logfren & R. K. Vander Meer), pp. 123 145. Westview Press Boulder, Colorado. Hlldobler, B. AND E.O. Wilson. The Ants Cambridge: Belknap Press of Harvard University Press 1990. pp. 596 608 Print Jaffe, K. M. Bazirjz B ena zet, and P. E. Howse 1979. An Integumentary Pheromone Secreting G land in Atta sp : Territorial Marking with a Colony Specific Pheromones in Atta cephalotes. Insect Physiology. 25: 833 839. Planque Robert, J. Bouwe van den Berg and Nigel R. Franks 2010. Recruitment Strategies and Colony Size in Ants. PLoS ONE 5(8): e11664. doi:10.1371/journal.pone.0011664 Roces, Flavio. 2002. Individual Complexity and Self Organization in Fo raging by Leaf Cutting Ants. Biology Bulletin. 202: 306 313. Vilela, E., Jaffe K. & Howse, P. 1987. Orientation in leaf cutting ants (Formicidae: Attini). Animal Behaviour, 35, 1443 1453. Wetterer, J., Shafir, S., Morrison, L., Lips, K., Gilbert, G., C ipollini, M. & Blaney, C. 1992. On and off trail orientation in the leaf cutting ant, Atta cephalotes (L.) (Hymenoptera: Formicidae). Journal of Kansas Entomological Society, 65, 96 98.
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Ausencia de polaridad en las feromonas y el uso de la brjula de orientacin en las hormigas zompopas (Atta cephalotes)
Absence of polarity in trail pheromones and use of sun-compass orientation in leafcutter ants Atta cephalotes
The complex social system of leafcutter ants, Atta cephalotes (Formicidae) requires a high degree of organization and efficiency to ensure the survival of the colony. This suggests that communication between individuals is both common and intricate, especially during the complicated foraging process. Chemical signaling is employed by returning, laden ants along foraging trails. This study tested for the presence of polar properties within these trail pheromones to convey orientation cues to workers. Using manipulated foraging trails of a single colony in San Luis, Costa Rica, I observed individual ant behavior at different times of day. Rather than finding a correlation
between ant direction and pheromone direction, A.cephalotes demonstrated a compass-like ability to navigate in vectors to their colony using the sun for navigation. These results indicate that a complicated navigation system in leafcutter ants, A. cephalotes has developed using light to determine relative position in space.
El sistema social complejo de las zompopas, Atta cephalotes (Formicidae) requiere de un alto grado de organizacin y eficiencia para asegurar la sobrevivencia de la colonia. Esto sugiere que la comunicacin entre individuos es comn e intrincado, especialmente durante el proceso de forrajeo. Las seales qumicas son utilizadas por las hormigas a lo largo del sendero de forrajeo. Este estudio prueba la presencia de propiedades polares dentro de estos senderos de feromonas para transmitir seales de orientacin a las obreras. Usando los senderos manipulados de forrajeo manipulados en una nica colonia de zompopas en San Luis, Costa Rica, observe el comportamiento de las hormigas a diferentes horas del da. En lugar de encontrar una correlacin entre la direccin de la hormiga y la direccin de la feromona, A. cephalotes muestra una habilidad similar a la brjula para navegar hacia la colonia, usando el sol para este fin. Estos resultados indican que existe un complicado sistema de navegacin en zompopas, A. cephalotes utiliza la luz para determinar la posicin relativa en el espacio.
Text in English.
Costa Rica--Puntarenas--Monteverde Zone--San Luis
Costa Rica--Puntarenas--Zona de Monteverde--San Luis
Tropical Ecology Fall 2010
Ecologa Tropical Otoo 2010
t Monteverde Institute : Tropical Ecology