Foraging Ecology Predicts Learning Performance in Insectivorous Bats

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Clarin, Theresa M A ^a   Ruczyński, Ireneusz ^a,b   Page, Rachel A ^c   Siemers, Björn M ^a  

^a MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^b MAMMAL RESEARCH INSTITUTE   (Poland)

^c Smithonian Trop Research Institute   (Panama)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BAT; CONTROLLED STUDY; ECOLOGICAL NICHE; ECOLOGICAL SPECIALIZATION; EXPLORATORY BEHAVIOR; FORAGING BEHAVIOR; LEARNING; MALE; MAZE TEST; MENTAL PERFORMANCE; MYOTIS CAPACCINII; MYOTIS EMARGINATUS; MYOTIS MYOTIS; NONHUMAN; REWARD; SKILL; SPECIES DIFFERENCE; TASK PERFORMANCE; WORKING MEMORY; ADAPTIVE BEHAVIOR; ANIMAL; CARNIVORY; COGNITION; ECOSYSTEM; PHYSIOLOGY; PREDATION; PSYCHOLOGY;

ANIMALIA; MAMMALIA; MYOTIS; MYOTIS CAPACCINII; MYOTIS EMARGINATUS; MYOTIS MYOTIS;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; CARNIVORY; CHIROPTERA; COGNITION; ECOSYSTEM; MAZE LEARNING; PREDATORY BEHAVIOR; SPECIES SPECIFICITY;

EID: 84878747475     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064823     Document Type: Article

References (68)

1. Overington SE, Dubois F, Lefebvre L, (2008) Food unpredictability drives both generalism and social foraging: a game theoretical model. Behavioral Ecology 19: 836-841.
2. Parker S, Gibson K, (1977) Object manipulation, tool use and sensorimotor intelligence as feeding adaptations in Cebus monkeys and great apes. Journal of Human Evolution 6: 623-641.
3. Rozin P, Kalat JW, (1971) Specific hungers and poison avoidance as adaptive specializations of learning. Psychological Review 78: 459-486.
4. Dukas R, Ratcliffe JM (2009) Introduction. In: Dukas R, Ratcliffe JM, editors. Cognitive Ecology II. Chicago: University Of Chicago Press.
5. Mettke-Hofmann C, Gwinner E, (2003) Long-term memory for a life on the move. Proceedings of the National Academy of Sciences of the United States of America 100: 5863-5866.
6. Gibson BM, Kamil AC, (2005) The fine-grained spatial abilities of three seed-caching corvids. Learning & behavior 33: 59-66.
7. Micheli F, (1997) Effects of experience on crab foraging in a mobile and a sedentary species. Animal behaviour 53: 1149-1159.
8. Day L, Crews D, Wilczynski W, (1999) Spatial and reversal learning in congeneric lizards with different foraging strategies. Animal behaviour 57: 393-407.
9. Haupt M, Eccard J, Winter Y, (2010) Does spatial learning ability of common voles (Microtus arvalis) and bank voles (Myodes glareolus) constrain foraging efficiency? Animal cognition 13: 783-791.
10. Godfrey-Smith P (2001) Environmental complexity and the evolution of cognition. In: Sternberg R, Kaufman J, editors. The evolution of intelligence. Mahwah, New Jersey: Lawrence Erlbaum Associates London. pp.223-250.
11. Tebbich S, Stankewitz S, Teschke I, (2012) The relationship between foraging, learning abilities and neophobia in two species of Darwin's finches. Ethology 118: 135-146.
12. Simmons NB (2005) Order Chiroptera. In: Wilson DE, Reeder DM, editors. Mammal species of the world: a taxonomic and geographic reference, vol 1. Baltimore: John Hopkins University Press. pp.312-529.
13. Simmons NB, (2005) An Eocene big bang for bats. Science 307: 527-528.
14. Norberg UM, Rayner JM, (1987) Ecolocigal morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philosophical Transactions of the Royal Society B 316: 335-427.
15. Jones G, Holderied MW, (2007) Bat echolocation calls: adaptation and convergent evolution. Proceedings of the Royal Society B 274: 905-912.
16. Jones G, Teeling EC, (2006) The evolution of echolocation in bats. Trends in Ecology & Evolution 21: 149-156.
17. Schnitzler H-U, Moss C, Denzinger A, (2003) From spatial orientation to food acquisition in echolocating bats. Trends in Ecology & Evolution 18: 386-394.
18. Weinbeer M, Kalko EKV, (2007) Ecological niche and phylogeny: the highly complex echolocation behavior of the trawling long-legged bat, Macrophyllum macrophyllum. Behavioral Ecology and Sociobiology 61: 1337-1348.
19. Meyer CFJ, Weinbeer M, Kalko EKV, (2005) Home-range size and spacing patterns of Macrophyllum macrophyllum (Phyllostomidae) foraging over water. Journal of Mammalogy 86: 587-598.
20. Kalko EKV, Schnitzler H-U, (1989) The echolocation and hunting behavior of Daubenton's bat, Myotis daubentoni. Behavioral Ecology and Sociobiology 24: 225-238.
21. Schnitzler H-U, Kalko EKV, Kaipf I, Grinnell AD, (1994) Fishing and echolocation behavior of the greater bulldog bat, Noctilio leporinus, in the field. Behavioral Ecology and Sociobiology 35: 327-345.
22. Siemers BM, (2001) Finding prey by associative learning in gleaning bats: experiments with a Nattereŕs bat Myotis nattereri. Acta Chiropterologica 3: 211-215.
23. Safi K, Dechmann DKN, (2005) Adaptation of brain regions to habitat complexity: a comparative analysis in bats (Chiroptera). Proceedings of the Royal Society B 272: 179-186.
24. Boonman AM, Boonman M, Bretschneider F, Van de Grind WA, (1998) Prey detection in trawling insectivorous bats: duckweed affects hunting behaviour in Daubenton's bat, Myotis daubentonii. Behavioral Ecology and Sociobiology 44: 99-107.
25. Siemers BM, Stilz P, Schnitzler H-U, (2001) The acoustic advantage of hunting at low heights above water: behavioural experiments on the European "trawling" bats Myotis capaccinii, M. dasycneme and M. daubentonii. The Journal of experimental biology 204: 3843-3854.
26. Siemers BM, Baur E, Schnitzler H-U, (2005) Acoustic mirror effect increases prey detection distance in trawling bats. Die Naturwissenschaften 92: 272-276.
27. Greif S, Siemers BM (2010) Innate recognition of water bodies in echolocating bats. Nature communications 1: DOI: 10.1038/ncomms1110. doi:10.1038/ncomms1110.
28. Ciechanowski M, Zaja{ogonek}c T, Zielińska A, Dunajski R, (2010) Seasonal activity patterns of seven vespertilionid bat species in Polish lowlands. Acta Theriologica 55: 301-314.
29. Ciechanowski M, Zaja{ogonek}c T, Biłas A, Dunajski R, (2007) Spatiotemporal variation in activity of bat species differing in hunting tactics: effects of weather, moonlight, food abundance, and structural clutter. Canadian Journal of Zoology 85: 1249-1263.
30. Almenar D, Aihartza J, Goiti U, Salsamendi E, Garin I, (2006) Habitat selection and spatial use by the trawling bat Myotis capaccinii (Bonaparte, 1837). Acta Chiropterologica 8: 157-167.
31. Biscardi S, Russo D, Casciani V, Cesarini D, Mei M, et al. (2007) Foraging requirements of the endangered long-fingered bat: the influence of micro-habitat structure, water quality and prey type. Journal of Zoology 273: 372-381.
32. Jones PL, Page RA, Hartbauer M, Siemers BM, (2010) Behavioral evidence for eavesdropping on prey song in two Palearctic sibling bat species. Behavioral Ecology and Sociobiology 65: 333-340.
33. Arlettaz R, (1996) Feeding behaviour and foraging strategy of free-living mouse-eared bats, Myotis myotis and Myotis blythii. Animal Behaviour 51: 1-11.
34. Goerlitz HR, Siemers BM, (2007) Sensory ecology of prey rustling sounds: acoustical features and their classification by wild grey mouse lemurs. Functional Ecology 21: 143-153.
35. Arlettaz R, Perrin N, Hausser J, (1997) Trophic resource partitioning and competition between the two sibling bat species Myotis myotis and Myotis blythii. Journal of animal ecology 66: 897-911.
36. Russo D, Jones G, Arlettaz R, (2007) Echolocation and passive listening by foraging mouse-eared bats Myotis myotis and M. blythii. The Journal of Experimental Biology 210: 166-176.
37. Siemers BM, Güttinger R, (2006) Prey conspicuousness can explain apparent prey selectivity. Current biology 16: R157-R159.
38. Schnitzler H-U, Kalko EKV, (2001) Echolocation by insect-eating bats. BioScience 51: 557-569.
39. Siemers BM, Schnitzler H-U, (2004) Echolocation signals reflect niche differentiation in five sympatric congeneric bat species. Nature 429: 657-661.
40. Wang J, Kanwal J, Zhang C, Jiang T, Lu G, et al. (2010) Seasonal habitat use by greater horseshoe bat Rhinolophus ferrumequinum (Chiroptera: Rhinolophidae) in Changbai Mountain temperate forest, Northeast China. Mammalia 74: 257-266.
41. Flaquer C, Puig-Montserrat X, Burgas A, Russo D, (2008) Habitat selection by Geoffroýs bats (Myotis emarginatus) in a rural Mediterranean landscape: implications for conservation. Acta Chiropterologica 10: 61-67.
42. Krull D, Schumm A, Metzner W, Neuweiler G, (1991) Foraging areas and foraging behavior in the notch-eared bat, Myotis emarginatus (Vespertilionidae). Behavioral Ecology and Sociobiology 28: 247-253.
43. Schumm A, Krull D, Neuweiler G, (1991) Echolocation in the notch-eared bat, Myotis emarginatus. Behavioral Ecology and Sociobiology 28: 255-261.
44. Zahn A, Bauer S, Kriner E, Holzhaider J, (2009) Foraging habitats of Myotis emarginatus in Central Europe. European Journal of Wildlife Research 56: 395-400.
45. Stadelmann B, Lin L-K, Kunz TH, Ruedi M, (2007) Molecular phylogeny of New World Myotis (Chiroptera, Vespertilionidae) inferred from mitochondrial and nuclear DNA genes. Molecular phylogenetics and evolution 43: 32-48.
46. Page RA, Von Merten S, Siemers BM, (2012) Associative memory or algorithmic search: A comparative study on learning strategies of bats and shrews. Animal cognition 15: 495-504.
47. Ruczynski I, Siemers BM, (2011) Hibernation does not affect memory retention in bats. Biology letters 7: 153-155.
48. Canadian Council On Animal Care (2003) CCAC species-specific recommendations on: BATS: 1-9. Available: http://www.ccac.ca/Documents/Standards/Guidelines/Add_PDFs/Wildlife_Bats.pdf. Accessed 2013 April 24.
49. R Development Core Team (2012) R: A language and environment for statistical computing. Available: http://www.r-project.org/Accessed 2013 April 24.
50. Dunn OJ, (1964) Multiple comparisons using rank sums. Technometrics 6: 241-252.
51. Bitterman ME, (1975) The comparative analysis of learning- are the laws of learning the same in all animals? Science 188: 699-709.
52. Tsoar A, Nathan R, Bartan Y, Vyssotski A, Dell'Omo G, et al. (2011) Large-scale navigational map in a mammal. Proceedings of the National Academy of Sciences of the United States of America 108: 718-724.
53. Levin E, Barnea A, Yovel Y, Yom-Tov Y, (2006) Have introduced fish initiated piscivory among the long-fingered bat? Mammalian Biology- Zeitschrift für Säugetierkunde 71: 139-143.
54. Aihartza J, Almenar D, Salsamendi E, Goiti U, Garin I, (2008) Fishing behaviour in the long-fingered bat Myotis capaccinii (Bonaparte, 1837): an experimental approach. Acta Chiropterologica 10: 287-301.
55. Aihartza J, Goiti U, Alemar D, Garin I, (2003) Evidences of piscivory by Myotis capaccinii (Bonaparte, 1837) in southern Iberian Peninsula. Acta chiropterologica 5: 193-198.
56. Verbeek M, Drent P, Wiepkema P, (1994) Consistent individual differences in early exploratory behaviour of male great tits. Animal Behaviour 48: 1113-1121.
57. Benus R, Bohus B, Koolhaas J, Van Oortmerssen GA, (1991) Heritable variation for aggression as a reflection of individual coping strategies. Experientia 47: 1008-1019.
58. Ruiz-Gomez MDL, Huntingford FA, Øverli Ø, Thörnqvist P-O, Höglund E, (2011) Response to environmental change in rainbow trout selected for divergent stress coping styles. Physiology & behavior 102: 317-322.
59. Dingemanse NJ, De Goede P, (2004) The relation between dominance and exploratory behavior is context-dependent in wild great tits. Behavioral Ecology 15: 1023-1030.
60. Ratcliffe JM, Fenton MB, Shettleworth SJ, (2006) Behavioral flexibility positively correlated with relative brain volume in predatory bats. Brain, behavior and evolution 67: 165-176.
61. Eisenberg J, Wilson D, (1978) Relative brain size and feeding strategies in the Chiroptera. Evolution 32: 740-751.
62. Reader SM, Laland KN, (2002) Social intelligence, innovation, and enhanced brain size in primates. Proceedings of the National Academy of Sciences of the United States of America 99: 4436-4441.
63. Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L, (2005) Big brains, enhanced cognition, and response of birds to novel environments. Proceedings of the National Academy of Sciences of the United States of America 102: 5460-5465.
64. Lefebvre L, Sol D, (2008) Brains,lifestyles and cognition: are there general trends? Brain, behavior and evolution 72: 135-144.
65. Krapp F, Niethammer J, editors (2011) Die Fledermäuse Europas. 1st ed. Wiebelsheim: AULA-Verlag GmbH.
66. Byrne RW, Bates LA, (2007) Sociality, evolution and cognition. Current biology 17: R714-723.
67. Dietz C, Von Helversen O, Nill D (2009) Bats of Britain, Europe and Northwest Africa. 1st ed. London: A & C Black Publishers Ltd.
68. Henry M, Stoner KE, (2011) Relationship between spatial working memory performance and diet specialization in two sympatric nectar bats. PLoS ONE 6: e23773 doi:10.1371/journal.pone.0023773.