Abstract
Social insect workers modify task performance according to age-related schedules of behavioral development, and/or changing colony labor requirements based on flexible responses that may be independent of age. Using known-age minor workers of the ant Pheidole dentata throughout 68 % of their 140-day laboratory lifespan, we asked whether workers found inside or outside the nest differed in task performance and if behaviors were correlated with and/or causally linked to changes in brain serotonin (5HT) and dopamine (DA). Our results suggest that task performance patterns of individually assayed minors collected at these two spatially different worksites were independent of age. Outside-nest minors displayed significantly higher levels of predatory behavior and greater activity than inside-nest minors, but these groups did not differ in brood care or phototaxis. We examined the relationship of 5HT and DA to these behaviors in known-age minors by quantifying individual brain titers. Both monoamines did not increase significantly from 20 to 95 days of age. DA did not appear to directly regulate worksite location, although titers were significantly higher in outside-nest than inside-nest workers. Pharmacological depletion of 5HT did not affect nursing, predation, phototaxis, or activity. Our results suggest that worker task capabilities are independent of age beyond 20 days, and only predatory behavior can be consistently predicted by spatial location. This could reflect worker flexibility or variability in the behavior of individuals collected at each location, which could be influenced by complex interactions between age, worksite location, social interactions, neuromodulators, and other environmental and internal regulators of behavior.
Significance statement
Physiological changes associated with worker age are considered to be important regulators of task performance in social insects. The extent to which worker age is correlated with behavior, and the degree to which developmental changes in neuromodulators control worker labor, however, are poorly understood. We found that ant workers are behaviorally flexible in respect to task performance at a given age, but differ in predatory response and activity level based on their worksite location (within or outside of the nest). Dopamine level was higher in outside-nest workers; serotonin did not appear to be causally linked to any behavior we examined. Our findings suggest that worker task performance can be independent of age, and workers maintain task efficacy throughout their lifespan while differing in some aspects of behavioral performance that may change with worksite location. Relationships between age, worksite, and neuromodulator titers appear to be complex.
Similar content being viewed by others
References
Akasaka S, Sasaki K, Harano K, Nagao T (2010) Dopamine enhances locomotor activity for mating in male honeybees (Apis mellifera L.). J Insect Physiol 56:1160–1166
Alekseyenko O, Chan Y-B, de la Paz FM, Bülow T, Pankratz MJ, Kravitz EA (2014) Single serotonergic neurons that modulate aggression in Drosophila. Curr Biol 24:2700–2702
Andrews JC, Fernández MP, Yu Q, Leary GP, Leung AKW, Kavanaugh MP, Kravitz EA, Certel SJ (2014) Octompamine neuromodulation regulates Gr32a-linked aggression and courtship pathways in Drosophila males. PLoS Genet 10:e1004356
Arnan X, Ferrandiz-Rovira M, Pladevall C, Rodrigo A (2011) Worker size-related task partitioning in the foraging strategy of a seed-harvesting ant species. Behav Ecol Sociobiol 65:1881–1890
Baracchi D, Cini A (2014) A socio-spatial combined approach confirms a highly compartmentalized structure in honeybees. Ethology 120:1167–1176
Barron AB, Robinson GE (2005) Selective modulation of task performance by octopamine in honey bee (Apis mellifera) division of labour. J Comp Physiol A 191:659–668
Ben-Shahar Y, Robichon A, Sokolowski MB, Robinson GE (2002) Influence of gene action across different time scales on behavior. Science 296:741–744
Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440
Blanchard G, Orledge G, Reynolds S, Franks N (2000) Division of labour and seasonality in the ant Leptothorax albipennis: worker corpulence and its influence on behaviour. Anim Behav 59:723–738
Bloch G, Robinson GE (2001) Chronobiology: reversal of honeybee behavioral rhythms. Nature 410:1048
Burd M (1996) Foraging performance by Atta colombica, a leaf-cutting ant. Am Nat 148:597–612
Calabi P, Traniello JFA (1989) Social organization in the ant Pheidole dentata: physical and temporal caste ratios lack ecological correlates. Behav Ecol Sociobiol 24:69–78
Cassill DL, Tschinkel WR (1995) Allocation of liquid food to larvae via trophallaxis in colonies of the fire ant, Solenopsis invicta. Anim Behav 50:801–813
Cohen J (1988) Statistical Power Analysis for the Behavioral Sciences. Lawrence Erlbaum Associates, Hillsdale, NJ
Constant N, Santorelli LA, Lopes JFS, Hughes WOH (2012) The effects of genotype, caste, and age on foraging performance in leaf-cutting ants. Behav Ecol 23:1284–1288
Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, Hughes KA, Robinson GE (2007) Vitellogenin, juvenile hormone, insulin signaling and queen honey bee longevity. Proc Natl Acad Sci U S A 104:7128–7133
Dolezal AG, Brent CS, Hölldobler B, Amdam GV (2012) Worker division of labor and endocrine physiology are associated in the harvester ant, Pogonomyrmex californicus. J Exp Biol 215:454–460
Duarte A, Weissing FJ, Pen I, Keller L (2011) An evolutionary perspective on self-organized division of labor in social insects. Annu Rev Ecol Evol S 42:91–110
Falibene A, Rössler W, Josens R (2012) Serotonin depresses feeding behaviour in ants. J Insect Physiol 58:7–17
Giraldo YM, Kamhi JF, Fourcassié V, Moreau M, Robson SKA, Rusakov A, Wimberly L, Diloreto A, Kordek A, Traniello JFA (2016) Lifespan behavioral and neural resilience in a social insect. Proc R Soc B 283:20152603
Giraldo YM, Patel E, Gronenberg W, Traniello JFA (2013) Division of labor and structural plasticity in an extrinsic serotonergic mushroom body neuron in the ant Pheidole dentata. Neurosci Lett 534:107–111
Giraldo YM, Traniello JFA (2014) Worker senescence and the sociobiology of aging in ants. Behav Ecol Sociobiol 68:1901–1919
Gordon DM (2010) Ant encounters: interaction networks and colony behavior. Princeton University Press, Princeton, NJ
Greene MJ, Gordon DM (2007) Interaction rate informs harvester ant task decisions. Behav Ecol 18:451–455
Gronenberg W, Heeren S, Hölldobler B (1996) Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J Exp Biol 199:2011–2019
Grüter C, Czaczkes TJ, Ratnieks FLW (2011) Decision making in ant foragers (Lasius niger) facing conflicting private and social information. Behav Ecol Sociobiol 65:141–148
Guerenstein PG, Hildebrand JG (2008) Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:161–178
Haehnel M, Menzel R (2012) Long-term memory and response generalization in mushroom body extrinsic neurons in the honeybee Apis mellifera. J Exp Biol 215:559–565
Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Memory 5:146–156
Hölldobler B, Wilson EO (1990) The Ants. Belknap Press of Harvard University Press. Cambridge, MA
Hölldobler B, Wilson EO (2009) The superorganism: the beauty, elegance, and strangeness of insect socities. W. W. Norton & Company, New York
Huang MH, Wheeler DE, Fjerdingstad EJ (2013) Mating system evolution and worker caste diversity in Pheidole ants. Mol Ecol 22:1998–2010
Ibarrarán Viniegra AS (2015) Inter-individual variability and division of labour in the ant Pheidole dentata. Dissertation, McGill University
Ilieş I, Muscedere ML, Traniello JFA (2015) Neuroanatomical and morphological trait clusters in the ant genus Pheidole: evidence for modularity and integration in brain structure. Brain Behav Evol 85:63–76
Ingram KK, Krummey S, LeRoux M (2009) Expression patterns of a circadian clock gene are associated with age-related polyethism in harvester ants, Pogonomyrmex occidentalis. BMC Ecol 9:7
Ingram KK, Oefner P, Gordon DM (2005) Task-specific expression of the foraging gene in harvester ants. Mol Ecol 14:813–818
Ito F, Higashi S (1991) A linear dominance hierarchy regulating reproduction and polyethism of the queenless ant Pachycondyla sublaevis. Naturwissenschaften 78:80–82
Johnson BR (2007) Within-nest temporal polyethism in the honey bee. Behav Ecol Sociobiol 62:777–784
Johnston AB, Wilson EO (1985) Correlates of variation in the major/minor ratio of the ant, Pheidole dentata. Ann Entomol Soc Am 78:8–11
Jones TA, Donlan NA, O’Donnell S (2009) Growth and pruning of mushroom body Kenyon cell dendrites during worker behavioral development in the paper wasp, Polybia aequatorialis (Hymenoptera: Vespidae). Neurobiol Learn Memory 92:485–495
Kamhi JF, Nunn K, Robson SKA, Traniello JFA (2015) Polymorphism and division of labour in a socially complex ant: neuromodulation of aggression in the Australian weaver ant, Oecophylla smaragdina. Proc R Soc B 282:20150704
Kamhi JF, Traniello JFA (2013) Biogenic amines and collective organization in a superorganism: neuromodulation of social behavior in ants. Brain Behav Evol 82:220–236
Kwapich CL, Tschinkel WR (2013) Demography, demand, death, and the seasonal allocation of labor in the Florida harvester ant (Pogonomyrmex badius). Behav Ecol Sociobiol 67:2011–2027
Kwapick CL, Tschinkel WR (2016) Limited flexibility and unusual longevity shape forager allocation in the Florida harvester ant (Pogonomyrmex badius). Behav Ecol Sociobiol 70:221–235
Lenoir A (1979) Le comportement alimentaire et la division du travail chez la fourmi Lasius niger (L.). Bull Biol Fr Belg 113:79–314
Libbrecht R, Oxley PR, Kronauer DJC, Keller L (2013) Ant genomics sheds light on the molecular regulation of social organization. Genome Biol 14:212
Lucas C, Nicolas M, Keller L (2015) Expression of foraging and Gp-9 are associated with social organization in the fire ant Solenopsis invicta. Insect Mol Biol 24:93–104
Lucas C, Sokolowski MB (2009) Molecular basis for changes in behavioral state in ant social behaviors. Proc Natl Acad Sci U S A 106:6351–6356
Marco Antonio DS, Guidugli-Lazzarini KR, do Nascimento AM, Simões ZLP, Hartfelder K (2008) RNAi-mediated silencing of vitellogenin gene function turns honeybee (Apis mellifera) workers into extremely precocious foragers. Naturwissenschaften 95:953–961
McQuillan HJ, Barron AB, Mercer AR (2012a) Age- and behavior-related changes in the expression of biogenic amine receptor genes in the antennae of honey bees (Apis mellifera). J Comp Physiol A 198:753–761
McQuillan HJ, Nakagawa S, Mercer AR (2012b) Mushroom bodies of the honeybee brain show cell population-specific plasticity in the expression of amine-receptor genes. Learn Memory 19:151–158
Meltzer CC, Smith G, DeKosky ST, Pollock BG, Mathis CA, Moore RY, Kupfer DJ, Reynolds CF (1998) Serotonin in aging, late-life depression, and Alzheimer’s disease: the emerging role of functional imaging. Neuropsychopharmacology 18:407–430
Mersch DP, Crespi A, Keller L (2013) Tracking individuals shows spatial fidelity is a key regulator of ant social organization. Science 340:1090–1093
Muscedere ML, Djermoun A, Traniello JFA (2013) Brood-care experience, nursing performance, and neural development in the ant Pheidole dentata. Behav Ecol Sociobiol 67:775–784
Muscedere ML, Helms Cahan S, Helms K, Traniello JFA (2016) Geographic and life-history variation in ant queen colony founding correlate with brain amine levels. Behav Ecol 27:271–278
Muscedere ML, Johnson N, Gillis BC, Kamhi JF, Traniello JFA (2012) Serotonin modulates worker responsiveness to trail pheromone in the ant Pheidole dentata. J Comp Physiol A 198:219–227
Muscedere ML, Traniello JFA (2012) Division of labor in the hyperdiverse ant genus Pheidole is associated with distinct subcaste- and age-related patterns of worker brain organization. PLoS ONE 7:e31618
Muscedere ML, Traniello JFA, Gronenberg W (2011) Coming of age in an ant colony: cephalic muscle maturation accompanies behavioral development in Pheidole dentata. Naturwissenschaften 98:783–793
Muscedere ML, Willey TA, Traniello JFA (2009) Age and task efficiency in the ant Pheidole dentata: young minor workers are not specialist nurses. Anim Behav 77:911–918
Mustard JA, Pham PM, Smith BH (2010) Modulation of motor behavior by dopamine and the D1-like dopamine receptor AmDOP2 in the honey bee. J Insect Physiol 56:422–430
Nahar P, Naqvi A, Basir SF (2004) Sunlight-mediated activation of an inert polymer surface for covalent immobilization of a protein. Anal Biochem 327:162–164
Nakagawa S, Foster T (2004) The case against retrospective statistical power analyses with an introduction to power analysis. Acta Ethol 7:103–108
Narendra A, Reid SF, Hemmi JM (2010) The twilight zone: ambient light levels trigger activity in primitive ants. Proc R Soc Lond B 277:1531–1538
Neckameyer WS (1996) Multiple roles for dopamine in Drosophila development. Dev Biol 176:209–219
Oster GF, Wilson EO (1978) Caste and Ecology in the Social Insects. Princeton University Press, Princeton, NJ
Pamminger T, Foitzik S, Kaufmann KC, Schützler N, Menzel F (2014) Worker personality and its association with spatially structured division of labor. PLoS One 9:e79616
PASS14 Power Analysis and Sample Size Software (2015) NCSS, LLC. Kaysville, Utah, USA. ncss.com/software/pass
Pinter-Wollman N, Bala A, Merrell A, Queirolo J, Stumpe MC, Holmes S, Gordon DM (2013) Harvester ants use interactions to regulate forager activation and availability. Anim Behav 86:197–207
Porter SD, Jorgensen CD (1981) Foragers of the harvester ant, Pogonomyrmex owyheei: a disposable caste? Behav Ecol Sociobiol 9:247–256
Powell S, Tschinkel W (1999) Ritualized conflict in Odontomachus brunneus and the generation of interaction-based task allocation: a new organizational mechanism in ants. Anim Behav 58:965–972
Ravary F, Lecoutey E, Kaminski G, Châline N, Jaisson P (2007) Individual experience alone can generate lasting division of labor in ants. Curr Biol 17:1308–1312
Robinson EJH, Feinerman O, Franks NR (2012) Experience, corpulence and decision making in ant foraging. J Exp Biol 215:2653–2659
Robinson EJH, Richardson TO, Sendova-Franks AB, Feinerman O, Franks NR (2009) Radio tagging reveals the roles of corpulence, experience and social information in ant decision making. Behav Ecol Sociobiol 63:627–636
Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37:637–665
Robinson GE, Page R Jr, Huang Z (1994) Temporal polyethism in social insects is a developmental process. Anim Behav 48:467–469
Rueppell O, Chandra SBC, Pankiw T, Fondrk MK, Beye M, Hunt G, Page RE (2006) The genetic architecture of sucrose responsiveness in the honeybee (Apis mellifera L.). Genetics 172:243–251
Scheiner R, Baumann A, Blenau W (2006) Aminergic control and modulation of honeybee behaviour. Curr Neuropharmacol 4:259–276
Schmid-Hempel P, Schmid-Hempel R (1984) Life duration and turnover of foragers in the ant Cataglyphis bicolor (Hymenoptera, Formicidae). Insect Soc 31:345–360
Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies. J Comp Physiol A Sensory, Neural, Behav Physiol 184:481–488
Schulz DJ, Robinson GE (2001) Octopamine influences division of labor in honey bee colonies. J Comp Physiol A 187:53–61
Seehuus S-C, Krekling T, Amdam GV (2006) Cellular senescence in honey bee brain is largely independent of chronological age. Exp Gerontol 41:1117–1125
Seeley TD (1982) Adaptive significance of the age polyethism schedule in honeybee colonies. Behav Ecol Sociobiol 11:287–293
Seid MA, Goode K, Li C, Traniello JFA (2008) Age- and subcaste-related patterns of serotonergic immunoreactivity in the optic lobes of the ant Pheidole dentata. Dev Neurobiol 68:1325–1333
Seid MA, Harris KM, Traniello JFA (2005) Age-related changes in the number and structure of synapses in the lip region of the mushroom bodies in the ant Pheidole dentata. J Comp Neurol 488:269–277
Seid MA, Traniello JFA (2005) Age-related changes in biogenic amines in individual brains of the ant Pheidole dentata. Naturwissenschaften 92:198–201
Seid MA, Traniello JFA (2006) Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants. Behav Ecol Sociobiol 60:631–644
Simola DF, Graham RJ, Brady CM, Enzmann BL, Desplan C, Ray A, Zwiebel LJ, Bonasio R, Reinberg D, Liebig J, Berger SL (2016) Epigenetic (re)programming of caste-specific behavior in the ant Camponotus floridanus. Science 351:aac6633-1- aac6633-9
Smith AR, Muscedere ML, Seid MA, Traniello JFA, Hughes WOH (2013) Biogenic amines are associated with worker task but not patriline in the leaf-cutting ant Acromyrmex echinatior. J Comp Physiol A 199:1117–1127
Smith DR, Hardy IEW, Gammell MP (2011) Power rangers: no improvement in the statistical power of analyses published in Animal Behaviour. Anim Behav 81:347–352
Stieb SM, Hellwig A, Wehner R, Rössler W (2012) Visual experience affects both behavioral and neuronal aspects in the individual life history of the desert ant Cataglyphis fortis. Dev Neurbiol 72:729–742
Thomas L (1997) Retrospective power analysis. Conserv Biol 11:276–280
Thomas ML, Elgar MA (2003) Colony size affects division of labour in the ponerine ant Rhytidoponera metallica. Naturwissenschaften 90:88–92
Toth AL, Robinson GE (2007) Evo-devo and the evolution of social behavior. Trends Genet 23:334–341
Traniello JFA (1978) Caste in a primitive ant: absence of age polyethism in Amblyopone. Science 202:770–772
Tsuruda JM, Amdam GV, Page RE (2008) Sensory response system of social behavior tied to female reproductive traits. PLoS ONE 3:e3397
Tsuruda JM, Page RE (2009) The effects of foraging role and genotype on light and sucrose responsiveness in honey bees (Apis mellifera L.). Behav Brain Res 205:132–137
Wilson EO (1976) Behavioral discretization and the number of castes in an ant species. Behav Ecol Sociobiol 1:141–154
Wilson EO (1985) The sociogenesis of insect colonies. Science 228:1489–1495
Wilson EO (2003) Pheidole in the New World: a dominant, hyperdiverse ant genus. Harvard University Press, Cambridge, MA
Wnuk A, Wiater M, Godzinska EJ (2011) Effect of past and present behavioural specialization on brain levels of biogenic amines in workers of the red wood ant Formica polyctena. Physiol Entomol 36:54–61
Wolf H (2008) Desert ants adjust their approach to a foraging site according to experience. Behav Ecol Sociobiol 62:415–425
Ziesmann J (1996) The physiology of an olfactory sensillum of the termite Schedorhinotermes lamanianus: carbon dioxide as a modulator of olfactory sensitivity. J Comp Physiol A 179:123–133
Acknowledgments
We thank Drs. Wulfila Gronenberg, Karen Warkentin, and Kimberly McCall for their critical reading of earlier drafts of the manuscript and three anonymous reviewers for constructive feedback. We also thank Dr. Sofia Ibarrarán Viniegra for sharing data on spatial fidelity and receptors. This work was supported by the National Institute on Aging of the National Institutes of Health (grant F31AG041589) to YMG and National Science Foundation grant IOS‐1354291 to JFT. Support was also provided by the Boston University Undergraduate Research Opportunity Program to AR, AK, and AD. The work presented here is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by L. Keller
This manuscript is a contribution to the special issue Integrative Analysis of Division of Labor—Guest Editors: Simon K. Robson, James F.A. Traniello 2.
Rights and permissions
About this article
Cite this article
Giraldo, Y.M., Rusakov, A., Diloreto, A. et al. Age, worksite location, neuromodulators, and task performance in the ant Pheidole dentata . Behav Ecol Sociobiol 70, 1441–1455 (2016). https://doi.org/10.1007/s00265-016-2153-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-016-2153-8