Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-23T07:56:56.905Z Has data issue: false hasContentIssue false

Fitness responses to co-infestation in fleas exploiting rodent hosts

Published online by Cambridge University Press:  18 August 2015

IRINA S. KHOKHLOVA
Affiliation:
Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 8499000 Midreshet Ben-Gurion, Israel
ELIZABETH M. DLUGOSZ
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 8499000 Midreshet Ben-Gurion, Israel
BORIS R. KRASNOV*
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 8499000 Midreshet Ben-Gurion, Israel
*
* Corresponding author. Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel. E-mail: [email protected]

Summary

To understand mechanisms behind positive interspecific co-occurrences in flea infracommunities, we asked whether co-infestation results in an increase of flea fitness (quantity and/or quality of the offspring). We studied reproductive performance of Xenopsylla ramesis and Parapulex chephrenis when they exploited their characteristic host (Meriones crassus and Acomys cahirinus, respectively) either alone or together with another species. We used egg production, the number of new imagoes, pre-imaginal survival and egg size as fitness-related variables and predicted that fitness will be higher in fleas feeding in mixed- than in single-species groups. In both fleas, mean number of eggs produced per female flea did not depend on experimental treatment. No effect of single- vs mixed-species infestation on the mean number of new imagoes per female and the number of emerged imagoes per egg was found for X. ramesis, whereas both these numbers were higher in mixed- than in single-species groups for P. chephrenis. X. ramesis produced eggs of similar size independently of treatment, whereas eggs produced by P. chephrenis in mixed-species groups were significantly larger than eggs produced in single-species groups. We conclude that an increase in reproductive performance as a response to co-infestation may be one of the mechanisms behind aggregative structure of flea infracommunities. However, this response may vary among flea species.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

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

REFERENCES

Berrigan, D. (1991). The allometry of egg size and number in insects. Oikos 60, 313321.Google Scholar
Brinkerhoff, R. J., Markeson, A. B., Knouft, J. A., Gage, K. L. and Montenieri, J. A. (2006). Abundance patterns of two Oropsylla (Ceratophyllidae: Siphonaptera) species on black-tailed prairie dog (Cynomys ludovicianus) hosts. Journal of Vector Ecology 31, 355363.Google Scholar
Bush, A. O. and Holmes, J. C. (1986). Intestinal helminths of lesser scaup ducks: patterns of association. Canadian Journal of Zoology 64, 132141.Google Scholar
Combes, C. (2001). Parasitism. The Ecology and Evolution of Intimate Interactions, University of Chicago Press, Chicago, USA.Google Scholar
Cox, F. E. G. (2001). Concomitant infections, parasites and immune responses. Parasitology 122, S23S38.Google Scholar
Demas, G. E. and Nelson, R. J. (1998). Photoperiod, ambient temperature, and food availability interact to affect reproductive and immune function in adult male deer mice (Peromyscus maniculatus). Journal of Biological Rhythms 13, 253262.Google Scholar
Faulkenberry, G. D. and Robbins, R. G. (1980). Statistical measures of interspecific association between the fleas of the gray-tailed vole, Microtus canicaudus Miller. Entomological News 91, 93101.Google Scholar
Fielden, L. J., Rechav, Y. and Bryson, N. R. (1992). Acquired immunity to larvae of Amblyomma marmoreum and A. hebraeum by tortoises, guinea-pigs and guinea-fowl. Medical and Veterinary Entomology 6, 251254.Google Scholar
Heylen, D. J. A. and Matthysen, E. (2008). Effect of tick parasitism on the health status of a passerine bird. Functional Ecology 22, 10991107.Google Scholar
Johnston, N. A., Trammell, R. A., Ball-Kell, S., Verhulst, S. and Toth, L. A. (2009). Assessment of immune activation in mice before and after eradication of mite infestation. Journal of the American Association for Laboratory Animal Science 48, 371377.Google Scholar
Jokela, J., Schmid-Hempel, P. and Rigby, M. C. (2000). Dr. Pangloss restrained by the Red Queen–steps towards a unified defence theory. Oikos 89, 267274.Google Scholar
Khokhlova, I. S., Spinu, M., Krasnov, B. R. and Degen, A. A. (2004). Immune response to fleas in a wild desert rodent: effect of parasite species, parasite burden, sex of host and host parasitological experience. Journal of Experimental Biology 207, 27252733.Google Scholar
Khokhlova, I. S., Ghazaryan, L., Krasnov, B. R. and Degen, A. A. (2008). Effects of parasite specificity and previous infestation of hosts on the feeding and reproductive success of rodent-infesting fleas. Functional Ecology 22, 530536.Google Scholar
Khokhlova, I. S., Fielden, L. J., Degen, A. A. and Krasnov, B. R. (2012). Ectoparasite fitness in auxiliary hosts: phylogenetic distance from a principal host matters. Journal of Evolutionary Biology 25, 20052013.Google Scholar
Khokhlova, I. S., Fielden, L. J., Williams, J. B., Degen, A. A. and Krasnov, B. R. (2013). Energy expenditure for egg production in arthropod ectoparasites: the effect of host species. Parasitology 140, 10701077.Google Scholar
Khokhlova, I. S., Pilosof, S., Fielden, L. J., Degen, A. A. and Krasnov, B. R. (2014). A trade-off between quantity and quality of offspring in haematophagous ectoparasites: the effect of the level of specialization. Journal of Animal Ecology 83, 397405.Google Scholar
Krasnov, B. R. (2008). Functional and Evolutionary Ecology of Fleas. A Model for Ecological Parasitology, Cambridge University Press, Cambridge, UK. Google Scholar
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S., Degen, A. A. and Rogovin, K. V. (1996). On the biology of Sundevall's jird (Meriones crassus Sundevall) in Negev Highlands, Israel. Mammalia 60, 375391.Google Scholar
Krasnov, B. R., Shenbrot, G. I., Medvedev, S. G., Vatschenok, V. S. and Khokhlova, I. S. (1997). Host-habitat relation as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitology 114, 159173.Google Scholar
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2001). The effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). Journal of Medical Entomology 38, 629637.Google Scholar
Krasnov, B. R., Khokhlova, I. S., Oguzoglu, I. and Burdelova, N. V. (2002). Host discrimination by two desert fleas using an odour cue. Animal Behaviour 64, 3340.Google Scholar
Krasnov, B. R., Sarfati, M., Arakelyan, M. S., Khokhlova, I. S., Burdelova, N. V. and Degen, A. A. (2003). Host-specificity and foraging efficiency in blood-sucking parasite: feeding patterns of a flea Parapulex chephrenis on two species of desert rodents. Parasitology Research 90, 393399.Google Scholar
Krasnov, B. R., Mouillot, D., Shenbrot, G. I., Khokhlova, I. S. and Poulin, R. (2005 a). Abundance patterns and coexistence processes in communities of fleas parasitic on small mammals. Ecography 28, 453464.Google Scholar
Krasnov, B. R., Burdelova, N. V., Khokhlova, I. S., Shenbrot, G. I. and Degen, A. A. (2005 b). Pre-imaginal interspecific competition in two flea species parasitic on the same rodent host. Ecological Entomology 30, 146155.Google Scholar
Krasnov, B. R., Stanko, M. and Morand, S. (2006 a). Are ectoparasite communities structured? Species co-occurrence, temporal variation and null models. Journal of Animal Ecology 75, 13301339.Google Scholar
Krasnov, B. R., Stanko, M., Khokhlova, I. S., Mosansky, L., Shenbrot, G. I., Hawlena, H. and Morand, S. (2006 b). Aggregation and species coexistence in fleas parasitic on small mammals. Ecography 29, 159168.Google Scholar
Krasnov, B. R., Korine, C., Burdelova, N. V., Khokhlova, I. S. and Pinshow, B. (2007). Between-host phylogenetic distance and feeding efficiency in haematophagous ectoparasites: rodent fleas and a bat host. Parasitology Research 101, 365371.Google Scholar
Krasnov, B. R., Matthee, S., Lareschi, M., Korallo-Vinarskaya, N. P. and Vinarski, M. V. (2010). Co-occurrence of ectoparasites on rodent hosts; null model analyses of data from three continents. Oikos 119, 120128.Google Scholar
Krasnov, B. R., Shenbrot, G. I. and Khokhlova, I. S. (2011). Aggregative structure is the rule in communities of fleas: null model analysis. Ecography 34, 751761.Google Scholar
Levine, J. M. (1999). Indirect facilitation: evidence and predictions from a riparian community. Ecology 80, 17621769.CrossRefGoogle Scholar
Lindsay, L. R. and Galloway, T. D. (1998). Reproductive status of four species of fleas (Insecta: Siphonaptera) on Richardson's ground squirrel (Rodentia: Sciuridae) in Manitoba, Canada. Journal of Medical Entomology 35, 423430.Google Scholar
Lochmiller, R. L. and Deeremberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 8798.Google Scholar
Pilosof, S., Lareschi, M. and Krasnov, B. R. (2012). Host body microcosm and ectoparasite infracommunities: arthropod ectoparasites are not spatially segregated. Parasitology 139, 17391748.Google Scholar
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. and R Core Team (2014). nlme: linear and nonlinear mixed effects models. R Package Version 3.1-118, http://CRAN.R-project.org/package=nlme Google Scholar
Pöykkö, H. and Mänttäri, S. (2012). Egg size and composition in an ageing capital breeder–consequences for offspring performance. Ecological Entomology 37, 330341.Google Scholar
Presley, S. J. (2007). Streblid bat fly assemblage structure on Paraguayan Noctilio leporinus (Chiroptera : Noctilionidae): nestedness and species co-occurrence. Journal of Tropical Ecology 23, 409417.Google Scholar
Presley, S. J. (2011). Interspecific aggregation of ectoparasites on bats: importance of hosts as habitats supersedes interspecific interactions. Oikos 120, 832841.Google Scholar
R Core Team (2013). R: a Language and Environment for Statistical Computing , R Foundation for Statistical Computing, Vienna, Austria, URL http://www.R-project.org/ Google Scholar
Ranzani-Paiva, M. J. T. and Silva-Souza, A. T. (2004). Co-infestation of gills by different parasite groups in the mullet, Mugil platanus Günther, 1880 (Osteichthyes, Mugilidae): effects on relative condition factor. Brazilian Journal of Biology 64, 677682.Google Scholar
Risco, D., Serrano, E., Fernández-Llario, P., Cuesta, J. M., Gonçalves, P., García-Jiménez, W. L., Martínez, R., Cerrato, R., Velarde, R., Gómez, L., Segalés, J. and Hermoso de Mendoza, J. (2014). Severity of bovine tuberculosis is associated with co-infection with common pathogens in wild boar. PLoS ONE 9, e110123.Google Scholar
Sánchez, S., Serrano, E., Gómez, M. S., Feliu, C. and Morand, S. (2014). Positive co-occurrence of flea infestation at a low biological cost in two rodent hosts in the Canary archipelago. Parasitology 141, 511521.Google Scholar
Sarfati, M., Krasnov, B. R., Ghazaryan, L., Khokhlova, I. S., Fielden, L. J. and Degen, A. A. (2005). Energy costs of blood digestion in a host-specific haematophagous parasite. Journal of Experimental Biology 208, 24892496.Google Scholar
Serrano, E. and Millán, J. (2014). What is the price of neglecting parasite groups when assessing the cost of co-infection? Epidemiology and Infection 142, 15331540.Google Scholar
Smith, C. C. and Fretwell, S. D. (1974). Optimal balance between size and number of offspring. American Naturalist 108, 499506.Google Scholar
Taylor, L. H., Mackinnon, M. J. and Read, A. F. (1998). Virulence of mixed-clone and single-clone infections of the rodent malaria Plasmodium chabaudi . Evolution 52, 583591.Google Scholar
Tello, J. S., Stevens, R. D. and Dick, C. W. (2008). Patterns of species co-occurrence and density compensation: a test for interspecific competition in bat ectoparasite infracommunities. Oikos 117, 693702.Google Scholar
Torres-Vila, L. M. and Rodríguez-Molina, M. C. (2002). Egg size variation and its relationship with larval performance in the Lepidoptera: the case of the European grapevine moth Lobesia botrana . Oikos 99, 272283.Google Scholar
Vazquez, D. P., Poulin, R., Krasnov, B. R. and Shenbrot, G. I. (2005). Species abundance patterns and the distribution of specialization in host-parasite interaction networks. Journal of Animal Ecology 74, 946955.Google Scholar
Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. and Smith, G. M. (2009). Mixed Effects Models and Extensions in Ecology with R, Springer, New York, USA.Google Scholar