Feel the heat: The effect of temperature on development, behavior and central pattern generation in 3rd instar Calliphora vicina larvae

Journal of Insect Physiology

Volumn 57, Issue 1, 2011, Pages 136-146

  Hückesfeld, Sebastian ^a   Niederegger, Senta ^b   Schlegel, Philipp ^a   Heinzel, H G ^a   Spieß, Roland ^a  

^a UNIVERSITY OF BONN   (Germany)

^b JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Diptera larvae; Fictive feeding; Pattern generation; Temperature

Indexed keywords

ADAPTIVE RADIATION; BEHAVIORAL ECOLOGY; DEVELOPMENTAL BIOLOGY; FEEDING BEHAVIOR; FLY; GENERATION TIME; HEAT BALANCE; LARVA; PHYSIOLOGICAL RESPONSE; SENSITIVITY ANALYSIS; TEMPERATURE EFFECT; TEMPERATURE GRADIENT;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; CENTRAL NERVOUS SYSTEM; FEEDING BEHAVIOR; FLY; GROWTH, DEVELOPMENT AND AGING; HEAT; LARVA; MOTOR ACTIVITY; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM; DIPTERA; FEEDING BEHAVIOR; HOT TEMPERATURE; LARVA; MOTOR ACTIVITY;

ANIMALIA; CALLIPHORA VICINA; DIPTERA;

EID: 78650206575     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2010.10.002     Document Type: Article

References (65)

1. Ameismeier F., Loftus R. Response characteristics of cold cell on the antenna of Locusta migratoria L. Journal of Comparative Physiology A 1988, 163:507-516.
2. Amrein H., Thorne N. Gustatory perception and behavior in Drosophila melanogaster. Current Biology 2005, 15:673-684.
3. Anderson G.S. Minimum and maximum development rates of some forensically important Calliphoridae (Diptera). Journal of Forensic Sciences 2000, 45:824-832.
4. Arbas E., Calabrese R. Rate modification in the heartbeat central pattern generator of the medicinal leech. Journal of Comparative Physiology A 1984, 155:783-794.
5. Armstrong G., Robertson R. A role for octopamine in coordinating thermoprotection of an insect nervous system. Journal of Thermal Biology 2006, 31:149-158.
6. Barclay J., Atwood H., Robertson R. Impairment of central pattern generation in Drosophila cysteine string protein mutants. Journal of Comparative Physiology A 2002, 188:71-78.
7. Benjamin P., Rose R., Slade C., Lacy M. Morphology of identified neurones in the buccal ganglia of Lymnaea stagnalis. The Journal of Experimental Biology 1979, 80:119-135.
8. Berrigan D., Pepin D. How maggots move: allometry and kinematics of crawling in larval diptera. Journal of Insect Physiology 1995, 41:329-337.
9. Bolwig N. Senses and sense organs of the anterior end of the house fly larvae. Videnskabelige Meddelelser Dansk Naturhistorisk Forening 1946, 109:81-217.
10. Büschges A. Sensory control and organization of neural networks mediating coordination of multisegmental organs for locomotion. Journal of Neurophysiology 2005, 93:1127-1135.
11. Cattaert D., Birman S. Blockade of the central generator of locomotor rhythm by noncompetitive NMDA receptor antagonists in Drosophila larvae. The Journal of Neurobiology 2001, 48:58-73.
12. Charabidze D., Bourel B., Leblanc H., Hedouin V., Gosset D. Effect of body length and temperature on the crawling speed of Protophormia terranovae larvae (Robineau-Desvoidy) (Diptera Calliphoridae). Journal of Insect Physiology 2008, 54:529-533.
13. Dasari S., Cooper R. Modulation of sensory-CNS-motor circuits by serotonin, octopamine, and dopamine in semi-intact Drosophila larva. Neuroscience Research 2004, 48:221-227.
14. Davis E. Temperature response of antennal receptors of the mosquito, Aedes aegypti. Journal of Comparative Physiology 1975, 96:223-236.
15. Decolmyn F. Neural basis of rhythmic behavior in animals. Science 1980, 210:492-498.
16. Dhaka A., Viswanath V., Patapoutian A. TRP ion channels and temperature sensation. Annual Reviews of Neuroscience 2006, 29:135-161.
17. Donovan S., Hall M., Turner B., Moncrieff C. Larval growth rates of the blowfly, Calliphora vicina over a range of temperatures. Medical and Veterinary Entomology 2006, 20:106-114.
18. Eisenhart F., Cacciatore T.W.K. A central pattern generator underlies crawling in the medicinal leech. Journal of Comparative Physiology A 2000, 186:631-643.
19. Fox L., Soll D., Wu C. Coordination and modulation of locomotion pattern generators in Drosophila larvae: effects of altered biogenic amine levels by the tyramine b hydroxylase mutation. The Journal of Neuroscience 2006, 26:1486-1498.
20. Gödde J., Haug T. Analysis of the electrical responses of antennal thermo- and hygroreceptors of Antheraea (Saturniidae, Lepidoptera) to thermal, mechanical, and electrical stimuli. Journal of Comparative Physiology A 1990, 167:391-401.
21. Godoy-Herrera R, Santander R., Figueroa J. A developmental and biometrical analysis of larval photoresponse of Drosophila. Animal Behaviour 1994, 48:251-262.
22. Grassberger M., Reiter C. Effect of temperature on development of forensically important holarctic blow fly Protophormia terraenovae (Robineau-Desvoidy) (Diptera: Calliphoridae). Forensic Science International 2002, 128:177-182.
23. Green C., Burnet B., Connolly K. Organization and pattern of inter- and intraspecific variation in the behaviour of Drosophila larvae. Animal Behaviour 1983, 31:282-291.
24. Hamada F., Rosenzweig M., Kang K., Pulver S., Ghezzi A., Jegla T., Garrity P. An internal thermal sensor controlling temperature preference in Drosophila. Nature 2008, 454:217-222.
25. Hendel T., Michels B., Neuser K., Schipanski A., Kaun K., Sokolowski M., Marohn F., Michel R., Heisenberg M., Gerber B. The carrot not the stick: appetitive rather than aversive gustatory stimuli support associative olfactory learning in individually assayed Drosophila larvae. Journal of Comparative Physiology A 2005, 191:265-279.
26. Honda I., Ishikawa Y., Matsumoto Y. Electrophysiological studies on the antennal olfactory cells of the onion fly, Hylemya antiqua MEIGEN (Diptera: Anthomyiidae). Applied Entomology and Zoology 1987, 22:417-423.
27. Janssen R. Thermal influence on nervous system function. Neuroscience and Biobehavioral Reviews 1992, 16:399-413.
28. Klose M., Chu D., Xiao C., Seroude L., Robertson R. Heat shock-mediated thermoprotection of larval locomotion comprised by ubiquitous overexpression of Hsp70 in Drosophila melanogaster. Journal of Neurophysiology 2005, 94:3563-3572.
29. Liu L., Yermolaieva O., Johnson W., Abboud F., Welsh M. Identification and function of thermosensory neurons in Drosophila larvae. Nature Neuroscience 2003, 6:267-273.
30. Loftus R. The response of the antennal cold receptor of Periplaneta americana to rapid temperature changes and to steady temperature. Zeitschrift für vergleichdende Physiologie 1968, 59:413-455.
31. Loftus R. Differential thermal components in the response of the antennal cold receptor of Periplaneta americana in slowly changing temperature. Zeitschrift für vergleichdende Physiologie 1969, 63:415-433.
32. Loftus R., Corbiere-Tichane G. Antennal warm and cold receptors of the cave beetle, Speophyes lucidulus Delar., in sensilla with a lammellated dendrite. I: Response to sudden temperature change. Journal of Comparative Physiology A 1981, 143:443-452.
33. MacKay-Lyons M. Central pattern generation of locomotion: a review of the evidence. Physical Therapy 2002, 82:69-83.
34. Marder E. Senseless motion. Nature 2002, 416:131-132.
35. Marder E., Bucher D. Central pattern generators and the control of rhythmic movements. Current Biology 2001, 11:R986-R996.
36. Marder E., Bucher D., Schulz D., Taylor A. Invertebrate central pattern generation moves along. Current Biology 2005, 15:658-699.
37. Marder E., Calabrese R. Principles of rhythmic motor pattern generation. Physiological Reviews 1996, 76:687-717.
38. McKemy D., Neuhauser W., Julius D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 2002, 416:52-58.
39. Montgomery J., Macdonald J. Effects of temperature on nervous system: implications for behavioral performance. The American Journal of Physiology 1990, 259:191-196.
40. Must A., Merivee E., Luik A., Mänd M., Heidemaa M. Responses of antennal campaniform sensilla to rapid temperature changes in ground beetles of the tribe platynini with different habitat preferences and daily activity rhythmus. Journal of Insect Physiology 2006, 52:506-513.
41. Must A., Merivee E., Mänd M., Luik A., Heidemaa M. Electrophysiological responses of the antennal campaniform sensilla to rapid changes of temperature in the ground beetles Pterostichus oblongopunctatus and Poecilus cupreus (tribe Pterostichini) with different ecological preferences. Physiological Entomology 2006, 31:278-285.
42. Niederegger S., Pastuscheck J., Mall G. Preliminary studies on the influence of fluctuating temperatures on the development of various forensically relevant flies. Forensic Science International 2010, 199:72-78.
43. Nishikawa M., Yokohari F., Ishibashi T. The antennal thermoreceptor of the camel cricket, Tachycines asynamorus. Journal of Insect Physiology 1985, 31:517-524.
44. Oppliger F., Guerin P., Vlimant M. Neurophysiological and behavioural evidence for an olfactory function for the dorsal organ and a gustatory one for the terminal organ in Drosophila melanogaster larvae. Journal of Insect Physiology 2000, 56:135-144.
45. Patapoutian A., Peier A., Story G., Viswanath V. Thermotrop channels and beyond: mechanisms of temperature sensation. Nature Reviews Neuroscience 2003, 4:529-539.
46. Reingold S., Gelperin A. Feeding motor programme in Limax. II: Modulation by sensory input in intact animals and isolated central nervous system. The Journal of Experimental Biology 1980, 85:1-19.
47. Reiter C. Zum Wachstumsverhalten der Maden der blauen Schmeißfliege Calliphora vicina. Zeitschrift für Rechtsmedizin 1984, 91:295-308.
48. Reye D., Pearson K. Entrainment of the locust central flight oscillator by wing stretch receptor stimulation. Journal of Comparative Physiology A 1988, 162:77-89.
49. Rosenzweig M., Brennan K., Tayler T., Phelps P., Patapoutian A., Garrity P. The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes and Development 2005, 19:419-424.
50. Sawin E., Harris L., Campos A., Sokolowski M. Sensorimotor transformation from light reception to phototactic behavior in Drosophila larvae (Diptera: Drosophilidae). Journal of Insect Behavior 1994, 7:553-567.
51. Schipanski A., Yarali A., Niewalda T., Gerber B. Behavioral analyses of sugar processing in choice, feeding, and learning in larval Drosophila. Chemical Senses 2008, 33:563-573.
52. Schmitz H., Schmitz A., Bleckmann H. A new type of infrared organ in the Australian " fire beetle" Merimna atrata (Coleoptera: Buprestidae). Naturwissenschaften 2000, 87:542-545.
53. Schmitz H., Trenner S. Electrophysiological characterization of the multipolar thermoreceptors in the " fire-beetle" Merimna atrata and comparison with the infrared sensilla of Melanophila acuminata (both Coleoptera, Buprestidae). Journal of Comparative Physiology A 2003, 189:715-722.
54. Schoofs A., Hanslik U., Niederegger S., Heinzel H.-G., Spieß R. The thoracic muscular system and its innervation in third instar Calliphora vicina larvae. II: Projection patterns of the nerves associated with the pro- and mesothorax and the pharyngeal complex. Journal of Morphology 2010, 271:969-979.
55. Schoofs A., Niederegger S., Ooyen A.v., Heinzel H.-G., Spieß R. The brain can eat: establishing the existence of a central pattern generator for feeding in third instar larvae of Drosophila virilis and Drosophila melanogaster. Journal of Insect Physiology 2010, 56:695-705.
56. Schoofs A., Niederegger S., Spieß R. From behavior to fictive feeding: anatomy, innervation and activation pattern of pharyngeal muscles of Calliphora vicina 3rd instar larvae. Journal of Insect Physiology 2009, 55:218-230.
57. Shetreat-Klein A, Cropper E. Afferent induced changes in rhythmic motor programs in the feeding circuitry of Aplysia. Journal of Neurophysiology 2004, 92:2312-2322.
58. Slone D., Gruner S. Thermoregulation in larval aggregations of carrion-feeding blow flies (Diptera: Calliphoridae). Journal of Medical Entomology 2007, 44:516-523.
59. Smarandache C., Daur N., Hedrich U., Stein W. Regulation of motor pattern frequency by reversals in proprioceptive feedback. European Journal of Neuroscience 2008, 28:460-474.
60. Song W., Onishi M., Jan L.Y., Jan Y.N. Peripheral multidentricic sensory neurons are necessary for rhythmic locomotion behavior in Drosophila larvae. Proceedings of the National Academy of Sciences 2007, 104:5199-5204.
61. Spieß R., Schoofs A., Heinzel H. Anatomy of the stomatogastric nervous system associated with the foregut in Drosophila melanogaster and Calliphora vicina third instar larvae. Journal of Morphology 2008, 269:272-282.
62. Tichy H. Hygro- and thermoreceptive triad in antennal senillum of the stick insect, Carausius morosus. Journal of Comparative Physiology A 1979, 132:149-152.
63. Warzecha A., Horstmann W., Egelhaaf M. Temperature-dependence of neuronal performance in the motion pathway of the blowfly Calliphora erythrocephala. The Journal of Experimental Biology 1999, 202:3161-3170.
64. Wendler G. The influence of proprioceptive feedback on locust flight co-ordination. The Journal of Comparative Physiology 1974, 88:173-200.
65. Xu H., Robertson R. Neural parameters contributing to temperature compensation in the flight CPG of the locust, Locusta migratoria. Brain Research 1996, 734:213-222.