Integrating temperature-dependent life table data into Insect Life Cycle Model for predicting the potential distribution of Scapsipedus icipe Hugel & Tanga
Autoři:
Magara H. J. Otieno aff001; Monica A. Ayieko aff001; Saliou Niassy aff002; Daisy Salifu aff002; Azrag G. A. Abdelmutalab aff002; Khamis M. Fathiya aff002; Sevgan Subramanian aff002; Komi K. M. Fiaboe aff003; Nana Roos aff004; Sunday Ekesi aff002; Chrysantus M. Tanga aff002
Působiště autorů:
School of Agriculture and Food Security, Jaramogi Oginga Odinga University Science and Technology (JOOUST), Bondo, Kenya
aff001; International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya
aff002; The International Institute of Tropical Agriculture (IITA), B.P. 2008 (Messa), Nkolbisson, Yaoundé, Cameroon
aff003; University of Copenhagen, Department of Nutrition, Exercise and Sports, Rolighedsvej, Frederiksberg C, Denmark
aff004
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222941
Souhrn
Scapsipedus icipe Hugel and Tanga (Orthoptera: Gryllidae) is a newly described edible cricket species. Although, there is substantial interest in mass production of S. icipe for human food and animal feed, no information exists on the impact of temperature on their bionomics. Temperature-dependent development, survival, reproductive and life table parameters of S. icipe was generated and integrated into advanced Insect Life Cycle Modeling software to describe relative S. icipe population increase and spatial spread based on nine constant temperature conditions. We examined model predictions and implications for S. icipe potential distribution in Africa under current and future climate. These regions where entomophagy is widely practiced have distinctly different climates. Our results showed that S. icipe eggs were unable to hatch at 10 and 40°C, while emerged nymphs failed to complete development at 15°C. The developmental time of S. icipe was observed to decrease with increased in temperature. The lowest developmental threshold temperatures estimated using linear regressions was 14.3, 12.67 and 19.12°C and the thermal constants for development were 185.2, 1111.1- and 40.7-degree days (DD) for egg, nymph and pre-adult stages, respectively. The highest total fecundity (3416 individuals/female/generation), intrinsic rate of natural increase (0.075 days), net reproductive rate (1330.8 female/female/generation) and shortest doubling time (9.2 days) was recorded at 30°C. The regions predicted to be suitable by the model suggest that S. icipe is tolerant to a wider range of climatic conditions. Our findings provide for the first-time important information on the impact of temperature on the biology, establishment and spread of S. icipe across the Africa continent. The prospect of edible S. icipe production to become a new sector in food and feed industry is discussed.
Klíčová slova:
Insects – Death rates – Africa – Sex ratio – Oviposition – Nymphs – Crickets – Fecundity
Zdroje
1. Halloran A. Edible insects in sustainable food systems. Eds. Flore Roberto, Vantomme Paul, and Roos Nanna. Springer. 2018.
2. Kelemu S, Niassy S, Torto B, Fiaboe K, Affognon H, Tonnang H, Maniania NK, Ekesi S. African edible insects for food and feed: inventory, diversity, commonalities and contribution to food security. JIFF. 2015; 1(2): 103–119.
3. Orinda MA, Mosi RO, Ayieko MA, Amimo FA. Growth performance of Common house cricket (Acheta domesticus) and field cricket (Gryllus bimaculatus) crickets fed on agro-byproducts. J Entomol Zool Stud. 2017; 5(5): 1138–1142.
4. FAO. Edible insects: Future Prospects for feed and food security. FAO Publication, 2013.
5. Ayieko MA, Ogola HJ, Ayieko IA. Introducing rearing crickets (gryllids) at household levels: adoption, processing and nutritional value. Journal of Insects as Food and Feed, Wageningen Academic Publishers. 2016; http://dx.doi.org/10.3920/JIFF2015.0080.
6. Münke-Svendsen C, Halloran A, Orina MA, Oloo JA, Magara HJO, Manyara NE, Ayieko MA, Ekesi S, Roos N. Insect production systems for food and feed in Kenya. GREEiNSECT Technical Brief #2. Copenhagen, Denmark. 2017.
7. Homman AM, Ayieko AM, Konyole SO, Roos N. Acceptability of biscuits containing 10% cricket (Acheta domesticus) compared to milk biscuits among 5-10-year-old Kenyan school children. JIFF. 2017; 3 (2): 95–103. https://doi.org/10.3920/JIFF2016.0054.
8. Tanga C, Magara HJO, Ayieko AM, Copeland RS, Khamis FM, Mohamed SA, Ombura FLO, Niassy S, Subramanian S, Fiaboe KKM, Roos N, Ekesi S, Hugel S. A new edible cricket species from Africa of the genus Scapsipedus. Zootaxa. 2018a; 4486 (3): 383–392. https://doi.org/10.11646/zootaxa.4486.3.9.
9. Magara HJ, Tanga CM, Ayieko MA, Hugel S, Mohamed SA, Khamis FM, Salifu D, Niassy S, Subramanian S, Fiaboe KMK and Roos N. Performance of Newly Described Native Edible Cricket Scapsipedus icipe (Orthoptera: Gryllidae) on Various Diets of Relevance for Farming. J Econ Entomol. 2019; 112(2): 653–664. doi: 10.1093/jee/toy397 30657915
10. Van Huis A. Potential of insects as food and feed in assuring food security. Annu Rev Entomol. 2013; 58: 563–83. doi: 10.1146/annurev-ento-120811-153704 23020616
11. Van Huis A, Van itterbeck J, Heetkamp MJW, Van den Brand H, Van Loon JJA. An exploration of greenhouse gas and ammonia production by insects’ species suitable for animal or human consumption. PloS ONE. 2010; 5(12).
12. Nyaga P. Good biosecurity practices in small scale commercial and scavenging production systems in Kenya. Rome: FAO. 2007; 157.
13. Pascucci S, Dentoni D, Mitsopoulus D. The perfect storm of business venturing? The case of entomology-based venture creation. Int J Food Agric Econ. 2015; 3(9): doi: 10.1186/s40100-014-0025-y
14. Yang PJ, Carey JR, Dowell RV. Temperature influences the development and demography of Bactrocera dorsalis (Diptera: Tephritidae) in China. Environ Entomol. 1994; 23: 971–974.
15. Hassall C, Thompson DJ, French GC, Harvey IF. Historical changes in the phenology of British odonata are related to climate. Glob Chang Biol. 2007; 13: 83–95.
16. Jaworski T, Hilszczański J. The effect of temperature and humidity changes on insect development and their impact on forest ecosystems in the context of expected climate change. For. Res. Pap. 2013; 74(4): 345–355.
17. Khadioli N, Tonnang ZEH, Muchugu E, Ong'amo G, Achia T, Kipchirchir I, Kroschel J, Le Ru B. Effect of temperature on the phenology of Chilo partellus (Swinhoe) (Lepidoptera, Crambidae); simulation and visualization of the potential future distribution of C. partellus in Africa under warmer temperatures through the development of life-table parameters. Bull Entomol Res. 2014; 104: 809–822. doi: 10.1017/S0007485314000601 25229840
18. Azrag GAA, Murungi LK, Tonnang HEZ, Mwenda D, Babin R. Temperature-dependent models of development and survival of an insect pest of African tropical highlands, the coffee antestia bug Antestiopsis thunbergii (Hemiptera: Pentatomidae). J. Therm. Biol. 2017; 70: 27–36. doi: 10.1016/j.jtherbio.2017.10.009 29108555
19. Stinner RE, Gutierrez AP, Butler GD. An Algorithm for Temperature-Dependent Growth Rate Simulation 1 2. Can Entomol. 1974; 106(5): 519–524.
20. Goodman D. Optimal life histories, optimal notation, and the value of reproductive value. Am. Nat. 1982; 119: 803–823.
21. Wagner TL, Olson RL, Willers JL. Modelling arthropod development time. J. Agric Entomol. 1991; 8: 251–270.
22. Brièere JF, Pracros P, Le Roux AY, Pierre JS. A novel rate model for temperature-dependent development for arthropods. Environ. Entomol. 1999; 28: 22–29.
23. Allahyari H. Decision making with degree-day in control program of Colorado potato beetle. PhD dissertation, University of Tehran, Tehran, Iran. 2005.
24. Wagner TL, Wu HI, Sharpe PJH, Schoolfield RM, Coulson RN. Modelling insect development rats: a literature review and application of the biophysical model. Ann Entomol Soc Am. 1984; 77: 208–225.
25. Worner SP. Performance of phenological models under variable temperature regimes: consequences of the Kaufmann or rate summation effect. Environ. Entomol. 1992; 21: 689–699.
26. Logan JA, Wollkind DJ, Hoyt SC, Tanigoshi LK. An analytical model for the description of temperature dependent rate phenomena in arthropods. Environ. Entomol. 1976; 5: 1133–1140.
27. Sharpe PJH, DeMichele DW. Reaction kinetics of poikilotherm development. J Theor Biol. 1977; 64: 649–670. doi: 10.1016/0022-5193(77)90265-x 846210
28. Roy M, Brodeur J, Cloutier C. Relationship between temperature and developmental rate of Stethorus punctillum (Coleoptera: Coccinellidae) and its prey Tetranychus mcdanieli (Acarina: Tetranychidae). Environ. Entomol. 2002; 31: 177–187.
29. Ma L, Wang X, Liu Y, Su MZ, Huang GH. Temperature effects and fecundity of Brachia macroscopa (Lepidoptera: Gelechiidae). PLoS ONE. 2017; 12(3) e0173065. doi: 10.1371/journal.pone.0173065 28253321
30. Sporleder M, Kroschel J., Quispe MRG, Lagnaoui A. A temperature-based simulation model for the potato tuberworm, Phthorimaea operculella Zeller (Lepidoptera; Gelechiidae). Environ. Entomol. 2004; 33: 477–486.
31. Melissa K. Herp Care Collection. Breeding and Raising the House Cricket. 2014: 1–5.
32. Wineriter SA, Walker TJ. Group and individual rearing of field crickets (Orthoptera: Gryllidae). J Entomol. News. 1988; 99: 53–62.
33. Clifford CW, Woodring JP. Methods for rearing the house cricket, Acheta domesticus (L.), along with baseline values for feeding rates, growth rates, development times, and blood composition. J Appl Entomol. 1990; 109: 1–14.
34. Yoshikazu CS, Yuka S, Shin-ichi A. Effects of body size and shape on mating frequency in the Brachypterous Grasshopper Podisma sapporensis. J. Orthoptera Res. 2008; 7(2): 243–248.
35. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2017: URL 〈https://www.R-project.org/〉.
36. Tonnang EZH, Juarez H, Carhuapoma P, Gonzales JC, Mendoza D, Sporleder M, Simon R, Kroschel J. ILCYM–insect life cycle modelling. A software package for developing temperature-based insect phenology models with applications for local, regional and global analysis of insect population and mapping. International Potato Center. 2013: 193.
37. Régnière. A method of describing and using variability in development rates of the simulation of insect phenology. Can Entomol. 1984; 116: 1367–1376.
38. Campbell A, Frazer BD, Gilber N, Guitierrez AP, Macauer. Temperature requirements of some aphids and their parasites. J Appl Ecol. 1974; 11: 431–438.
39. Akaike H. A new look at the statistical model identification. IEEE Transactions on Automatic Control. 1974; 19: 716–723.
40. Marquardt DW. An algorithm for least-squares estimation of non-linear parameters. J. Soc. Ind. Appl. MATH. 1963; 11: 431–441.
41. Wang R, Lan Z, Ting Y. Studies on mathematical models of the relationship between insect development and temperature. Acta Ecol. Sin. 1982; 2: 47–57.
42. Bonnar JD. The Gamma Function. Seattle, USA. Create Space Independent Publishing Platform. 2010.
43. Hilbert DW, Logan JA. Empirical model of nymphal development for the migratory grasshopper, Melanoplus sanguinipes (Orthoptera: Acrididae). Environ Entomol. 1983: 12(1): 1–5.
44. Curry GL, Feldman RM, Smith KC. A stochastic model of a temperature-dependent population. Theor Popul Biol. 1978; 13: 197–213. 694782
45. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high-resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 2005; 25: 1965–1978.
46. IPCC (Intergovernmental Panel on Climate Change). Climate Change 2007: Impacts, Adaptation and Vulnerability. The contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom. 2007.
47. Govindasamy B, Buffy PB, Coquard J. High-resolution simulations of global climate, part 2: effects of increased greenhouse gases. Clim Dyn. 2003; 21: 391–404.
48. Ramirez J, Jarvis A. Downscaling Global Circulation Model Outputs: The Delta Method. Decision and Policy Analysis Working Paper No. 1: International Center for Tropical Agriculture (CIAT), Cali, Colombia. 2010.
49. Logan JA, Régnière J, Powell JA. Assessing the impacts of global warming on forest pest dynamics. Front Ecol Environ. 2003; 1: 130–137.
50. Børge JD, Overgaard J, Malte H, Gianotten J. Role of temperature on growth and metabolic rate in the tenebrionid beetles Alphitobius diaperinus and Tenebrio molitor. J. Insect Physiol. 2018; 107; 89–96. doi: 10.1016/j.jinsphys.2018.02.010 29477466
51. Roe RM, Clifford CW, Woodring JP. The effect of temperature on feeding, growth, and metabolism during the last larval stadium of the female house cricket, Acheta domesticus. J. Insect Physiol. 1980; 26(9): 639–644.
52. Booth DT, Kiddell K. Temperature and the energetics of development in the house cricket (Acheta domesticus). J. Insect Physiol. 2007; 53: 950–953. doi: 10.1016/j.jinsphys.2007.03.009 17481649
53. Adamo SA, Lovett MME. Some like it hot: the effects of climate change on reproduction, immune function and disease resistance in the cricket Gryllus texensis. J Exp Biol. 2011; 214: 1997–2004. doi: 10.1242/jeb.056531 21613515
54. Chemura A, Musundire R, Chiwona-Karltun L. Modelling habitat and spatial distribution of the edible insect Henicus whellani Chop (Orthoptera: Stenopelmatidae) in south-eastern districts of Zimbabwe. JIFF. 2018; 4(4): 229–238.
55. Merkel G. The effects of temperature and food quality on the larval development of Gryllus bimaculatus (Orthoptera, Gryllidae). Oecologia. 1977; 30(2): 129–140. doi: 10.1007/BF00345416 28309428
56. Masaki S, Walker TJ. Cricket life cycles. J Evol Biol. 1987; 121: 349–423.
57. Ghouri ASK, McFarlane JE. Observations on the development of crickets. Can Entomol. 1958; 90(3): 158–165.
58. Bate J. Life history of Acheta domesticus (Insecta Orthoptera Gryllidae). Pedobiologia. 1971; 11: 159–172.
59. Kraus WF. Is male back space limiting? An investigation into the demography of the giant water bug Abedus indentatus (Heteroptera: Belostomatidae). J Insect Behav. 1989; 2: 623–648.
60. Kruse KC. Male backspace availability in the giant waterbug {Belosloma Jlumineum Say). Behav Ecol Sociobiol. 1990; 26: 281–289.
61. Régnière J, Powell J, Bentz B, Nealis V. Effect of temperature on the development, survival and reproduction of insects: Experimental design, data analysis and modelling. J. Insect Physiol. 2012; 58: 634–647. doi: 10.1016/j.jinsphys.2012.01.010 22310012
62. Bowling CC. The biology of the house cricket Acheta domesticus. M.S. Thesis. University of Arkansas, Fayetteville, USA. 1955.
63. Howe RW. Temperature effects on embryonic development in insects. Annu Rev Entomol. 1967; 12(1): 15–42.
64. Tanga CM, Khamis FM, Tonnang HE, Rwomushana I, Mosomtai G, Mohamed SA, Ekesi S. Risk assessment and spread of the potentially invasive Ceratitis rosa Karsch and Ceratitis quilicii De Meyer, Mwatawala & Virgilio sp. Nov. using life-cycle simulation models: Implications for phytosanitary measures and management. PloS one. 2018; 13(1): p.e0189138. doi: 10.1371/journal.pone.0189138 29304084
65. Soh BSB, Kekeunou S, Nanga NS, Dongmo M, Rachid. Effect of temperature on the biological parameters of the cabbage aphid Brevicoryne brassicae. J Ecol Evol. 2018; 1–13. doi: 10.1002/ee3.4639
66. Vargas RI, Walsh WA, Kanehisa D, Stark JD, Nishida T. Comparative demography of three Hawaiian fruit flies (Diptera: Tephritidae) at alternating temperatures. Ann Entomol Soc Am. 2000; 93: 75–81.
67. Kaspi R, Mossinson S, Drezner T, Kamensky B, Yuval B. Effects of larval diet on development rates and reproductive maturation of male and female Mediterranean fruit flies. Physiol Entomol. 2002; 27(1): 29–38.
68. Patton RL. Growth and development parameters for Acheta domesticus. Ann Entomol Soc Am. 1978; 71(1): 40–42.
69. Renacci M, Strambi C. Juvenile hormone levels, vitellogenin and ovarian development in Acheta domesticus. J Exp. 1983; 39: 618–620.
70. Destephano DB, Brady UE, Farr CA. Factors influencing oviposition behaviour in the cricket, Acheta domesticus. Ann Entomol Soc Am. 1982; 75: 111–114.
71. Reiss MJ. The allometry of growth and reproduction. Cambridge University Press. 1991.
72. Forrest TG. Insect size tactics and developmental strategies. Oecologia. 1987; 73(2): 178–184. doi: 10.1007/BF00377505 28312285
73. Honěk A. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos. 1993; 483–492.
74. Berrigan D. The allometry of egg size and number in insects. Oikos. 1991; 313–321.
75. Kasule FK. Associations of fecundity with adult size in the cotton stainer bug Dysdercus fasciatus. Heredity. 1991; 66(2): 281.
76. Peckarsky BL, Cowan CA, Penton MA, Anderson C. Sublethal consequences of stream‐dwelling predatory stoneflies on mayfly growth and fecundity. Ecology. 1993; 74(6): 1836–1846.
77. Xui RD, Ali A. Oviposition, fecundity, and body size of a pestiferous midge, Chironomus crassicaudatus (Diptera: Chironomidae). Environ Entomol. 1994; 23(6): 1480–1484.
78. Chi H, Yang TC. Two-sex life table and predation rate of Propylaea japonica Thunberg (Coleoptera: Coccinellidae) fed on Myzus persicae (Sulzer) (Homoptera: Aphididae). Environ Entomol. 2003; 32(2): 327–333.
79. Haghani M, Fathipour Y, Talebi AA, Baniameri V. Temperature-dependent development of Diglyphus isaea (Hymenoptera: Eulophidae) on Liriomyza sativae (Diptera: Agromyzidae) on cucumber. J Pest Sci. 2007; 80: 71–77.
80. Lachenicht MW, Clusella-Trullas S, Boardman L, Le Roux C, Terblanche JS. Effects of acclimation temperature on thermal tolerance, locomotion performance and respiratory metabolism in Acheta domesticus L. (Orthoptera: Gryllidae). J Insect Physiol. 2010; 56: 822–830. doi: 10.1016/j.jinsphys.2010.02.010 20197070
81. Khaliq A, Javed M, Sohail M, Muhammad S. Environmental effects on insects and their population dynamics. J Entomol Zool Stud. 2014; 2(2): 1–7.
82. Terblanche JS, Chown SL. The effects of temperature, body mass and feeding on metabolic rate in the tsetse fly Glossina morsitans centralis. Physiol Entomol. 2007; 32(2): 175–180.
83. Nijhout HF, Riddiford LM, Mirth C, Shingleton AW, Suzuki Y, Callier V. The developmental control of size in insects. Wiley Interdisciplinary Reviews: Dev Biol. 2014; 3(1): 113–134.
84. Mirth CK, Riddiford LM. Size assessment and growth control: how adult size is determined in insects. BioEssays. 2007; 29: 344–355. doi: 10.1002/bies.20552 17373657
85. Stevens GC. The latitudinal gradient and Geographical range: how so many species coexist in the tropics. Am Nat. 1989; 133: 519–524.
86. Nespolo RF, Lardies MA, Bozinovic F. Intrapopulational variation in the standard metabolic rate of insects: repeatability, thermal tendency and sensitivity (Q10) of oxygen consumption in a cricket. J Exp Biol. 2003; 206: 4309–4315. doi: 10.1242/jeb.00687 14581600
87. Frel A, Gu H, Cardona C, Dorn S. Antixenosis and antibiosis of common beans to Thripspalmi. J Econ Entomol. 2003; 93: 1577–1584.
88. Van Huis A. Insects as food in Sub-Saharan Africa. J. Insect Sci. 2003; 23: 163–185.
89. Ramos-Elorduy J. Insects: a hopeful food source. In: Paoletti M.G. (ed.) Ecological implications of minilivestock: potential of insects, rodents, frogs and snails. Science Publishers, Enfield, MT, USA. 2005: 263–291.
90. Silow CA. Edible and other insects of mid-western Zambia; studies in Ethno-Entomology II. Antikvariat Thomas Andersson, Uppsala, Sweden. 1976: 223.
91. Takeda J. The dietary repertory of the Ngandu people of the tropical rain forest: an ecological and anthropological study of the subsistence activities and food procurement technology of a slash-and burn agriculturist in the Zaire river basin. African Study Monographs Supplementary. 1990; 11: 1–75.
92. Malaisse F. Food supply in African open forests: an ecological and nutritional approach. Se nourrir en foret claire africaine: approche ecologique et nutritionnelle. Les Presses Agronomiques de Gembloux, A.S.B.L., Gembloux, Belgium. 1997. 384.
93. Roulon-Doko P. Chasse, cueillette et cultures chez les Gbaya de Centrafrique. L’Harmattan, Paris, France. 1998.
94. Obopile M, Seeletso TG. Eat or not eat: an analysis of the status of entomophagy in Botswana. Food Secur. 2013; 5: 817–824.
95. Battisi DS, Naylor RL. Historical Warnings of Future Food Insecurity with Unprecented Seasonal Heat, Science. J Sci. 2009; 323: 240–244. http://dx.org/10.1126/science.1164363.
96. Dillon ME, Wang G, Huey RB. Global metabolic impacts of recent climate warming. Nature. 2010; 467(7316): 704–706. doi: 10.1038/nature09407 20930843
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