Starch granules identification and automatic classification based on an extended set of morphometric and optical measurements

Abstract Starch granules have been found to be preserved in association with archaeological remains and their identification may provide direct botanical evidences of the plants used by ancient humans. However, subtle morphological differences between starch granules make their taxonomic identifications difficult. In order to improve the identification of these plant remains, we used an image analysis program that measures up to 123 different optical and morphological characters. With Random Forest tests we analyzed ~ 5000 starch granules extracted from underground storage organs (USO), seeds, and fruits of 20 different East African edible plant species. Our results show that correct identification rates are up to 74% for some species ( Echinochloa colona, Cyperus rodundus) , ~ 80% for some suprageneric taxa (Poaceae, Fabaceae), and 80% for underground storage organs. However, on average, success rates are just ~ 53% for species (up to 70% with a dataset reduced to herbaceous species), 60% for families, and 72% for plant parts. Yet, this automated system is not perfect, but it is still more powerful than the human eye, for which the average success rate is just of 25% for species level identifications. We evaluated the performance of our system and found that accuracy rates of identifications of starch granules are highly sensitive to the number of groups (species) to identify (r 2  = 0.83) and, to a lesser extent to the number of characters used by the identification system (r 2  = 0.87). It is therefore crucial to narrow down as much as possible the number of target species, by analyzing additional proxies. We conclude that better results can be achieved if the candidate field is narrowed. If not, the automated identification of starch granules will remain unsatisfactory to provide acceptable interpretations in archaeological contexts.

[1]  C. R. Peters Shell strength and primate seed predation of nontoxic species in eastern and southern Africa , 1993, International Journal of Primatology.

[2]  Zhou Guangming,et al.  Starch grain analysis reveals Late Neolithic plant utilization in the middle reaches of the Ganjiang River , 2012 .

[3]  F. Marlowe,et al.  Tubers as fallback foods and their impact on Hadza hunter-gatherers. , 2009, American journal of physical anthropology.

[4]  I. Rovner On transparent blindfolds: Comments on identifying maize in Neotropical sediments and soils using cob phytoliths , 2004 .

[5]  Y. Gally,et al.  Optical measurements to determine the thickness of calcite crystals and the mass of thin carbonate particles such as coccoliths , 2014, Nature Protocols.

[6]  L. Aiello,et al.  The Expensive-Tissue Hypothesis: The Brain and the Digestive System in Human and Primate Evolution , 1995, Current Anthropology.

[7]  P Dardenne,et al.  Classification of modified starches by fourier transform infrared spectroscopy using support vector machines. , 2005, Journal of agricultural and food chemistry.

[8]  S. Copeland Vegetation and plant food reconstruction of lowermost Bed II, Olduvai Gorge, using modern analogs. , 2007, Journal of human evolution.

[9]  Mark Horrocks,et al.  Evidence for introduced taro (Colocasia esculenta) and lesser yam (Dioscorea esculenta) in Lapita-era (c. 3050–2500 cal. yr BP) deposits from Bourewa, southwest Viti Levu Island, Fiji , 2007 .

[10]  M. Maslin,et al.  Early Human Speciation, Brain Expansion and Dispersal Influenced by African Climate Pulses , 2013, PloS one.

[11]  S. Moyà-Solà,et al.  Dietary Specialization during the Evolution of Western Eurasian Hominoids and the Extinction of European Great Apes , 2014, PloS one.

[12]  J. Yravedra,et al.  Earliest Porotic Hyperostosis on a 1.5-Million-Year-Old Hominin, Olduvai Gorge, Tanzania , 2012, PloS one.

[13]  Matthew J. Collins,et al.  Automated Classification of Starch Granules Using Supervised Pattern Recognition of Morphological Properties , 2010 .

[14]  D. Pearsall,et al.  Root and tuber phytoliths and starch grains document manioc (Manihot esculenta) arrowroot (Maranta arundinacea) and llerén (Calathea sp.) at the real alto site Ecuador , 2006, Economic Botany.

[15]  Luc Beaufort,et al.  Automatic recognition of coccoliths by dynamical neural networks , 2004 .

[16]  L. Wadley,et al.  Microscopic residues as evidence of hafting on backed tools from the 60 000 to 68 000 year-old Howiesons Poort layers of Rose Cottage Cave, South Africa , 2004 .

[17]  M. L. Robertson,et al.  Evolutionary perspectives on human nutrition: The influence of brain and body size on diet and metabolism , 1994, American journal of human biology : the official journal of the Human Biology Council.

[18]  E. Baquedano,et al.  Phytoliths infer locally dense and heterogeneous paleovegetation at FLK North and surrounding localities during upper Bed I time, Olduvai Gorge, Tanzania , 2010, Quaternary Research.

[19]  Robin Torrence,et al.  Identification of starch granules using image analysis and multivariate techniques , 2004 .

[20]  R.M. Haralick,et al.  Statistical and structural approaches to texture , 1979, Proceedings of the IEEE.

[21]  D. Pearsall,et al.  Maize can still be identified using phytoliths: response to Rovner , 2004 .

[22]  Richard Potts,et al.  Hominin evolution in settings of strong environmental variability , 2013 .

[23]  Max Kuhn,et al.  Applied Predictive Modeling , 2013 .

[24]  Xinhua Zhuang,et al.  Image Analysis Using Mathematical Morphology , 1987, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[25]  F. Diez-Martín,et al.  New insights into hominin lithic activities at FLK North Bed I, Olduvai Gorge, Tanzania , 2010, Quaternary Research.

[26]  Q. Ge,et al.  Starch grain analysis reveals function of grinding stone tools at Shangzhai site, Beijing , 2009 .

[27]  M. Lombard Distribution Patterns of Organic Residues on Middle Stone Age Points from Sibudu Cave, Kwazulu-Natal, South Africa , 2004 .

[28]  A. Varki Loss of N‐glycolylneuraminic acid in humans: Mechanisms, consequences, and implications for hominid evolution , 2002, American journal of physical anthropology.

[29]  Hans Beeckman,et al.  First archaeological evidence of banana cultivation in central Africa during the third millennium before present , 2001 .

[30]  Anne-Béatrice Dufour,et al.  The ade4 Package: Implementing the Duality Diagram for Ecologists , 2007 .

[31]  F. Diez-Martín,et al.  Paleoenvironmental and paleoecological reconstruction of a freshwater oasis in savannah grassland at FLK North, Olduvai Gorge, Tanzania , 2010, Quaternary Research.

[32]  M. Bruno,et al.  Diversity of cultivars and other plant resources used at habitation sites in the Llanos de Mojos, Beni, Bolivia: evidence from macrobotanical remains, starch grains, and phytoliths , 2012 .

[33]  Peter J. A. Shaw,et al.  Multivariate Statistics for the Environmental Sciences , 2003 .

[34]  Tim J. Bennett,et al.  Middle Stone Age starch acquisition in the Niassa Rift, Mozambique , 2008, Quaternary Research.

[35]  D. Piperno Identifying crop plants with phytoliths (and starch grains) in Central and South America: A review and an update of the evidence , 2009 .

[36]  J. Cui,et al.  Identification of starch granules using a two-step identification method , 2014 .

[37]  J. Yravedra,et al.  Was FLK North levels 1–2 a classic “living floor” of Oldowan hominins or a taphonomically complex palimpsest dominated by large carnivore feeding behavior? , 2010, Quaternary Research.

[38]  L. Alcalá,et al.  Woodworking activities by early humans: a plant residue analysis on Acheulian stone tools from Peninj (Tanzania). , 2001, Journal of human evolution.

[39]  D. Pearsall,et al.  Maize in ancient Ecuador: results of residue analysis of stone tools from the Real Alto site , 2004 .

[40]  P. Goldberg,et al.  Middle Stone Age Bedding Construction and Settlement Patterns at Sibudu, South Africa , 2011, Science.

[41]  A. Coster,et al.  What starch grain is that? – A geometric morphometric approach to determining plant species origin , 2015 .

[42]  Michael J. Rogers,et al.  Cutmarked bones from Pliocene archaeological sites at Gona, Afar, Ethiopia: implications for the function of the world's oldest stone tools. , 2005, Journal of human evolution.

[43]  M. Teaford,et al.  Diet and the evolution of the earliest human ancestors. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[44]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[45]  T. Hayakawa,et al.  Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Zhong-Zhen Zhao,et al.  A novel and effective multistage classification system for microscopic starch grain images , 2009, Microscopy research and technique.

[47]  D. Dollfus,et al.  Fat neural network for recognition of position-normalised objects , 1999, Neural Networks.

[48]  M. Domínguez‐Rodrigo Meat-eating by early hominids at the FLK 22 Zinjanthropus site, Olduvai Gorge (Tanzania): an experimental approach using cut-mark data. , 1997, Journal of human evolution.

[49]  Richard Fullagar,et al.  Integrating Phytoliths within Use-Wear/Residue Studies of Stone Tools , 1999 .

[50]  P Colonna,et al.  Starch granules: structure and biosynthesis. , 1998, International journal of biological macromolecules.

[51]  J. Mercader Mozambican Grass Seed Consumption During the Middle Stone Age , 2009, Science.

[52]  Z. Alemseged,et al.  Diet of Australopithecus afarensis from the Pliocene Hadar Formation, Ethiopia , 2013, Proceedings of the National Academy of Sciences.

[53]  D. Pearsall,et al.  Identifying maize in neotropical sediments and soilsusing cob phytoliths , 2003 .

[54]  R. Fullagar,et al.  Clues to Stone Tool Function Re-examined: Comparing Starch Grain Frequencies on Used and Unused Obsidian Artefacts , 1998 .

[55]  Jill Thompson,et al.  The 'human revolution' in lowland tropical Southeast Asia: the antiquity and behavior of anatomically modern humans at Niah Cave (Sarawak, Borneo). , 2007, Journal of human evolution.

[56]  Leo Breiman,et al.  Random Forests , 2001, Machine Learning.

[57]  Richard Fullagar,et al.  Early and mid Holocene tool-use and processing of taro (Colocasia esculenta), yam (Dioscorea sp.) and other plants at Kuk Swamp in the highlands of Papua New Guinea , 2006 .