Identification of Cichlid Fishes from Lake Malawi Using Computer Vision

Background The explosively radiating evolution of cichlid fishes of Lake Malawi has yielded an amazing number of haplochromine species estimated as many as 500 to 800 with a surprising degree of diversity not only in color and stripe pattern but also in the shape of jaw and body among them. As these morphological diversities have been a central subject of adaptive speciation and taxonomic classification, such high diversity could serve as a foundation for automation of species identification of cichlids. Methodology/Principal Finding Here we demonstrate a method for automatic classification of the Lake Malawi cichlids based on computer vision and geometric morphometrics. For this end we developed a pipeline that integrates multiple image processing tools to automatically extract informative features of color and stripe patterns from a large set of photographic images of wild cichlids. The extracted information was evaluated by statistical classifiers Support Vector Machine and Random Forests. Both classifiers performed better when body shape information was added to the feature of color and stripe. Besides the coloration and stripe pattern, body shape variables boosted the accuracy of classification by about 10%. The programs were able to classify 594 live cichlid individuals belonging to 12 different classes (species and sexes) with an average accuracy of 78%, contrasting to a mere 42% success rate by human eyes. The variables that contributed most to the accuracy were body height and the hue of the most frequent color. Conclusions Computer vision showed a notable performance in extracting information from the color and stripe patterns of Lake Malawi cichlids although the information was not enough for errorless species identification. Our results indicate that there appears an unavoidable difficulty in automatic species identification of cichlid fishes, which may arise from short divergence times and gene flow between closely related species.

[1]  Philippe Grosjean,et al.  Enumeration, measurement, and identification of net zooplankton samples using the ZOOSCAN digital imaging system , 2004 .

[2]  T. Kocher,et al.  A sympatric sibling species complex of Petrotilapia Trewavas from Lake Malawi analysed by enzyme electrophoresis (Pisces: Cichlidae) , 1982 .

[3]  Samy Bengio,et al.  Links between perceptrons, MLPs and SVMs , 2004, ICML.

[4]  K. R. Mckaye,et al.  GENETIC EVIDENCE FOR ALLOPATRIC AND SYMPATRIC DIFFERENTIATION AMONG COLOR MORPHS OF A LAKE MALAWI CICHLID FISH , 1984, Evolution; international journal of organic evolution.

[5]  Carol A. Stepien,et al.  Molecular systematics of fishes , 1998 .

[6]  T. Kocher,et al.  Speciation in rapidly diverging systems: lessons from Lake Malawi , 2001, Molecular ecology.

[7]  I. Kornfield,et al.  Hybrid origin of a cichlid population in Lake Malawi: implications for genetic variation and species diversity , 2003, Molecular ecology.

[8]  Andrew Rova,et al.  One Fish, Two Fish, Butterfish, Trumpeter: Recognizing Fish in Underwater Video , 2007, MVA.

[9]  W. Rice,et al.  LABORATORY EXPERIMENTS ON SPECIATION: WHAT HAVE WE LEARNED IN 40 YEARS? , 1993, Evolution; international journal of organic evolution.

[10]  Aimee E. Howe,et al.  Origins of Shared Genetic Variation in African Cichlids , 2012, Molecular biology and evolution.

[11]  I. Kornfield,et al.  Retention of an ancestral polymorphism in the Mbuna species flock (Teleostei: Cichlidae) of Lake Malawi , 1993 .

[12]  O. Seehausen,et al.  Disruptive sexual selection on male nuptial coloration in an experimental hybrid population of cichlid fish , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  Andrew Blake,et al.  "GrabCut" , 2004, ACM Trans. Graph..

[14]  I. Kornfield.  Evidence for rapid speciation in African cichlid fishes , 1978, Experientia.

[15]  J. Deutsch.  Colour diversification in Malawi cichlids: evidence for adaptation, reinforcement or sexual selection? , 1997 .

[16]  R. Nielsen,et al.  Using nuclear haplotypes with microsatellites to study gene flow between recently separated Cichlid species , 2004, Molecular ecology.

[17]  G. Turner,et al.  Repeated colonization and hybridization in Lake Malawi cichlids , 2011, Current Biology.

[18]  Vladimir Kolmogorov,et al.  "GrabCut": interactive foreground extraction using iterated graph cuts , 2004, ACM Trans. Graph..

[19]  J. Hey,et al.  On the origin of Lake Malawi cichlid species: A population genetic analysis of divergence , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[20]  T. Kocher,et al.  Phylogeny of a rapidly evolving clade: the cichlid fishes of Lake Malawi, East Africa. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Seehausen,et al.  Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection , 1999 .

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

[23]  Corinna Cortes,et al.  Support-Vector Networks , 1995, Machine Learning.

[24]  Fei Li,et al.  Classification of real and pseudo microRNA precursors using local structure-sequence features and support vector machine , 2005, BMC Bioinformatics.

[25]  T. Dayan,et al.  Ecological and community‐wide character displacement: the next generation , 2005 .

[26]  J. Streelman,et al.  Do constructional constraints influence cichlid craniofacial diversification? , 2007, Proceedings of the Royal Society B: Biological Sciences.

[27]  G. Turner,et al.  Isolation and characterization of microsatellite loci in the cichlid fish Pseudotropheus zebra , 1997, Molecular ecology.

[28]  D. Rujescu,et al.  Evidence of statistical epistasis between DISC1, CIT and NDEL1 impacting risk for schizophrenia: biological validation with functional neuroimaging , 2010, Human Genetics.

[29]  M. Arnegard,et al.  New markers for new species: microsatellite loci and the East African cichlids. , 2001, Trends in ecology & evolution.

[30]  Andrew Zisserman,et al.  Image Classification using Random Forests and Ferns , 2007, 2007 IEEE 11th International Conference on Computer Vision.

[31]  O. Seehausen,et al.  The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex) , 1998, Behavioral Ecology and Sociobiology.

[32]  D. R. Cutler,et al.  Utah State University From the SelectedWorks of , 2017 .

[33]  D. Schluter,et al.  Male–male competition and nuptial–colour displacement as a diversifying force in Lake Victoria cichlid fishes , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  Thomas W. Schoener,et al.  Resource Partitioning in Ecological Communities , 1974, Science.

[35]  I. Kornfield,et al.  AFRICAN CICHLID FISHES: Model Systems for Evolutionary Biology , 2000 .

[36]  Sang-Hee Lee,et al.  Butterfly species identification by branch length similarity entropy , 2012 .

[37]  Takakazu Ishimatsu,et al.  A Morphological Approach to Fish Discrimination , 1998, MVA.

[38]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.

[39]  M. Schneider,et al.  Speciation through sensory drive in cichlid fish , 2008, Nature.

[40]  Frank Storbeck,et al.  Fish species recognition using computer vision and a neural network , 2001 .

[41]  L. Sneddon,et al.  Guidelines for the treatment of animals in behavioural research and teaching , 2012, Animal Behaviour.

[42]  A. Konings.  Malaŵi cichlids in their natural habitat , 2001 .

[43]  Rasmus Larsen,et al.  Shape and Texture Based Classification of Fish Species , 2009, SCIA.

[44]  W. Pitts,et al.  A Logical Calculus of the Ideas Immanent in Nervous Activity (1943) , 2021, Ideas That Created the Future.

[45]  M. O'Neill,et al.  Automated species identification: why not? , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[46]  J. D. Fry,et al.  LABORATORY EXPERIMENTS ON SPECIATION , 2009 .

[47]  E. Hert.  Female choice based on egg-spots in Pseudotropheus aurora Burgess 1976, a rock-dwelling cichlid of Lake Malawi, Africa , 1991 .

[48]  C. Klingenberg.  MorphoJ: an integrated software package for geometric morphometrics , 2011, Molecular ecology resources.

[49]  Justin Talbot,et al.  Implementing GrabCut , 2004 .

[50]  Michael Mayo,et al.  Automatic species identification of live moths , 2006, Knowl. Based Syst..

[51]  Rui Li,et al.  Automated Classification of Skippers based on Parts Representation , 2008 .

[52]  M. Arnegard,et al.  DIVERGENCE WITH GENE FLOW IN THE ROCK‐DWELLING CICHLIDS OF LAKE MALAWI , 2000, Evolution; international journal of organic evolution.

[53]  Jung Uk Cho,et al.  Field Programmable Gate Array (FPGA) Based Fish Detection Using Haar Classifiers , 2009 .

[54]  I. Kornfield,et al.  CHAPTER 3 – Molecular Systematics of a Rapidly Evolving Species Flock: The mbuna of Lake Malawi and the Search for Phylogenetic Signal , 1997 .

[55]  G. Turner,et al.  Reproductive isolation among closely related Lake Malawi cichlids: can males recognize conspecific females by visual cues? , 1999, Animal Behaviour.

[56]  G. Turner,et al.  Laboratory mating trials indicate incipient speciation by sexual selection among populations of the cichlid fish Pseudotropheus zebra from Lake Malawi , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[57]  Shumeet Baluja,et al.  Large scale image-based adult-content filtering , 2006, VISAPP.

[58]  Kai Huang,et al.  Boosting accuracy of automated classification of fluorescence microscope images for location proteomics , 2004, BMC Bioinformatics.

[59]  T. Kocher.  Adaptive evolution and explosive speciation: the cichlid fish model , 2004, Nature Reviews Genetics.

[60]  J. Endler.  Gene Flow and Population Differentiation , 1973, Science.

[61]  Jeremy D. Raincrow,et al.  Nuclear gene variation and molecular dating of the cichlid species flock of Lake Malawi. , 2006, Molecular biology and evolution.

[62]  F. Rohlf,et al.  Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks , 1990 .

[63]  F. Rohlf,et al.  Ecological character displacement in Plethodon: biomechanical differences found from a geometric morphometric study. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[64]  J. Streelman,et al.  Hybridization and contemporary evolution in an introduced cichlid fish from Lake Malawi National Park , 2004, Molecular ecology.

[65]  E. Trewavas.  Nouvel examen des genres et sous-genres du complexe Pseudotropheus-Melanochromis du lac Malawi (Pisces, Perciformes, Cichlidae) , 1983 .

[66]  D. Delvaux.  AGE OF LAKE MALAWI (NYASA) AND WATER LEVEL FLUCTUATIONS , 1995 .

[67]  Chih-Jen Lin,et al.  Combining SVMs with Various Feature Selection Strategies , 2006, Feature Extraction.

[68]  Tae-Kun Seo,et al.  Classification of Nucleotide Sequences Using Support Vector Machines , 2010, Journal of Molecular Evolution.

[69]  Lorenzo Bruzzone,et al.  A Novel Transductive SVM for Semisupervised Classification of Remote-Sensing Images , 2006, IEEE Transactions on Geoscience and Remote Sensing.

[70]  D. Schluter,et al.  Ecological Character Displacement and Speciation in Sticklebacks , 1992, The American Naturalist.

[71]  I. Kornfield,et al.  Evolution of the mitochondrial DNA control region in the mbuna (Cichlidae) species flock of lake Malawi, East Africa , 1997, Journal of Molecular Evolution.

[72]  J. Losos.  Ecological character displacement and the study of adaptation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[73]  Thomas G. Dietterich,et al.  Automated insect identification through concatenated histograms of local appearance features: feature vector generation and region detection for deformable objects , 2007, 2007 IEEE Workshop on Applications of Computer Vision (WACV '07).

[74]  D. Adams,et al.  Body shape variation in relation to resource partitioning within cichlid trophic guilds coexisting along the rocky shore of Lake Malawi , 2003 .

[75]  Martin I. Taylor,et al.  Intraspecific sexual selection on a speciation trait, male coloration, in the Lake Victoria cichlid Pundamilia nyererei , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[76]  G. Turner,et al.  Divergent selection during speciation of Lake Malawi cichlid fishes inferred from parallel radiations in nuptial coloration , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[77]  Guannan Gao,et al.  Probabilistic Hough Transform , 2011 .