Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-06-03T04:28:28.328Z Has data issue: false hasContentIssue false
  • English
  • Français

Off-host longevity of the winged dispersal stage of Carnus hemapterus (Insecta: Diptera) modulated by gender, body size and food provisioning

Published online by Cambridge University Press:  08 August 2018

Jesús Veiga Open the ORCID record for Jesús Veiga [Opens in a new window] ,
Eulalia Moreno ,
Jesús Benzal  and
Francisco Valera Open the ORCID record for Francisco Valera [Opens in a new window]
Jesús Veiga
Affiliation:
Departamento de Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas (EEZA-CSIC), Ctra. de Sacramento s/n, La Cañada de San Urbano, Almería E-04120, Spain.
Eulalia Moreno
Affiliation:
Departamento de Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas (EEZA-CSIC), Ctra. de Sacramento s/n, La Cañada de San Urbano, Almería E-04120, Spain.
Jesús Benzal
Affiliation:
Departamento de Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas (EEZA-CSIC), Ctra. de Sacramento s/n, La Cañada de San Urbano, Almería E-04120, Spain.
Francisco Valera*
Affiliation:
Departamento de Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas (EEZA-CSIC), Ctra. de Sacramento s/n, La Cañada de San Urbano, Almería E-04120, Spain.
*
Author for correspondence: Francisco Valera, E-mail: pvalera@eeza.csic.es
Get access Rights & Permissions [Opens in a new window]

Abstract

Highlighting the dispersal ecology of parasites is important for understanding epidemiological, demographic and coevolutionary aspects of host–parasite interactions. Yet, critical aspects of the dispersal stage of parasites, such as longevity and the factors influencing it, are poorly known. Here we study the lifespan of the dispersal stage of an ectoparasitic dipteran, Carnus hemapterus, and the impact of gender, body size and food provisioning on longevity. We found that freshly emerged imagoes survive at most less than 4 days. Longevity increased with body size and, since this parasite exhibits sexual size dimorphism, the bigger females lived longer than males. However, controlling for body size suggests that males lived relatively longer than females. Furthermore, a humid environment and food provisioning (flowers) significantly increased individual life spans. We discuss the relative importance of spatial and temporal dispersal in relation to the infectious potential of this parasite.

Keywords

Body sizeCarnus hemapterusfood sourceslongevitysexual size dimorphismFlower provisioning increased life span, suggesting that this haematophagous fly can refuel during dispersal.
Type
Research Article
Information
Parasitology , Volume 146 , Issue 2 , February 2019 , pp. 241 - 245
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Blanckenhorn, WU, Preziosi, RF and Fairbairn, DJ (1995) Time and energy constraints and the evolution of sexual size dimorphism – to eat or to mate? Evolutionary Ecology 9, 369–381.Google Scholar
Bohonak, AJ and Jenkins, DG (2003) Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecology Letters 6, 783–796.Google Scholar
Botzler, RG and Brown, RN (2014) Foundations of Wildlife Diseases. Oakland, California, USA: University of California Press.Google Scholar
Brake, I (2011) World catalog of the family Carnidae (Diptera, Schizophora). Myia 12, 113–169.Google Scholar
Briegel, H and Horler, E (1993) Multiple blood meals as reproductive strategy in Anopheles (Diptera, Culicidae). Journal of Medical Entomology 30, 975–985.Google Scholar
Brown, CR and Brown, MB (1996) Coloniality in the Cliff Swallow: The Effect of Group Size on Social Behaviour. Chicago, Illinois, USA: University of Chicago Press.Google Scholar
Brown, CR and Brown, MB (2004) Group size and ectoparasitism affect daily survival probability in a colonial bird. Behavioral Ecology and Sociobiology 56, 498–511.Google Scholar
Bujan, J, Yanoviak, SP and Kaspari, M (2016) Dessication resistance in tropical insects: causes and mechanisms underlying variability in a Panama ant community. Ecology and Evolution 6, 6282–6291.Google Scholar
Calero-Torralbo, MA (2011) Factores ecológicos y mecanismos implicados en la variabilidad de la interacción entre un ectoparásito generalista (Carnus hemapterus) y sus hospedadores (PhD thesis) Universidad de Granada, Granada, Spain.Google Scholar
Calero-Torralbo, MA, Václav, R and Valera, F (2013) Intra-specific variability in life-cycles synchronization between an ectoparasitic fly and its avian host. Oikos 122, 274–284.Google Scholar
Carroll, AL and Quiring, DT (1993) Interactions between size and temperature influence fecundity and longevity of a tortricid moth, Zeiraphera canadensis. Oecologia 93, 233–241.Google Scholar
Chen, L, Onagbola, EO and Fadamiro, HY (2005) Effects of temperature, sugar availability, gender, mating, and size on the longevity of phorid fly Pseudacteon tricuspis (Diptera: Phoridae). Environmental Entomology 34, 246–255.Google Scholar
Clayton, DH, Lee, PLM, Tompkins, DM and Brodie, ED III (1999) Reciprocal natural selection on host-parasite phenotypes. The American Naturalist 154, 261–270.Google Scholar
Clements, AN (1955) The sources of energy for flight in mosquitoes. Journal of Experimental Biology 32, 547–554.Google Scholar
Compton, SG (2002) Sailing with the wind: dispersal by small flying insects. In Bullock, D (ed.) Dispersal Ecology. Oxford, UK: British Ecological Society, Blackwells, pp. 113–133.Google Scholar
Cônsoli, FL and Parra, JRP (1995) Effects of constant and alternating temperatures on Trichogramma galloi Zucchi (Hym., Trichogrammatidae) biology. II. Parasitism capacity and longevity. Journal of Applied Entomology 119, 667–670.Google Scholar
Darwin, C (1871) The Descent of Man, and Selection in Relation to Sex. London: John Murray.Google Scholar
Dell Inc (2016) Dell Statistica (data analysis software system), version 13. Software.dell.com.Google Scholar
Dudley, R (2000) The Biomechanics of Insect Flight. Princeton, New Jersey, USA: Princeton University Press.Google Scholar
Fairbairn, DJ (1997) Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics 28, 659–687.Google Scholar
Foster, WA (1995) Mosquito sugar feeding and reproductive energetics. Annual Review of Entomology 40, 443–474.Google Scholar
Fox, CW, Dublin, L and Pollitt, SJ (2003) Gender differences in lifespan and mortality rates in two seed beetle species. Functional Ecology 17, 619–626.Google Scholar
Grimaldi, D (1997) The bird flies, Genus Carnus: species revision, generic relationships and a fossil Meoneura in amber (Diptera: Carnidae). American Museum Novitates. N° 3190, pp. 30. American Museum of Natural History, New York.Google Scholar
Guiguen, C, Launay, H and Beaucournu, JC (1983) Ectoparasites des oiseaux en Bretagne. I. Répartition et écologie d'un diptère hematophage nouveau pour la France: Carnus hemapterus Nitzsch. Revue Française d'Entomologie 5, 54–62.Google Scholar
Haas, W (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106, 349–364.Google Scholar
Hairston, NG (2000) Temporal dispersal: ecological and evolutionary implications of prolonged egg diapause. American Zoologist 40, 1039–1040.Google Scholar
Hairston, NG and Kearns, CM (2002) Temporal dispersal: ecological and evolutionary aspects of zooplankton egg banks and the role of sediment mixing. Integrative and Comparative Biology 42, 481–491.Google Scholar
Hanski, I (1988) Four kinds of extra long diapause in insects: a review of theory and observations. Annales Zoologici Fennici 25, 37–53.Google Scholar
Harper, GH, Marchant, A and Boddington, DG (1992) The ecology of the hen flea Ceratophyllus gallinae and the moorhen flea Dasypsyllus gallinulae in nest boxes. Journal of Animal Ecology 61, 317–327.Google Scholar
Hassell, MP (2000) The Spatial and Temporal Dynamics of Host-Parasitoid Interactions. Oxford, UK: Oxford University Press.Google Scholar
Hasson, E, Fanara, JJ, Rodriguez, C, Vilardi, JC, Reig, OA and Fontdevila, A (1993) The evolutionary history of Drosophila buzzatii. XXVII. Thorax length is positively correlated with longevity in a natural population from Argentina. Genetics 92, 61–65.Google Scholar
Hoi, H, Kristofík, J, Darolová, A and Hoi, C (2010) Are parasite intensity and related costs of the milichiid fly Carnus hemapterus related to host sociality? Journal of Ornithology 151, 907–913.Google Scholar
Johnson, CG (1969) Migration and Dispersal of Insects by Flight. London, UK: Methuen.Google Scholar
Kirkpatrick, CE and Colvin, BA (1989) Ectoparasitic fly Carnus hemapterus (Diptera: Carnidae) in a nesting population of common barn-owls (Strigiformes: Tytonidae). Journal of Medical Entomology 26, 109–112.Google Scholar
Kjellberg, F, Doumesche, B and Bronstein, JL (1988) Longevity of a fig wasp (Blastophaga psenes). Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen C91, 117–122.Google Scholar
Kleindorfer, S and Dudaniec, RY (2009) Love thy neighbour? Social nesting pattern, host mass and nest size affect ectoparasite intensity in Darwin's tree finches. Behavioral Ecology and Sociobiology 63, 731–739.Google Scholar
Lessard, E and Boivin, G (2013) Effect of low temperature on emergence, fecundity, longevity and host-feeding by Trichogramma brassicae. BioControl 58, 319–329.Google Scholar
Lessells, CM and Boag, PT (1987) Unrepeatable repeatabilities: a common mistake. The Auk 104, 116–121.Google Scholar
Liker, A, Markus, M, Vozár, A, Zemankovics, E and Rózsa, L (2001) Distribution of Carnus hemapterus in a starling colony. Canadian Journal of Zoology 79, 574–580.Google Scholar
Manda, H, Gouagna, LC, Foster, WA, Jackson, RR, Beier, JC, Githure, JI and Hassanali, A (2007) Effect of discriminative plant-sugar feeding on the survival and fecundity of Anopheles gambiae. Malaria Journal 6, 113.Google Scholar
McCoy, KD, Boulinier, T, Tirard, C and Michalakis, Y (2003) Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution 57, 288–296.Google Scholar
Mellanby, K (1932) The influence of atmospheric humidity on the thermal death point of a number of insects. Journal of Experimental Biology 9, 222–231.Google Scholar
Nilssen, AC (1997) Factors affecting size, longevity and fecundity in the reindeer oestrid flies Hypoderma tarandi (L.) and Cephenemyia trompe (Modeer). Ecological Entomology 22, 294–304.Google Scholar
Papp, L (1998) Family carnidae. In Papp, L and Darvas, B (eds), Manual of Palaearctic Diptera. Budapest: Science Herald, vol. 3, pp. 211–217.Google Scholar
Roff, D (1993) The Evolution of Life Histories. Theory and Analysis. New York, USA: Springer.Google Scholar
Roulin, A (1998) Cycle de reproduction et abondance du diptère parasite Carnus hemapterus dans les nicheés de chouettes effraies Tyto alba. Alauda 66, 265–272.Google Scholar
Roulin, A (1999) Fécondité de la mouche Carnus hemapterus, ectoparasite des jeunes chouettes effraies Tyto alba. Alauda 67, 205–212.Google Scholar
Sivinski, JM (1993) Longevity and fecundity in the Caribbean fruit fly (Diptera: Tephritidae): effects of mating, strain and body size. Florida Entomologist 76, 635–644.Google Scholar
Soltész, Z, Seres, N and Kovács-Hostyánszki, A (2018) Dipteran assemblages in Red-footed Falcon (Falco vespertinus) nest boxes. Acta Zoologica Academiae Scientiarum Hungaricae 64, 91–102.Google Scholar
Taylor, F (1981) Ecology and evolution of physiological time in insects. American Naturalist 117, 1–23.Google Scholar
Tochen, S, Woltz, JM, Dalton, DT, Lee, JC, Wiman, NG and Walton, VM (2015) Humidity affects population of Drosophyla suzukii (Diptera: Drosophylae) in blueberry. Journal of Applied Entomology 140, 47–57.Google Scholar
Tochen, S, Walton, VM and Lee, JC (2016) Impact of floral feeding on adult Drosophila suzukii survival and nutrient status. Journal of Pest Science 89, 793–802.Google Scholar
Václav, R, Calero-Torralbo, MA and Valera, F (2008) Ectoparasite load is linked to ontogeny and cell-mediated immunity in an avian host system with pronounced hatching asynchrony. Biological Journal of the Linnean Society 94, 463–473.Google Scholar
Valera, F and Zídková, L (2012) Reproductive anatomy and fecundity estimation of the haematophagous ectoparasite Carnus hemapterus. Parasitology Research 110, 1733–1739.Google Scholar
Valera, F, Casas-Crivillé, A and Hoi, H (2003) Interspecific parasite exchange in a mixed colony of birds. Journal of Parasitology 89, 245–250.Google Scholar
Valera, F, Casas-Crivillé, A and Calero-Torralbo, MA (2006) Prolonged diapause in the ectoparasite Carnus hemapterus: how frequent is it in parasites? Parasitology 133, 179–188.Google Scholar
Ward, SA, Leather, SR, Pickup, J and Harrington, R (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology 67, 763–773.Google Scholar
Winkler, K, Wäckers, F, Bukovinszkine-Kissa, G and van Lenteren, J (2006) Sugar resources are vital for Diadegma semiclausum fecundity under field conditions. Basic and Applied Ecology 7, 133–140.Google Scholar
Wright, GA and Schiestl, FP (2009) The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Functional Ecology 23, 841–851.Google Scholar
Yu, BT, Ding, YM, Mo, XC, Liu, N, Li, HJ and Mo, JC (2016) Survivorship and fecundity of Culex pipiens pallens feeding on flowering plants and seed pods with differential preferences. Acta Tropica 155, 51–57.Google Scholar