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The modern and fossil record of farming behavior

Published online by Cambridge University Press:  21 August 2019

Shannon Hsieh
Affiliation:
Department of Earth and Environmental Sciences, University of Illinois at Chicago, 845 West Taylor Street, Chicago, Illinois 60607, U.S.A. E-mail: [email protected], [email protected], [email protected]
Alec Schassburger
Affiliation:
Department of Earth and Environmental Sciences, University of Illinois at Chicago, 845 West Taylor Street, Chicago, Illinois 60607, U.S.A. E-mail: [email protected], [email protected], [email protected]
Roy E. Plotnick
Affiliation:
Department of Earth and Environmental Sciences, University of Illinois at Chicago, 845 West Taylor Street, Chicago, Illinois 60607, U.S.A. E-mail: [email protected], [email protected], [email protected]

Abstract

Farming is a behavior in which an organism promotes the growth and reproduction of other organisms in or on a substrate as a food source. A number of trace fossils have been suggested to record the occurrence of farming behavior. These include the deep-sea graphoglyptid trace fossils, proposed to be microbial farms on the seafloor, and terrestrial fossil social insect nests thought to represent fungicultural behavior. The presumed farming behavior of graphoglyptids is the basis of the ethological category agrichnia. Four criteria have been proposed as diagnostic of farming behavior, and these can be applied to both observed modern and proposed trace fossil examples of farming behavior. The evidence for farming behavior in the social insect trace record is strong but is much weaker in the case of graphoglyptids. The use of agrichnia as an ethological category should be limited to well-supported cases.

Type
On The Record
Copyright
Copyright © The Paleontological Society. All rights reserved 2019 

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References

Literature Cited

Aanen, D. K. 2006. As you reap, so shall you sow: coupling of harvesting and inoculating stabilizes the mutualism between termites and fungi. Biology Letters 2:209212.Google Scholar
Aanen, D. K., Eggleton, P., Rouland-Lefevre, C., Guldberg-Frøslev, T., Rosendahl, S., and Boomsma, J. J.. 2002. The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proceedings of the National Academy of Sciences USA 99:1488714892.Google Scholar
Ashforth, E. J., Olive, P. J., and Ward, A. C.. 2011. Phylogenetic characterisation of bacterial assemblages and the role of sulphur-cycle bacteria in an Arenicola marina bioturbated mesocosm. Marine Ecology Progress Series 439:1930.Google Scholar
Baroni Urbani, C. 1980. First description of fossil gardening ants (Amber collection Stuttgart and Natural History Museum Basel; Hymenoptera: Formicidae. I: Attini.). Stuttgarter Beiträge zur Naturkunde B 54:113.Google Scholar
Brock, D. A., Douglas, T. E., Queller, D. C., and Strassmann, J. E.. 2011. Primitive agriculture in a social amoeba. Nature 469:393.Google Scholar
Brock, D. A., Read, S., Bozhchenko, A., Queller, D. C., and Strassmann, J. E.. 2013. Social amoeba farmers carry defensive symbionts to protect and privatize their crops. Nature Communications 4:2385.Google Scholar
Brock, D. A., Canas, A., Jones, K., Queller, D. C., and Strassmann, J. E.. 2017. Exposure to dense bacteria lawns does not cause the social amoeba Dictyostelium discoideum to carry bacteria through the social stage. PeerJ Preprints 5:e2698v1.Google Scholar
Bromley, R. G. 1996. Trace fossils: biology, taxonomy and applications, 2nd ed. Chapman and Hall, London.Google Scholar
Bromley, R. G. 1990. Trace fossils. biology and taphonomy. Unwin & Hyman, London.Google Scholar
Buatois, L. A., and Mángano, G. M.. 2011. Ichnology. Cambridge University Press, Cambridge.Google Scholar
Carricart-Ganivet, J. P., Carrera-Parra, L. F., Quan-Young, L. I., and García-Madrigal, M. S.. 2004. Ecological note on Troglocarcinus corallicola (Brachyura: Cryptochiridae) living in symbiosis with Manicina areolata (Cnidaria: Scleractinia) in the Mexican Caribbean. Coral Reefs 23:215217.Google Scholar
Duringer, P., Schuster, M., Genise, J. F., Likius, A., Mackaye, H. T., Vignaud, P., and Brunet, M.. 2006. The first fossil fungus gardens of Isoptera: oldest evidence of symbiotic termite fungiculture (Miocene, Chad basin). Naturwissenschaften 93:610615.Google Scholar
Duringer, P., Schuster, M., Genise, J. F., Mackaye, H. T., Vignaud, P., and Brunet, M.. 2007. New termite trace fossils: galleries, nests and fungus combs from the Chad basin of Africa (Upper Miocene–Lower Pliocene). Palaeogeography, Palaeoclimatology, Palaeoecology 251:323353.Google Scholar
Ekdale, A. A. 1980. Graphoglyptid burrows in modern deep-sea sediment. Science 207:304306.Google Scholar
Ekdale, A. A., Bromley, R. G., and Pemberton, S. G.. 1984. Ichnology: the use of trace fossils in sedimentology and stratigraphy. Society of Economic Paleontologists and Mineralogists Short Course 15:1317.Google Scholar
Farrell, B. D., Sequeira, A. S., O'Meara, B. C., Normark, B. B., Chung, J. H., and Jordal, B. H.. 2001. The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55:20112027.Google Scholar
Fernández-Marín, H., Zimmerman, J. K., Nash, D. R., Boomsma, J. J., and Wcislo, W. T.. 2009. Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants. Proceedings of the Royal Society of London B 276:22632269.Google Scholar
Frey, R. W., Howard, J. D., and Pryor, W. A.. 1978. Ophiomorpha: its morphologic, taxonomic, and environmental significance. Palaeogeography, Palaeoclimatology, Palaeoecology 23:199229.Google Scholar
Fuchs, T. 1895. Studien über Fucoiden and Hieroglyphen. Akademie der Wissenschaften zu Wien, mathematischnaturwissenschaftliche Klasse, Denkschriften 62:369448.Google Scholar
Genise, J. F., Alonso-Zarza, A. M., Krause, J. M., Sánchez, M. V., Sarzetti, L., Farina, J. L., González, M. G., Cosarinsky, M., and Bellosi, E. S.. 2010. Rhizolith balls from the Lower Cretaceous of Patagonia: just roots or the oldest evidence of insect agriculture? Palaeogeography, Palaeoclimatology, Palaeoecology 287:128142.Google Scholar
Genise, J. F., Melchor, R. N., Sánchez, M. V., and González, M. G.. 2013. Attaichnus kuenzelii revisited: a Miocene record of fungus-growing ants from Argentina. Palaeogeography, Palaeoclimatology, Palaeoecology 386:349363.Google Scholar
Grosberg, R. K., Vermeij, G. J., and Wainwright, P. C.. 2012. Biodiversity in water and on land. Current Biology 22:R900R903.Google Scholar
Hata, H., and Kato, M.. 2002. Weeding by the herbivorous damselfish Stegastes nigricans in nearly monocultural algae farms. Marine Ecology Progress Series 237:227231.Google Scholar
Hata, H., and Kato, M.. 2003. Demise of monocultural algal farms by exclusion of territorial damselfish. Marine Ecology Progress Series 263:159167.Google Scholar
Hata, H., and Kato, M.. 2006. A novel obligate cultivation mutualism between damselfish and Polysiphonia algae. Biology Letters 2:593596.Google Scholar
Honeycutt, C. E., and Plotnick, R.. 2005. Mathematical analysis of Paleodictyon: a graph theory approach. Lethaia 38:345350.Google Scholar
Hylleberg, J. 1975. Selective feeding by Abarenicola pacifica with notes on Abarenicola vagabunda and a concept of gardening in lugworms. Ophelia 14:113137.Google Scholar
Klompmaker, A. A., Portell, R. W., and Van Der Meij, S. E.. 2016. Trace fossil evidence of coral-inhabiting crabs (Cryptochiridae) and its implications for growth and paleobiogeography. Scientific Reports 6:23443.Google Scholar
Kobayashi, C., Fukasawa, Y., Hirose, D., and Kato, M.. 2008. Contribution of symbiotic mycangial fungi to larval nutrition of a leaf-rolling weevil. Evolutionary Ecology 22:711722.Google Scholar
Lassuy, D. R. 1980. Effects of “farming” behavior by Eupomacentrus lividus and Hemiglyphidodon plagiometopon on algal community structure. Bulletin of Marine Science 30:304312.Google Scholar
Laza, J. H. 1982. Signos de actividad atribuibles a Atta (Myrmicidae, Hymenoptera) en el Mioceno de la provincia de La Pampa, República Argentina. Significación paleozoogeográfica. Ameghiniana 19:109124.Google Scholar
Lehane, J. R., and Ekdale, A. A.. 2013a. Fractal analysis of graphoglyptid trace fossils. Palaios 28:2332.Google Scholar
Lehane, J. R., and Ekdale, A. A.. 2013b. Pitfalls, traps, and webs in ichnology: traces and trace fossils of an understudied behavioral strategy. Palaeogeography, Palaeoclimatology, Palaeoecology 375:5969.Google Scholar
Löwemark, L. 2015. Testing ethological hypotheses of the trace fossil Zoophycos based on Quaternary material from the Greenland and Norwegian seas. Palaeogeography, Palaeoclimatology, Palaeoecology 425:113.Google Scholar
McQuaid, C. D., and Froneman, P. W.. 1993. Mutualism between the territorial intertidal limpet Patella longicosta and the crustose alga Ralfsia verrucosa. Oecologia 96:128133.Google Scholar
Menezes, C., Vollet-Neto, A., Marsaioli, A. J., Zampieri, D., Fontoura, I. C., Luchessi, A. D., and Imperatriz-Fonseca, V. L.. 2015. A Brazilian social bee must cultivate fungus to survive. Current Biology 25:28512855.Google Scholar
Miller, W. III. 2014. Mystery of the graphoglyptids. Lethaia 47:13.Google Scholar
Mueller, U. G. 2002. Ant versus fungus versus mutualism: ant–cultivar conflict and the deconstruction of the attine ant–fungus symbiosis. American Naturalist 160:S67S98.Google Scholar
Mueller, U. G., and Gerardo, N.. 2002. Fungus-farming insects: multiple origins and diverse evolutionary histories. Proceedings of the National Academy of Sciences USA 99:1524715249.Google Scholar
Mueller, U. G., Rehner, S. A., and Schultz, T. R.. 1998. The evolution of agriculture in ants. Science 281:20342038.Google Scholar
Mueller, U. G., Gerardo, N. M., Aanen, D. K., Six, D. L., and Schultz, T. R.. 2005. The evolution of agriculture in insects. Annual Review of Ecology, Evolution, and Systematics 36:563595.Google Scholar
Ott, J. A., Fuchs, B., Fuchs, R., and Malasek, A.. 1976. Observations on the biology of Callianassa stebingi Borrodaille and Upogebia litoralis Risso and their effect upon the sediment. Senckenbergiana Maritima 8:6179.Google Scholar
Pion, M., Spangenberg, J. E., Simon, A., Bindschedler, S., Flury, C., Chatelain, A., Bshary, R., Job, D., and Junier, P.. 2013. Bacterial farming by the fungus Morchella crassipes. Proceedings of the Royal Society of London B 280:20132242.Google Scholar
Plagányi, É. E., and Branch, G. M.. 2000. Does the limpet Patella cochlear fertilize its own algal garden? Marine Ecology Progress Series 194:113122.Google Scholar
Plotnick, R. E. 2012. Behavioral biology of trace fossils. Paleobiology 38:459473.Google Scholar
Reichardt, W. 1988. Impact of bioturbation by Arenicola marina on microbiological parameters in intertidal sediments. Marine Ecology Progress Series. 44:149158.Google Scholar
Riisgard, H. U., and Banta, G. T.. 1998. Irrigation and deposit feeding by the lugworm Arenicola marina, characteristics and secondary effects on the environment. A review of current knowledge. Vie et Milieu 48:243258.Google Scholar
Roberts, E. M., Todd, C. N., Aanen, D. K., Nobre, T., Hilbert-Wolf, H. L., O'Connor, P. M., Tapanila, L., Mtelela, C., and Stevens, N. J.. 2016. Oligocene termite nests with in situ fungus gardens from the Rukwa Rift Basin, Tanzania, support a Paleogene African origin for insect agriculture. PLoS ONE 11:e0156847.Google Scholar
Röder, H. 1971. Gangsysteme von Paraonis fulgens Levinsen 1883 (Polychaeta) in okologischer, ethologischer,und aktuopalaontologischer Sicht. Senckenbergiana maritima 3:351.Google Scholar
Rohfritsch, O. 2008. Plants, gall midges, and fungi: a three-component system. Entomologia Experimentalis et Applicata 128:208216.Google Scholar
Rona, P. A., Seilacher, A., de Vargas, C., Gooday, A. J., Bernhard, J. M., Bowser, S., Vetriani, C., Wirsen, C. O., Mullineaux, L., Sherrell, R., Grassle, J. F., Low, S., and Lutz, R. A.. 2009. Paleodictyon nodosum: a living fossil on the deep-sea floor. Deep-Sea Research, part II (Topical Studies in Oceanography) 56:17001712.Google Scholar
Schultz, T. R., Mueller, U. G., Currie, C. R., and Rehner, S. A.. 2005. Pp. 149190 in Vega, F. E. and Blackwell, M., eds., Insect–fungal associations: ecology and evolution. Oxford University Press, New York.Google Scholar
Seilacher, A. 2007. Trace fossil analysis. Springer Science & Business Media, Berlin.Google Scholar
Seilacher, A. 1977. Pattern analysis of Paleodictyon and related trace fossils. In Crimes, T. P. and Harper, J. C., eds., Trace fossils 2. Geological Journal, Special Issue 9:289–334.Google Scholar
Silliman, B. R., and Newell, S. Y.. 2003. Fungal farming in a snail. Proceedings of the National Academy of Sciences USA 100:1564315648.Google Scholar
Silva, P. D., Leal, I. R., Wirth, R., and Tabarelli, M.. 2007. Harvesting of Protium heptaphyllum (Aubl.) March. seeds (Burseraceae) by the leaf-cutting ant Atta sexdens L. promotes seed aggregation and seedling mortality. Brazilian Journal of Botany 30:553560.Google Scholar
Stimson, J. 1973. The role of the territory in the ecology of the intertidal limpet Lottia gigantea (Gray). Ecology 54:10201030.Google Scholar
Thutupalli, S., Uppaluri, S., Constable, G. W., Levin, S. A., Stone, H. A., Tarnita, C. E., and Brangwynne, C. P.. 2017. Farming and public goods production in Caenorhabditis elegans populations. Proceedings of the National Academy of Sciences USA 114:22892294.Google Scholar
Toki, W., Tanahashi, M., Togashi, K., and Fukatsu, T.. 2012. Fungal farming in a non-social beetle. PLoS ONE 7:e41893.Google Scholar
Uchman, A. 2003. Trends in diversity, frequency and complexity of graphoglyptid trace fossils: evolutionary and palaeoenvironmental aspects. Palaeogeography Palaeoclimatology Palaeoecology 192:123142.Google Scholar
Uchman, A., and Wetzel, A.. 2012. Deep-sea fans. In Knaust, D., and Bromley, R. G., eds. Trace fossils as indicators of sedimentary environments. Developments in Sedimentology 64:643–671. Elsevier, Amsterdam.Google Scholar
Vallon, L. H., Rindsberg, A. K., and Bromley, R. G.. 2016. An updated classification of animal behaviour preserved in substrates. Geodinamica Acta 28:520.Google Scholar
Wheatcroft, R. A. 1991. Trace fossils: biology and taphonomy (RG Bromley). Limnology and Oceanography 36:216217.Google Scholar
Woodin, S. A. 1977. Algal “gardening” behavior by nereid polychaetes: effects on soft-bottom community structure. Marine Biology 44:3942.Google Scholar
Zhu, Z., van Belzen, J., Hong, T., Kunihiro, T., Ysebaert, T., Herman, P. M., and Bouma, T. J.. 2016. Sprouting as a gardening strategy to obtain superior supplementary food: evidence from a seed-caching marine worm. Ecology 97:32783284.Google Scholar