Comparative analysis of optional hunting behavior in Cricetinae hamsters using the data compression approach.

Behavioral sequences Data compression Evolution Hamsters Homogeneity Hunting

Journal

Frontiers in zoology
ISSN: 1742-9994
Titre abrégé: Front Zool
Pays: England
ID NLM: 101231669

Informations de publication

Date de publication:
15 Jul 2024
Historique:
received: 15 11 2023
accepted: 09 07 2024
medline: 16 7 2024
pubmed: 16 7 2024
entrez: 15 7 2024
Statut: epublish

Résumé

Research into the hunting behavior in members of the Cricetidae family offers an opportunity to reveal what changes in the predatory behavioral sequences occur when a rodent species shifts from an omnivorous to a predatory lifestyle. The study tests the following hypotheses: are there phylogenetic differences in the divergence of species' predatory lifestyles in hamsters or do ecological factors lead to shaping their hunting behavior? We applied the data compression approach for performing comparative analysis of hunting patterns as biological "texts." The study presents a comparative analysis of hunting behaviors in five Cricetinae species, focusing on the new data obtained for the desert hamster Phodopus roborovskii whose behavior has never been studied before. The hunting behavior of P. roborovskii appeared to be the most variable one. In contrast, behavioral sequences in P. campbelli and Allocricetulus curtatus display more significant order and predictability of behavior during hunting. Optional hunting behavior in the most ancient species P. roborovskii displayed similarities with obligate patterns in "young" Allocricetulus species. It thus turned out to be the most advanced hunter among members of the Phodopus genus. Differences in hunting sequences among Phodopus representatives suggest that the hunting behavior of these species, despite its optional mode, was subject to selection during species splitting within the genus. These results did not reveal the role played by phylogenetic differences in the divergence of species' predatory lifestyles. They suggested that ecological conditions are the main factors in speciation of the hunting behavior in hamsters.

Identifiants

pubmed: 39010094
doi: 10.1186/s12983-024-00540-4
pii: 10.1186/s12983-024-00540-4
doi:

Types de publication

Journal Article

Langues

eng

Pagination

19

Subventions

Organisme : Russian Science Foundation
ID : 22-74-00079

Informations de copyright

© 2024. The Author(s).

Références

JrSO L. The Rodentia as omnivores. Q Rev Biol. 1970;45:351–72.
doi: 10.1086/406647
Langley WM. Specializations in the predatory behavior of grasshopper mice (Onychomys leucogaster and O. torridus): A comparison with the golden hamster (Mesocricetus auratus). J Comp Psychol. 1987;101:322.
doi: 10.1037/0735-7036.101.4.322
Langley WM. Comparison of predatory behaviors of deer mice (Peromyscus maniculatus) and grasshopper mice (Onychomys leucogaster). J Comp Psychol. 1994;108:394.
doi: 10.1037/0735-7036.108.4.394
Rowe AH, Rowe MP. Physiological resistance of grasshopper mice (Onychomys spp.) to Arizona bark scorpion (Centruroides exilicauda) venom. Toxicon. 2008;52:597–605.
pubmed: 18687353 doi: 10.1016/j.toxicon.2008.07.004
Sarko DK, Leitch DB, Girard I, Sikes RS, Catania KC. Organization of somatosensory cortex in the Northern grasshopper mouse (Onychomys leucogaster), a predatory rodent. J Comp Neurol. 2011;519:64–74.
pubmed: 21120928 pmcid: 3064439 doi: 10.1002/cne.22504
Rowe AH, Xiao Y, Rowe MP, Cummins TR, Zakon HH. Voltage-gated sodium channel in grasshopper mice defends against bark scorpion toxin. Science. 2013;342:441–6.
pubmed: 24159039 pmcid: 4172297 doi: 10.1126/science.1236451
Timberlake W, Washburne DL. Feeding ecology and laboratory predatory behavior toward live and artificial moving prey in seven rodent species. Anim Learn Behav. 1989;17:2–11.
doi: 10.3758/BF03205206
Konczal M, Koteja P, Orlowska-Feuer P, Radwan J, Sadowska ET, Babik W. Genomic response to selection for predatory behavior in a mammalian model of adaptive radiation. Mol Biol Evol. 2016;33:2429–40.
pubmed: 27401229 doi: 10.1093/molbev/msw121
Reznikova Z, Levenets J, Panteleeva S, Ryabko B. Studying hunting behaviour in the striped field mouse using data compression. Acta Ethol. 2017;20:165–73.
doi: 10.1007/s10211-017-0260-9
Rowe KC, Achmadi AS, Esselstyn JA. Repeated evolution of carnivory among Indo-Australian rodents. Evolution. 2016;70:653–65.
pubmed: 26826614 doi: 10.1111/evo.12871
Arregoitia LD, D’Elía G. Classifying rodent diets for comparative research. Mamm Rev. 2021;51:51–65.
doi: 10.1111/mam.12214
Arregoitia LD, Fisher DO, Schweizer M. Morphology captures diet and locomotor types in rodents. R Soc Open Sci. 2017;4: 160957.
doi: 10.1098/rsos.160957
Langley WM. Development of predatory behaviour in the southern grasshopper mouse (Onychomys torridus). Behaviour. 1986;99:275–95.
doi: 10.1163/156853986X00586
Polsky RH. The Ontogeny of Predatory Behaviour in the Golden Hamster (Mesocricetus a. auratus). Behaviour. 1977;61:26–56.
doi: 10.1163/156853977X00478
Reznikova Z, Levenets J, Panteleeva S, Novikovskaya A, Ryabko B, Feoktistova N, Gureeva A, Surov A. Using the data-compression method for studying hunting behavior in small mammals. Entropy. 2019;21:368.
pubmed: 33267082 pmcid: 7514852 doi: 10.3390/e21040368
Langley WM. Evolutionary changes in the predatory attack of carnivorous rodents: A comparative analysis emphasizing grasshopper mice (Onychomys spp.). J Comp Psychol. 2021;135:114–26.
pubmed: 33555907 doi: 10.1037/com0000257
Eisenberg JF, Leyhausen P. The Phylogenesis of Predatory Behavior in Mammals. Z Tierpsychol. 1972;30:59–93.
pubmed: 5063891 doi: 10.1111/j.1439-0310.1972.tb00844.x
Carleton MD, Eshelman RE. A Synopsis of Fossil Grasshopper Mice, Genus Onychomys, and their Relationships to Recent Species. Claude W. Hibbard Memorial Volume VII. Pap Palaeontol. 1979;7:1–63.
Vorontsov NN. Nizshie khomyakoobraznye (Cricetidae) mirovoi fauny (Lower Cricetidae (Cricetidae) of the World Fauna), Ch. 1, in series Fauna SSSR (Fauna of the USSR): Mlekopitayushchie (Mammals). Leningrad: Nauka; 1982.
Vorontsov NN. The ways of food specialization and evolution of the alimentary system in Muroidea. In Symposium Theriologicum. Prague: Publ House Czeck. Acado Sci; 1962. p. 360–77.
Feoktistova NY. Khomyachki roda Phodopus. Sistematika, filogeografiya, ekologiya, fiziologiya, povedenie, khimicheskaya kommunikatsiya (Hamsters of the Genus Phodopus: Taxonomy, Phylogeography, Ecology, Physiology, Behavior, and Chemical Communication). Moscow: KMK; 2008.
Feoktistova NY, Kropotkina MV, Potashnikova EV, Gureeva AV, Kuznetsova EV, Surov AV. Speciation in Allopatric Species of the Hamster Subfamily Cricetinae (Rodentia, Cricetidae). Biol Bull Russ Acad Sci. 2019;9:230–42.
Müller D, Hauer J, Schöttner K, Fritzsche P, Weinert D. Seasonal adaptation of dwarf hamsters (Genus Phodopus): differences between species and their geographic origin. J Comp Physiol B. 2015;185:917–30.
pubmed: 26323343 doi: 10.1007/s00360-015-0926-4
Neumann K, Michaux J, Lebedev V, Yigit N, Colak E, Ivanova N, Poltoraus A, Surov A, Markov G, Maak S, Naumann S, Gattermann R. Molecular phylogeny of the Cricetinae subfamily based on the mitochondrial cytochrome b and 12S rRNA genes and the nuclear vWF gene. Mol Phylogenet Evol. 2006;39:135–48.
pubmed: 16483801 doi: 10.1016/j.ympev.2006.01.010
Lebedev VS, Bannikova AA, Neumann K, Ushakova MV, Ivanova NV, Surov AV. Molecular phylogenetics and taxonomy of dwarf hamsters Cricetulus Milne-Edwards, 1867 (Cricetidae, Rodentia): description of a new genus and reinstatement of another. Zootaxa. 2018;4387:331–49.
pubmed: 29689907 doi: 10.11646/zootaxa.4387.2.5
Levenets JV, Panteleeva SN, Reznikova ZI, Gureeva AV, Feoktistova NY, Surov AV. Experimental comparative analysis of hunting behavior in four species of Cricetinae hamsters. Biol Bull Russ Acad Sci. 2019;46:1182–91.
doi: 10.1134/S1062359019090097
Levenets J, Novikovskaya A, Panteleeva S, Reznikova Z, Ryabko B. Using Data-Compressors for Classification Hunting Behavioral Sequences in Rodents as “Ethological Texts.” Mathematics. 2020;8:579.
doi: 10.3390/math8040579
Ryabko B, Reznikova Z, Druzyaka A, Panteleeva S. Using ideas of Kolmogorov complexity for studying biological texts. Theory Comput Syst. 2013;52:133–47.
doi: 10.1007/s00224-012-9403-6
Ryabko B, Guskov A, Selivanova I, Using data-compressors for statistical analysis of problems on homogeneity testing and classification. In,. IEEE International Symposium on Information Theory (ISIT), Aachen. Germany. 2017;2017:121–5.
Kolynchuk A. “Phodopus roborovskii” (On-line), Animal Diversity Web. 2015. Accessed 27 Aug 2023. http://animaldiversity.org/accounts/Phodopus_roborovskii/ .
Ramachandran V, Joshi M, Ambekar M, Charoo SA, Ramakrishnan U. The desert hamster Phodopus roborovskii (Satunin, 1903) (Rodentia, Cricetidae) from north-western Tibetan plateau, Ladakh, India: an addition to the mammalian fauna of the Indian subcontinent. Mammalia. 2020;84:253–8.
doi: 10.1515/mammalia-2018-0199
Wilson DE, Reeder D. Mammal Species of the World: A Taxonomic and Geographic Reference. Baltimore: J. Hopkins Univ. Press; 2005.
doi: 10.56021/9780801882210
Reznikova Z, Panteleeva S, Novikovskaya A, Levenets J, Lopatina N, Litvinov Y. Flexibility and rigidity in hunting behaviour in rodents: is there room for cognition? Anim Cogn. 2022;25:731–43.
pubmed: 34993671 doi: 10.1007/s10071-021-01588-z
Mohan K, Das S, Singh M. Leaf dicers of Nelliyampathy: Observations of preconsumptive latex avoidance by a sciurid. Ecology. 2024;105:e4294.
pubmed: 38558226 doi: 10.1002/ecy.4294
Kendall M, Stuart A. The advanced theory of statistics. Inference and relationship. 3rd ed. London: Griffin; 1961.
Casarrubea M, Sorbera F, Crescimanno G. Multivariate data handling in the study of rat behavior: an integrated approach. Behav Res Methods. 2009;41:772–81.
pubmed: 19587191 doi: 10.3758/BRM.41.3.772
Vermeij GJ. Unsuccessful predation and evolution. Am Nat. 1982;120:701–20.
doi: 10.1086/284025
Bissett C, Bernard RTF. Habitat selection and feeding ecology of the cheetah (Acinonyx jubatus) in thicket vegetation: is the cheetah a savanna specialist? J Zool. 2007;271:310–7.
doi: 10.1111/j.1469-7998.2006.00217.x
Wilson AM, Lowe JC, Roskilly K, Hudson PE, Golabek KA, McNutt JW. Locomotion dynamics of hunting in wild cheetahs. Nature. 2013;498:185–9.
pubmed: 23765495 doi: 10.1038/nature12295
Panteleeva SN, Levenets JV, Novikovskaya AA, Reznikova ZI, Lopatina NV, Litvinov YN. Experimental Investigations of Hunting Behavior in the Mountain Voles Alticola strelzowi and Alticola Tuvinicus (Rodentia, Cricetidae). Biol Bull Russ Acad Sci. 2020;47:1059–65.
doi: 10.1134/S1062359020080099
Ryurikov GB, Tolstov IV, Surov AV. Sexual and aggressive patterns in behavior of 7 hamster species in captivity. Adv Ethol Suppl. 2004;38:77.
Ruffer DG. Agonistic behavior of the northern grasshopper mouse (Onychomys leucogaster breviauritus). J Mammal. 1968;49:481–7.
pubmed: 5691424 doi: 10.2307/1378206
Sherbrooke WC. Predatory behavior of captive greater roadrunners feeding on horned lizards. Wilson Bull. 1990;102:171–4.

Auteurs

J Levenets (J)

Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, Novosibirsk, 630091, Russia. jan.levenets@gmail.com.

S Panteleeva (S)

Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, Novosibirsk, 630091, Russia.
Novosibirsk State University, Novosibirsk, 630090, Russia.

Zh Reznikova (Z)

Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, Novosibirsk, 630091, Russia.
Novosibirsk State University, Novosibirsk, 630090, Russia.

A Gureeva (A)

A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 119071, Russia.

V Kupriyanov (V)

A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 119071, Russia.

N Feoktistova (N)

A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 119071, Russia.

A Surov (A)

A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 119071, Russia.

Classifications MeSH