Rhizolith balls from the Lower Cretaceous of Patagonia: Just roots or the oldest evidence of insect agriculture?

Palaeogeography, Palaeoclimatology, Palaeoecology

Volumn 287, Issue 1-4, 2010, Pages 128-142

  Genise, Jorge F ^a   Alonso Zarza, Ana María ^b   Krause, J Marcelo ^a   Sánchez, M Victoria ^c   Sarzetti, Laura ^a   Farina, Juan L ^d   González, Mirta G ^c   Cosarinsky, Marcela ^c   Bellosi, Eduardo S ^c  

^a MUSEO PALEONTOLÓGICO EGIDIO FERUGLIO   (Argentina)

^b Universidad Complutense de Madrid CSIC   (Spain)

^c MUSEO ARGENTINO DE CIENCIAS NATURALES BERNARDINO RIVADAVIA   (Argentina)

^d Museo Municipal de Ciencias Naturales Lorenzo Scaglia   (Argentina)

Author keywords

Cretaceous; Insect agriculture; Insect trace fossils; Patagonia; Rhizolith balls

Indexed keywords

CRETACEOUS; FOSSIL RECORD; ICHNOLOGY; MICROMORPHOLOGY; ORGANIC MATTER; PHYLOGENY; RHIZOLITH; SCANNING ELECTRON MICROSCOPY; TERMITE;

PATAGONIA;

ASTACOIDEA; ATTINI; BACTERIA (MICROORGANISMS); FORMICIDAE; FUNGI; HEXAPODA; ISOPTERA;

EID: 76949096033     PISSN: 00310182     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.palaeo.2010.01.028     Document Type: Article

References (101)

1. Agosti D., Grimaldi D., and Carpenter J.M. Oldest known ant fossils discovered. Nature 391 (1997) 447
2. Alonso-Zarza A.M., Silva P.G., Goy J.L., and Zazo C. Fan-surface dynamics and biogenic calcrete development: Interactions during ultímate phases of fan evolucion in the semiarid SE Spain (Murcia). Geomorphology 24 (1998) 147-167
3. Alonso-Zarza A.M., Genise J.F., Cabrera M.C., Mangas J., Martín-Pérez A., Valdeolmillos A., and Dorado-Valiño M. Megarhizoliths in Pleistocene aeolian deposits on Gran Canaria (Spain): ichnological and palaeoenvironmental significance. Palaeogeography, Palaeoclimatology, Palaeoecology 265 (2008) 39-61
4. Barbour E.H. Nature, structure, and phylogeny of Daemonelix. Bulletin of the Geological Society of America 8 (1897) 305-314
5. Baroni-Urbani C. First description of fossil gardening ants. Stuttgarter Beiträge zur Naturkunde 54 (1980) 1-13
6. Batra L.R., and Batra S.W.T. The fungus gardens of insects. Scientific American 217 (1967) 112-120
7. Bedatou E., Melchor R.N., Bellosi E.S., and Genise J.F. Crayfish burrows from Late Jurassic-Late Cretaceous continental deposits of Patagonia: Argentina. Their palaeoecological, palaeoclimatic and palaeobiogeographical significance. Palaeogeography, Palaeoclimatology, Palaeoecology 257 (2008) 169-184
8. Bidartondo M.I., Kretzer A.M., Pine E.M., and Bruns T.D. High root concentration and uneven ectomycorrhizal diversity near Sarcodes sanguinea (Ericaceae): a cheater that stimulates its victims?. American Journal of Botany 87 (2000) 1783-1788
9. Bonetto A.A. Las hormigas cortadoras de la Provincia de Santa Fe. Dirección General de Recursos Naturales de la Provincia de Santa Fe (1959) 84 pp.
10. Bordy E.M., Bumby A.J., Catuneanu O., and Eriksson P.G. Advanced early Jurassic termite (Insecta: Isoptera) nests: evidence from the Clarens Formation in the Tuli Basin, Southern Africa. Palaios 19 (2004) 68-78
11. Brady S.G., Schultz T.R., Fisher B.L., and Ward P.S. Evaluating alternative hypotheses for the early evolution and diversification of ants. Proceedings of the National Academy of Sciences 103 (2006) 18172-18177
12. Bromley R., Buatois L., Genise J.F., Labandeira C., Mángano G., Melchor R., Schlirf M., and Uchman A. Comments on the paper "Reconnaissance of Upper Jurassic Morrison Formation ichnofossils, Rocky Mountain Region, USA: paleoenvironmental, stratigraphic, and paleoclimatic significance of terrestrial and freshwater ichnocoenoses" by Stephen T. Hasiotis. Sedimentary Geology 200 (2007) 141-150
13. Bruch C. Contribución al estudio de las hormigas de la provincia de San Luis. Revista del Museo de La Plata 23 2da serie (1916) 291-357
14. Bruch C. Costumbres y nidos de hormigas. Anales de la Sociedad Científica Argentina 83 (1917) 202-316
15. Bruch C. Estudios mirmecológicos. Anales del Museo de Historia Natural de Buenos Aires 34 (1928) 341-360
16. Bucher E.H. Observaciones ecológicas sobre los artrópodos del bosque chaqueño de Tucuman. Revista de la Facultad de Ciencias Exactas, Físicas y Naturales de Córdoba Nueva Serie Biología 1 (1974) 35-122
17. Carballido J.L., Pol D., Apesteguía S., Bellosi E.S., and Krause M. New materials of Chubutisaurus insignis (Sauropoda, Titanosauriformes) and basal titanosauriform relationships. Resúmenes del III Congreso Latinoamericano de Paleontología de Vertebrados, Neuquén, Argentina (2008) 46
18. Chapela I.H., Rehner S.A., Schultz T.R., and Mueller U.G. Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266 (1994) 1691-1694
19. Chebli G.A., Nakayama C., Sciutto J.C., and Serraiotto A.A. Estratigrafía del Grupo Chubut en la región central de la provincia homónima. Actas del Congreso Geológico Argentino 1 6 (1976) 375-392
20. Codignotto J., Nullo F., Panza J., and Proserpio C. Estratigrafía del Grupo Chubut entre Paso de Indios y Las Plumas, provincia del Chubut, Argentina. Actas del Congreso Geológico Argentino 1 7 (1978) 471-480
21. Coutinho L.M. Aspectos ecológicos da saúva no cerrado - a saúva, as queimadas e sua possível relaçao na ciclagem de nutrientes minerais. Boletim de Zoologia de la Universidad de Sao Paulo 8 (1984) 1-9
22. Cramer M.D., and Hawkins H.J. A physiological mechanism for the formation of root casts. Palaeogeography, Palaeoclimatology, Palaeoecology 274 (1984) 125-133
23. Currie C.R., Scott J.A., Summerbell R.C., and Malloch D. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398 (1999) 701-704
24. Currie C.M., Wong B., Stuart A.E., Schultz T.R., Rehner S.A., Mueller U.G., Sung G., Spatafora J.W., and Straus N.A. Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 299 (2003) 386-388
25. Daguerre J.B. Hormigas del género Atta Frabicius de la Argentina. Revista de la Sociedad Entomológica Argentina 12 (1945) 438-460
26. de la Providencia I., de Souza F.A., Fernandez F., Delmas N.S., and Declerck S. Arbuscular micorrhizal fungi reveal distinct patterns of anostomosis formation and hyphal healing mechanisms between different phylogenetic groups. New Phytologist 165 (2005) 261-271
27. Dell B., Malajczuk N., and Thomson G.T. Ectomycorrhiza formation in Eucalyptus V. A tuberculate ectomycorrhiza of Eucalyptus pilularius. New Phytologist 114 (1990) 633-640
28. Dubiel R.F., Blodgett R.H., and Bown T.M. Lungfish burrows in the Upper Triassic Chinle and Dolores Formation, Colorado Plateau. Journal of Sedimentary Petrology 57 (1987) 512-521
29. Duringer P., Schuster M., Genise J.F., Likius A., Mackaye H., Vignaud P., and Brunet M. The first fossil fungus gardens of Isoptera: oldest evidence of symbiotic termite fungiculture (Miocene, Chad Basin). Naturwissenschaften 93 (2006) 610-615
30. Duringer P., Schuster M., Genise J.F., Mackaye H., Vignaud P., and Brunet M. New termite trace fossils: galleries, nests and fungus combs from the Chad Basin of Africa (Upper Miocene-Lower Pliocene). Palaeogeography, Palaeoclimatology, Palaeoecology 251 (2007) 323-353
31. Engel M.S., and Krishna K. Family-group names for termites. American Museum Novitates 3432 (2004) 1-9
32. Eschenbrenner V. Contribution des Termites á la micro-agrégation des solstropicaux. Cahier Orstom, Série Pédologie 22 (1986) 397-408
33. Garling L. Origin of ant-fungus mutualism: a new hypothesis. Biotropica 11 (1979) 284-291
34. Garnier-Sillam E., Toutain F., Villemin G., and Renoux J. Etudes preliminaries des meules originales du termite xylophage Sphaerotermes sphaerothorax (Sjostedt). Insectes Sociaux 36 (1989) 293-312
35. Genise J.F. Inadvertent advances on ichnotaxonomy of non-animal trace fossils: a contribution to the status quo. Abstract Book of the III Workshop on Ichnotaxonomy (2006), Czech Geological Institute, Prague 10-11
36. Genise J.F., Bellosi E.S., Melchor R.N., and Cosarinsky M.I. Comment-Advanced Early Jurassic termite (Insecta:Isoptera) nests: evidence from the Clarens Formation in the Tuli Basin, Southern Africa (Bordy et al., 2004). Palaios 20 (2005) 303-305
37. Genise J.F., Bedatou E., and Melchor R.N. Terrestrial crustacean breeding trace fossils from the Cretaceous of Patagonia (Argentina): palaeobiological and evolutionary significance. Palaeogeography, Palaeoclimatology, Palaeoecology 264 (2008) 128-139
38. Giovannetti M., Sbrana C., Avio L., and Strani P. Patterns of below-ground plant interconnections established by means of arbuscular mycorrhizal networks. New Phytologist 164 (2004) 175-181
39. Gobetz K.E. Possible burrows of mylagaulids (Rodentia: Aplodontoidea: Mylagaulidae) from the late Miocene (Barstovian) Pawnee Creek Formation of northeastern Colorado. Palaeogeography, Palaeoclimatology, Palaeoecology 237 (2006) 119-136
40. Grassé P., and Noirot C. Sur le nid et la biologie du Sphaerotermes sphaerothorax (Sjöstedt). Annales des Sciences Naturelles, Zoologie 11 Série 10 (1948) 149-165
41. Grimaldi D.A., and Agosti D. A formicinae in New Jersey Cretaceous amber (Hymenoptera: Formicidae) and early evolution of the ants. Proceedings of the National Academy of Science 97 (2000) 13678-13683
42. Grimaldi D.A., and Engel M.S. Evolution of the Insects (2005), Cambridge University Press, New York 755 pp.
43. Growns I.O., and Richardson A.M. Diet and burrowing habits of the freshwater crayfish, Parastacoides tasmanicus tasmanicus Clark (Decapoda: Parastacidae). Australian Journal of Marine and Freshwater Research 39 (1988) 525-534
44. Hasiotis S.T. Reconnaissance of Upper Jurassic Morrison Formation ichnofossils, Rocky Mountain Region, USA: paleoenvironmental, stratigraphic, and paleoclimatic significance of terrestrial and freshwater ichnocoenoses. Sedimentary Geology 167 (2004) 177-268
45. Hasiotis S.T., Wellner R.W., Martin A.J., and Demko T.M. Vertebrate burrows from Triassic and Jurassic continental deposits of North America and Antarctica: their paleoenvironmental and paleoecological significance. Ichnos 11 (2004) 103-124
46. Hobbs H.H. The crayfishes of Georgia. Smithsonian Contributions to Zoology 318 (1981) 1-536
47. Hölldobler B., and Wilson E.O. The Ants (1990), Harvard University Press, Cambridge, Masschusetts 732 pp.
48. Horwitz P., and Knott B. The burrowing habit of the koonac Cherax plebeius (Decapoda: Parastacidae). West Australian Naturalist 15 (1983) 113-117
49. Horwitz P.H., Richardson A.M., and Boulton A. The burrow habitat of two sympatric species of land crayfish, Engaeus urostrictus and E. tuberculatus (Decapoda: Parastacidae). Victorian Naturalist 102 (1985) 188-197
50. Jacoby M. Observacoes e experiéncias sóbre Atta sexdens rubropilosa Forel visando facilitar seu combate. Boletim do Ministerio de Agricultura do Rio de Janeiro 12 (1944) 1-55
51. Jonkman J.C. The external and internal structure and growth of nests of the leaf-cutting ant Atta vollenweideri Forel, 1893 (Hym: Formicidae). Part II. Zeitschrift für Angewandte Entomologie 89 (1980) 217-246
52. Klappa C.F. Rhizoliths in terrestrial carbonates: classification, recognition, genesis and significance. Sedimentology 27 (1980) 613-629
53. Kraus M.J., and Hasiotis S.T. Significance of different modes of rhizolith preservation to interpreting paleoenvironmental and paleohydrologic settings: examples from Paleogene paleosols, Bighorn Basin, Wyoming, U.S.A. Journal of Sedimentary Research 76 (2006) 633-646
54. Lake P.S., and Newcombe K.J. Observations on the ecology of the crayfish Parastacoides tasmanicus (Decapoda: Parastacidae) from South-Western Tasmania. Australian Zoology 18 (1975) 197-214
55. Lamont B.B. Structure, ecology, physiology and root clusters - a review. Plant and Soil 248 (2003) 1-19
56. Laza J.H. Signos de actividad atribuibles a Atta (Myrmicidae) en el Mioceno de la Provincia de La Pampa, República Argentina. Significación paleozoogeográfica. Ameghiniana 19 (1982) 109-124
57. Lesta P.J. Estratigrafía de la Cuenca del Golfo de San Jorge. Actas de las Terceras Jornadas Geológicas Argentinas 1 (1968) 251-289
58. Loisy C., Verrecchia E.P., and Dufour P. Microbial origin for pedogenid micrite associated with a carbonate paleosol (Champagne, France). Sedimentary Geology 126 (1999) 193-204
59. Mariconi F.A. As Saúvas. Editora Agronómica Ceres, San Pablo (1970) 155 pp.
60. Martin L.D., and Bennett D.K. The burrows of the Miocene beaver Palaeocastor, Western Nebraska, U.S.A. Palaeogeography, Palaeoclimatology, Palaeoecology 221 (1977) 173-193
61. Matheny P.B., Curtis J.M., Hofstetter V., Aime M.C., Moncalvo J.M., Ge Z.W., Yang Z.L., Slot J.C., Ammirati J.F., Baroni T.J., Bougher N.L., Hughes K.W., Lodge D.J., Kerrigan R.W., Seidl M.T., Aanen D.K., DeNitis M., Daniele G.M., Desjardin D.E., Kropp B.R., Norvel L.L., Parker A., Vellinga E.C., Vilgalys R., and Hibbett D.S. Major clades of Agaricales: a multilocus phylogenetic overview. Mycologia 98 (2006) 982-995
62. Matheny, B., Moncalvo, J.M., Redhead, S.A., 2007. Agaricales. Version 09 May 2007. http://tolweb.org/Agaricales/20551/2007.05.09 in The Tree of Life Web Project, http://tolweb.org/.
63. Mayhé-Nunes A.J., and Jaffé K. On the biogeography of Attini (Hymenoptera: Formicidae). Ecotropicos 11 (1998) 45-54
64. Mikuláš R. Notes on the concept of plant trace fossils related to plant-generated sedimentary structures. Vestník Cěského Geologického Ústavu 74 (1999) 39-42
65. Moser J.C. Contents and structure of Atta texana nest in summer. Annals of the Entomological Society of America 56 (1962) 286-291
66. Mueller U.G., and Rabeling C. A breakthrough innovation in animal evolution. Proceedings of the National Academy of Sciences 105 (2008) 5287-5288
67. Mueller U.G., Rehner S.A., and Schultz T.R. The evolution of agriculture in ants. Science 281 (1998) 2034-2038
68. Mueller U.G., Schultz T.R., Currie C.R., Adams R.M., and Malloch D. The origin of the attine ant-fungus mutualism. Quarterly Review of Biology 76 (2001) 169-197
69. Mueller U.G., Gerardo N.M., Aanen D.K., Six D.L., and Schultz T.R. The evolution of agriculture in insects. Annual Review of Ecology and Evolutionary Systematic 36 (2005) 563-595
70. Mueller, U.G., Dash, D., Rabeling, C., Rodrigues, A., 2008. Coevolution between attine ants and actinomycete bacteria: a reevaluation. Evolution. 62, 2894-2912
71. Munkacsi A.B., Pan J.J., Villesen P., Mueller U.G., Blackwell M., and McLaughlin D.J. Convergent coevolution in the domestication of coral mushrooms by fungus-growing ants. Proceedings of the Royal Society of London B 271 (2004) 1777-1782
72. Musacchio E.A. Carófitas del Cretácico inferior en sedimentitas ̈chubutenses̈ al este de La Herrería, Chubut. Ameghiniana 9 (1972) 354-356
73. Musacchio E.A., and Chebli G. Ostrácodos no marinos y carófitas del Cretácido inferior en las provincias de Chubut y Neuquén, Argentina. Ameghiniana 12 (1975) 70-95
74. Nel A., Perrault G., Perrichot V., and Néraudeau D. The oldest ant in the Lower Cretaceous amber of Charente-Maritime (SW France) (Insecta: Hymenoptera: Formicidae). Geologica Acta 2 (2004) 23-29
75. Newmann G., and Martinoia E. Cluster roots - an underground adaptation for survival in extreme environments. Trends in Plant Science 7 (2002) 162-167
76. Peterson R.L., Massicotte H.B., and Melville L.H. Mycorrhizas: Anatomy and Cell Biology (2004), NRC Research Press, Otawa 173 pp.
77. Pochon J., De Barjac H., and Roche A. Recherches sur la digestion de la cellulose chez le termite Sphaerotermes sphaerothorax. Annales de l'lnstitut Pasteur 96 (1959) 352-355
78. Proserpio C.A. Descripción geológica de la Hoja 44e, Valle General Racedo, provincia del Chubut. Boletín de la Dirección Nacional de Minería y Geología 201 (1987) 1-92
79. Rabeling C., Verhaagh M., and Engels W. Comparative study of nest architecture and colony structure of the fungus-growing ants, Mycocepurus goeldii and M. smithii. Journal of Insect Science 7 (2007) article 40. (www.insectscience.org)
80. Richardson A.M. The effect of the burrows of a crayfish on the respiration of the surrounding soil. Soil Biology and Biochemistry 15 (1983) 239-242
81. Richardson A.M., and Wong V. The effect of a burrowing crayfish, Parastacoides sp., on the vegetation of Tasmanian wet Heathlands. Freshwater Crayfish 10 (1995) 174-182
82. Rouland-Lefévre C. Symbiosis with fungi. In: Abe T., Bignell D.E., and Higashi M. (Eds). Termites: Evolution, Sociality, Symbioses, Ecology (2000), Kluwer Academic, Dordrecht 289-306
83. Rudolph E.H. Aspectos fisicoquímicos del habitat y morfología de las galerias del camaron excavador Parastacus nicoletti (Philippi, 1882) (Decapoda: Parastacidae) en el sur de Chile. Gayana Zoología 61 (1997) 97-108
84. Sánchez-Peña S.R. New view on origin of attine ant-fungus mutualism: exploitation of a pre-existing insect-fungus symbiosis (Hymenoptera: Formicidae). Annals of the Entomological Society of America 98 (2005) 151-164
85. Schultz T.R. The fungus-growing ant genus Apterostigma in Dominican amber. In: Snelling, R.R., Fisher, B.L., Ward, P.S. (Eds). Advances in ant systematics (Hymenoptera: Formicidae): homage to E.O. Wilson-50 years of contributions. Memoirs of the American Entomological Institute 80 (2007) 425-436
86. Schultz T.R., and Brady S.G. Major evolutionary transitions in ant agriculture. Proceedings of the National Academy of Sciences 105 (2008) 5435-5440
87. Shane M.W., and Lambers H. Cluster roots: a curiosity in context. Pland and Soil 274 (2005) 101-125
88. Skene K.N. Cluster roots: some ecological considerations. Journal of Ecology 86 (1998) 1060-1064
89. Smith R. Helical burrow casts of therapsid origin from the Beaufort Group (Permian) of South Africa. Palaeogeography, Palaeoclimatology, Palaeoecology 60 (1987) 155-170
90. Somoza R., and Zaffarana C. Mid-Cretaceous polar standstill of South America, motion of the Atlantic hotspots and the birth of the Andean cordillera. Earth and Planetary Science Letters 271 (2008) 267-277
91. Suter P.J., and Richardson A.M. The biology of two species of Engaeus (Decapoda: Parastacidae) in Tasmania III. Habitat, food, associated fauna and distribution. Australian Journal of Marine and Freshwater Research 28 (1977) 95-103
92. Thorne B.L., Grimaldi D.A., and Krishna K. Early fossil history of the termites. In: Abe T., Bignell D.E., and Higashi M. (Eds). Termites: Evolution, Sociality, Symbioses, Ecology (2000), Kluwer Academic, Dordrecht 77-93
93. Verrecchia E.P., and Verrecchia K.E. Needle fiber calcite: a critical review and a proposed classification. Journal of Sedimentary Research 64 (1994) 650-664
94. Villesen P., Mueller U.G., Schultz T.R., Adams R.M., and Bouck A.M. Evolution of ant-cultivar specialization and cultivar switching in Apterostigma fungus growing ants. Evolution 58 (2004) 2252-2265
95. Weber N.A. Gardening Ants: The Attines (1972), The American Philosophical Society, Philadelphia 146 pp.
96. Wheeler W.M. Ants (1910), Columbia University Press, New York 663 pp.
97. Wright V.P. The role of fungal biomineralization in the formation of Early Carboniferous soil fabrics. Sedimentology 33 (1986) 831-838
98. Yelinek K., and Chin K. Probable dung beetle burrows associated with Daemonelix (beaver burrows) in the Miocene Harrison Formation, Nebraska, U.S.A. In: Bromley R.S., Buatois L.A., Mángano G., Genise J.F., and Melchor R.N. (Eds). Sediment-Organism Interactions: A Multifaceted Ichnology. SEPM Special Publication vol. 88 (2007) 345-352 Oklahoma
99. Zamith A.P., Mariconi F.A., and Paiva Castro U. Contribuiçáo para o conhecimento da "saúva mata pasto" Atta bispherica Forel 1908. Anais da Escola Superior de Agricultura "Luiz de Queiroz" 18 (1961) 327-338
100. Zolessi L.C., and Abenante Y.P. Nidificación y mesoetología de Acromyrmex en el Uruguay III. Acromyrmex (A.) hispidus Santschi, 1925 (Hymenoptera, Formicidae). Revista de Biología del Uruguay 1 (1973) 151-165
101. Zolessi L.C., and González L.A. Nidificación y mesoetología de Acromyrmex en el Uruguay II. Acromyrmex (Acromyrmex) lobicornis (Emery, 1887) (Hymenoptera, Formicidae). Revista de Biología del Uruguay 1 (1974) 37-57