Skip to main content
Log in

Intraspecific variation of body size in fleas: effects of host sex and flea phenology

  • Arthropods and Medical Entomology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

We investigated the effects of host sex and flea phenology (estimated as periods of high versus low abundance) on individual body size in four fleas of small mammals. Amalaraeus penicilliger and Ctenophthalmus uncinatus are ectoparasites of the bank vole Myodes glareolus, whereas Doratopsylla dasycnema and Palaeopsylla soricis are ectoparasites of the common shrew Sorex araneus. We found significant effects of host sex and phenology on the body size of all flea species, although there was no general trend in the directions of these effects. Larger A. penicilliger were found on female hosts, whereas larger P. soricis were found on male hosts. In the remaining species, larger fleas were collected from male hosts during periods of high abundance (male C. uncinatus and female D. dasycnema) and from female hosts during periods of low abundance (male C. uncinatus). Regarding phenology, larger fleas were recorded during periods of either high (A. penicilliger, C. uncinatus, D. dasycnema) or low (C. uncinatus, P. soricis) abundance, but this depended on flea and/or host sex. We conclude that the directions of the host sex and phenology effects varied between flea species. Furthermore, the direction of the host sex effect was mediated by the effect of phenology and vice versa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agosta SJ (2010) Male body size and mating success and their relation to larval host plant history in the moth Rothschildia lebeau in Costa Rican dry forest. Biotropica 42:201–207

    Article  Google Scholar 

  • Angilletta M, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509

    Article  PubMed  Google Scholar 

  • Aragón P, Fitze PS (2014) Geographical and temporal body size variation in a reptile: roles of sex, ecology, phylogeny and ecology structured in phylogeny. PLoS One 9:e104026

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Balashov YS, Bochkov AV, Vashchonok VS, Grigor'eva LA, Tret’yakov KV (2002) Structure and seasonal dynamics of the community ectoparasites in the bank vole in the Ilmen-Volkhov lowland. Parazitologyia 36:433–446 (in Russian)

    Google Scholar 

  • Berger D, Walters R, Gotthard K (2008) What limits insect fecundity? Body size- and temperature-dependent egg maturation and oviposition in a butterfly. Funct Ecol 22:523–529

  • Berger D, Olofsson M, Friberg M, Karlsson B, Wiklund C, Gotthard K (2012) Intraspecific variation in body size and the rate of reproduction in female insects – adaptive allometry or biophysical constraint? J Anim Ecol 81:1244–1258

    Article  PubMed  Google Scholar 

  • Blanckenhorn WU (1997) Altitudinal life history variation in the dung flies Scathophaga stercoraria and Sepsis cynipsea. Oecologia 109:342–352

    Article  CAS  PubMed  Google Scholar 

  • Bolnick DI, Amarasekare P, Araújo MS, Bürger R, Levine JM, Novak M, Rudolf VHW, Schreiber SJ, Urban MC, Vasseur D (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192

    Article  PubMed  PubMed Central  Google Scholar 

  • Brinck-Lindroth G, Smit FGAM (2007) The fleas (Siphonaptera) of Fennoscandia and Denmark. Koninklijke Brill, Leiden

    Book  Google Scholar 

  • Bronson FH (1989) Mammalian reproductive biology. University of Chicago Press, Chicago

    Google Scholar 

  • Brown JH (1995) Macroecology. University of Chicago Press, Chicago

    Google Scholar 

  • Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

    Article  Google Scholar 

  • Gillespie MA, Birkemoe T, Sverdrup-Thygeson A (2017) Interactions between body size, abundance, seasonality, and phenology in forest beetles. Ecol Evol 7:1091–1100

    Article  PubMed  PubMed Central  Google Scholar 

  • Gribbin SD, Thompson DJ (1990) Asymmetric intraspecific competition among larvae of the damselfly Ischnura elegans (Zygoptera: Coenagrionidae). Ecol Entomol 15:37–42

    Article  Google Scholar 

  • Griffiths JI, Petchey OL, Pennekamp F, Childs DZ (2018) Linking intraspecific trait variation to community abundance dynamics improves ecological predictability by revealing a growth-defence trade-off. Funct Ecol 32:496–508

    Article  Google Scholar 

  • Gromov VS (2009) Parental care in captive red-backed vole (Clethrionomys rutilus). Contemp Probl Ecol 2:1–6

    Article  Google Scholar 

  • Honěk A (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483–492

    Article  Google Scholar 

  • Horne CR, Hirst AG, Atkinson D (2017) Insect temperature–body size trends common to laboratory, latitudinal and seasonal gradients are not found across altitudes. Funct Ecol 32:948–957

    Article  Google Scholar 

  • Hsu M-H, Wu W-J (2001) Off-host observations of mating and postmating behaviors in the cat flea (Siphonaptera: Pulicidae). J Med Entomol 38:352–360

    Article  CAS  PubMed  Google Scholar 

  • Khokhlova IS, Serobyan V, Degen AA, Krasnov BR (2010a) Host gender and offspring quality in a flea parasitic on a rodent. J Exp Biol 213:3299–3304

    Article  PubMed  Google Scholar 

  • Khokhlova IS, Hovhanyan A, Degen AA, Krasnov BR (2010b) The effect of larval density on pre-imaginal development in two species of desert fleas. Parasitology 137:1925–1935

    Article  CAS  PubMed  Google Scholar 

  • Khokhlova IS, Serobyan V, Degen AA, Krasnov BR (2011) Discrimination of host sex by a haematophagous ectoparasite. Anim Behav 81:275–281

    Article  Google Scholar 

  • Khokhlova IS, Pilosof S, Fielden LJ, Degen AA, Krasnov BR (2014) A trade-off between quantity and quality of offspring in haematophagous ectoparasites: the effect of the level of specialization. J Anim Ecol 83:397–405

    Article  PubMed  Google Scholar 

  • Kiefer D, Warburton EM, Khokhlova IS, Krasnov BR (2016) Reproductive consequences of female size in haematophagous ectoparasites. J Exp Biol 219:2368–2376

    Article  PubMed  Google Scholar 

  • Kortet R, Taskinen J, Sinisalo T, Jokinen I (2003) Breeding-related seasonal changes in immunocompetence, health state and condition of the cyprinid fish, Rutilus rutilus L. Biol J Linn Soc 78:117–127

    Article  Google Scholar 

  • Krasnov BR (2008) Functional and evolutionary ecology of fleas: a model for ecological parasitology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV (2001) The effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). J Med Entomol 38:629–637

    Article  CAS  PubMed  Google Scholar 

  • Krasnov BR, Burdelova NV, Shenbrot GI, Khokhlova IS (2002) Annual cycles of four flea species (Siphonaptera) in the Central Negev desert. Med Vet Entomol 16:266–276

    Article  CAS  PubMed  Google Scholar 

  • Krasnov BR, Burdelov SA, Khokhlova IS, Burdelova NV (2003) Sexual size dimorphism, morphological traits and jump performance in seven species of desert fleas (Siphonaptera). J Zool (Lond) 261:181–189

    Article  Google Scholar 

  • Krasnov BR, Morand S, Hawlena H, Khokhlova IS, Shenbrot GI (2005) Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146:209–217

    Article  PubMed  Google Scholar 

  • Krasnov BR, Bordes F, Khokhlova IS, Morand S (2012) Gender-biased parasitism in small mammals: patterns, mechanisms, consequences. Mammalia 76:1–13

    Article  Google Scholar 

  • Lack D (1947) The significance of clutch-size. Ibis 89:302–352

    Article  Google Scholar 

  • Lang JD (1996) Factors affecting the seasonal abundance of ground squirrel and wood rat fleas (Siphonaptera) in San Diego County, California. J Med Entomol 33:790–804

    Article  CAS  PubMed  Google Scholar 

  • Laska A, Rector BG, Kuczyński L, Scoracka A (2017) Is body size important? Seasonal changes in morphology in two grass-feeding Abacarus mites. Exp Appl Acarol 72:317–328

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee SE, Johnstone IP, Lee RP, Opdebeeck JP (1999) Putative salivary allergens of the cat flea, Ctenocephalides felis. Vet Immunol Immunopathol 69:229–237

    Article  CAS  PubMed  Google Scholar 

  • Lenth R (2020) emmeans: estimated marginal means, aka least-squares means. R package version 1.4.8. https://CRAN.R-project.org/package=emmeans. Accessed 9 March 2020

  • Liberman V, Khokhlova IS, Degen AA, Krasnov BR (2013) Reproductive consequences of host age in a desert flea. Parasitology 140:461–470

    Article  PubMed  Google Scholar 

  • Miller RA, Harper JM, Galecki A, Burke DT (2002) Big mice die young: early life growth predicts longevity in genetically heterogeneous mice. Aging Cell 1:22–29

    Article  CAS  PubMed  Google Scholar 

  • Najafpour P, Rasekh A, Esfandiari M (2018) Maternal rearing condition and age affect progeny fitness in the parasitoid wasp Lysiphlebus fabarum. Entomol Exp Appl 166:24–31

    Article  Google Scholar 

  • Nijhout HF (2003) The control of body size in insects. Dev Biol 261:1–9

    Article  CAS  PubMed  Google Scholar 

  • Peat J, Darvill B, Ellis J, Goulson D (2005) Effects of climate on intra- and inter-specific size variation in bumblebees. Funct Ecol 19:145–151

    Article  Google Scholar 

  • Pelletier F, Page KA, Ostiguy T, Festa-Bianchet M (2005) Fecal counts of lungworm larvae and reproductive effort in bighorn sheep, Ovis canadensis. Oikos 110:473–480

    Article  Google Scholar 

  • Peters RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2019) nlme: linear and nonlinear mixed effects models. R package version 3.1–142, https://CRAN.R-project.org/package=nlme. Accessed 9 March 2020

  • R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria URL https://www.R-project.org. Accessed 9 March 2020

  • Rodrigues D, Moreira GRP (2004) Seasonal variation in larval host plants and consequences for Heliconius erato (Lepidoptera: Nymphalidae) adult body size. Austral Ecol 29:437–445

    Article  Google Scholar 

  • Rolff J (2002) Bateman’s principle and immunity. Proc R Soc Lond B 269:867–872

    Article  Google Scholar 

  • Rothschild M, Schlein J, Parker K, Neville C, Sternberg S (1975) The jumping mechanism of Xenospylla cheopis. III. Execution of the jump and activity. Phil Trans R Soc Lond B 271:499–515

    Article  CAS  Google Scholar 

  • Schneider W, Takken W, MacCall PJ (2000) Interspecific competition between sibling species larvae of An. arabiensis and An. gambiae. Med Vet Entomol 14:165–170

    Article  CAS  PubMed  Google Scholar 

  • Silverman J, Rust MK, Reierson DA (1981) Influence of temperature and humidity on survival and development of the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). J Med Entomol 18:78–83

    Article  CAS  PubMed  Google Scholar 

  • Surkova EN, Korallo-Vinarskaya NP, Vinarski MV, Stanko M, Warburton EM, van der Mescht L, Khokhlova IS, Krasnov BR (2018) Sexual size dimorphism and sex ratio in arthropod ectoparasites: contrasting patterns at different hierarchical scales. Int J Parasitol 48:969–978

    Article  PubMed  Google Scholar 

  • Vashchonok VS (2006) Species composition, host association and niche differentiation in fleas of small mammals in the Ilmen-Volkhov lowland. Parazitologyia 40:425–437 (in Russian)

    Google Scholar 

  • Vashchonok VS, Tret’yakov KA (2003) The seasonal dynamics of flea (Siphonaptera) numbers on bank voles (Clethrionomys glareolus) in the north part of Novgorod region. Parazitologyia 37:177–190 (in Russian)

    Google Scholar 

  • Vashchonok VS, Tret’yakov KA (2004) Seasonal dynamics of a flea number (Siphonaptera) on the common shrew (Sorex araneus) in the north part of the Novgorod oblast. Parazitologyia 38:503–514 (in Russian)

    Google Scholar 

  • Vashchonok VS, Tret’yakov KA (2005) The seasonal dynamics of fleas (Siphonaptera) abundance on Apodemus uralensis in the northern part of Novgorod region. Parazitologyia 39:270–277 (in Russian)

    Google Scholar 

  • Xu M (2016) Ecological scaling laws link individual body size variation to population abundance fluctuation. Oikos 125:288–299

    Article  Google Scholar 

  • Zirbel KE, Alto BW (2018) Maternal and paternal nutrition in a mosquito influences offspring life histories but not infection with an arbovirus. Ecosphere 9:e02469

    Article  Google Scholar 

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1024

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This is publication no. 1085 of the Mitrani Department of Desert Ecology.

Funding

This study was supported by the Russian Foundation for Basic Research (grant no. 19-04-00759 to SGM) and the Ministry of Science and Higher Education of the Russian Federation (project no. АААА-А19-119020790133-6 to SGM).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Boris R. Krasnov.

Ethics declarations

This article relies on previously collected data deposited at the Zoological Institute of the Russian Academy of Sciences (Saint Petersburg, Russia) and does not contain experiments with human participants or animals. For this type of study, formal consent is not required.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Julia Walochnik

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 72 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Medvedev, S.G., Sedikhin, N.V. & Krasnov, B.R. Intraspecific variation of body size in fleas: effects of host sex and flea phenology. Parasitol Res 119, 3211–3220 (2020). https://doi.org/10.1007/s00436-020-06867-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-020-06867-1

Keywords

Navigation