Oecologia (2003) 134:365–372 DOI 10.1007/s00442-002-1122-2
POPULATION ECOLOGY
Boris R. Krasnov · Irina S. Khokhlova · Georgy I. Shenbrot
Density-dependent host selection in ectoparasites: An application of isodar theory to fleas parasitizing rodents Received: 9 July 2002 / Accepted: 27 October 2002 / Published online: 19 December 2002 Springer-Verlag 2002
Abstract Parasites should make the same decisions that every animal makes regarding fitness reward. They can maximize reproductive success by selection of those habitats that guarantee the greatest fitness output. We consider the host population as a habitat of a parasite population. Consequently, hosts (=habitats) that differ quantitatively or qualitatively will support different numbers of parasites. The nature of habitat selection can be detected by isodars, lines along which habitat selection yields equivalent fitness reward. We applied this approach to study host selection of five fleas, each infesting two desert rodents. Xenopsylla conformis, Xenopsylla ramesis, Nosopsyllus iranus theodori and Stenoponia tripectinata medialis parasitize Gerbillus dasyurus and Meriones crassus. Synosternus cleopatrae pyramidis parasitizes Gerbillus andersoni allenbyi and Gerbillus pyramidum. Three fleas (X. conformis, X. ramesis and S. c. pyramidis) were able to perceive quantitative (amount of the resource; e.g. organic matter in the nest for flea larvae) and/or qualitative (pattern of resource acquisition; e.g. host defensiveness) differences between hosts. Two other fleas did not perceive between-host differences. X. conformis was a density-dependent host selector that showed sharp selectivity at low density. X. ramesis and S. c. pyramidis were density-independent host selectors with a direct correspondence of density with habitat quality. N. i. theodori and S. t. medialis were nonselectors with no relationship at all between density and host quality. The results of the application of the isodar B. R. Krasnov ()) · G. I. Shenbrot Ramon Science Centre and Mitrani Department of Desert Ecology, Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev, P.O. Box 194, 80600 Mizpe Ramon, Israel e-mail:
[email protected] Tel.: +972-8-6586337 Fax: +972-8-6586369 I. S. Khokhlova The Wyler Department of Dryland Agriculture, Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, Israel
theory suggest that ectoparasites, like other animals, behave as if they are able to make choices and decisions that favour environments in which their reproductive benefit is maximized. Keywords Parasites · Habitat selection · Fitness · Quantitative host difference · Qualitative host difference
Introduction A common theme in modern evolutionary ecology is that the behaviour of an individual is greatly influenced by the evolutionary motivation to maximize life-time fecundity (Lomnicki 1988). One of the mechanisms to maximize reproductive success is to select those habitats that guarantee the greatest fitness output. This statement is a keystone of the theory of habitat selection (Rosenzweig 1981, 1989, 1991) that is based on the mechanism of the ideal free distribution (IFD; Fretwell and Lucas 1970). According to this theory, fitness is a negative function of population density. Consequently, the relationships between fitness and density will be reflected in the distribution and abundance of individuals across habitats. Habitats that differ quantitatively or qualitatively will support different numbers of individuals. Habitat selection has been studied extensively in various animal taxa. However, most studies have been conducted on free-living animals, whereas habitat selection in parasites attracted much less attention. The main reason for this deficiency from an evolutionary ecology perspective is related to the common parasitological approach in which a parasite is considered as the “object” rather than the “subject” of the environmental and evolutionary processes that influence its behaviour and habitat selection (Sukhdeo and Bansemir 1996; Poulin and Morand 2000). In other words, parasitologists rarely consider parasites as individuals that make decisions regarding foraging and reproductive success (Sukhdeo and Sukhdeo 1994). Nevertheless, parasites form a large proportion of the diversity of life. Parasitism is suggested
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to be more common than all other feeding strategies (Sukhdeo and Bansemir 1996) and parasites supposedly make the same decisions that every animal has to make regarding resource acquisition and fitness reward. Parasite individuals are distributed across host individuals and, thus, the host population can be considered as a habitat of a parasite population. A habitat patch for a parasite is its individual host that provides the parasite with a place for living, foraging and mating. This is especially true for arthropod ectoparasites because their contact with the host is usually intermittent and an individual parasite during its lifetime can move from one host individual to another. When fitness decreases with density increase, individuals should successively occupy habitats of ever declining quality as their population grows. If the form of the density-dependent relationship is known, we can infer the habitat selection response simply by examining patterns of density in different habitats using isodar analysis. Isodar theory (Morris 1987a, 1987b; 1988, 1990) allows one to test the fit of population densities across habitats to an IFD model. This theory explains the mechanisms of habitat selection and demonstrates that quantitative and qualitative differences between habitats lead to predictable and easily tested differences in population density. These differences can be expressed as characteristic isodars, which are lines of equal fitness, and are plotted in density space (N1 plotted on N2) as lines at every point of which the fitness of individuals in one habitat is equal to that of individuals in another. To the left of the isodar, there are too many individuals in the habitat with the greater fitness relative to those in the other habitat, and the fitness there is depressed. A densitydependent habitat selector should move to the alternative habitat. To the right of the isodar, fitness in the habitat with the lower fitness is depressed. Isodars, thus, can be used to infer the nature of differences between habitats and help us to understand the form of population regulation (Morris 1987a, 1987b, Morris 1988) as follows: (1) the slopes of the isodars indicate qualitative habitat preferences as population density varies; (2) the intercepts of the isodars can be used to indicate the quantitative differences in habitat richness perceived by the consumers; and (3) nonsignificant regressions imply density-independent habitat selection. The isodar approach has been successfully applied to the population ecology of free-living animals (mammals – Morris 1989, 1996; Ovadia and Abramsky 1995; Abramsky et al. 1997; Shenbrot and Krasnov 2000; birds – Fernandez-Juricic 2001; fish – Rodriguez 1995). However, this approach has never been applied to the population ecology of parasites, though some are known to follow an IFD of density-dependent habitat selection (Kelly and Thompson 2000). Fleas (Siphonaptera) are permanent satellites of higher vertebrates, being most abundant and diverse on small mammals. Fleas possess numerous traits that suggest an important role of habitat selection in their evolution and host preference. They usually alternate between periods
when they occur on the body of their host and periods when they occur in its burrow or nest. In most cases, egg, larval and pupal development is entirely off-host. The larvae are not parasitic (except for a single species, Uropsylla tasmanica; Vatschenok 1988) and feed on organic debris and materials found in the burrow and/or nest of the host. The majority of rodent fleas parasitize more than one host species and the degree of association between a particular flea species and a particular host species varies (Marshall 1981). In addition, an individual flea is able to relocate from one host individual to another. This host-to-host transfer can occur either via social interactions between hosts or when a host individual visits an alien burrow or by the flea leaving its host and dispersing freely (Marshall 1981). The transfer can be between individuals of the same host species (analogous to among-patch within-habitat dispersal of free-living animals) as well as between individuals of different host species (analogous to inter-habitat dispersal). We studied the distribution of fleas on rodents in the Negev desert, Israel and found that in habitats of nonsandy plains, each of four flea species, namely Xenopsylla conformis, Xenopsylla ramesis, Nosopsyllus iranus theodori and Stenoponia tripectinata medialis, parasitize the two most common rodent species, Gerbillus dasyurus (average adult body mass 20 g) and Meriones crassus (average adult body mass 80 g) (Krasnov et al. 1997, 1998, 1999). These two hosts co-exist in several habitats of the study area (Krasnov et al. 1996a). In sand dunes of Holot Agur and Holot Halutza, one flea species, Synosternus cleopatrae pyramidis, parasitizes two co-habitating gerbils, Gerbillus andersoni allenbyi (average adult body mass 26 g) and Gerbillus pyramidum (average adult body mass 40 g) (Krasnov et al. 1999). We assume that the two rodent host species represent two habitats for a particular flea species. We attempt to explain flea distribution between the two hosts in the framework of the theory of habitat selection, which, in this application, can be considered as the theory of host selection. We hypothesized that fleas arrange themselves close to an IFD. We used isodars to detect the adaptive nature of their host selection. The predictions are that if fleas at various densities are able to access and choose the hosts in which their expected reproductive success is maximized, then a significant relationship will exist between the densities on the two hosts. In other words, host-selecting fleas are probably able to perceive interhost differences and have mechanisms to select those hosts (Fretwell and Lucas 1970; Rosenzweig 1981). If fleas are unable to make a choice, then no significant isodar will be found.
Materials and methods Study areas The study was conducted in the Ramon erosion cirque (3030'– 3040'N; 3439'–3505'E) and in Holot Agur-Holot Halutza regions
367 (3054'–3100’N; 3423'–3442'E), in the Negev desert, Israel. The climate of the Ramon cirque is characterized by hot, dry summers (mean daily air temperature during July is 34C) and relatively cold winters (mean daily temperature during January is 12.5C). Annual rainfall is 100 mm on the northern rim and 56 mm in the bottom of the cirque. The dominant vegetation consists of Retama raetam, Zygophyllum dumosum, Artemisia monosperma, Anabasis articulata, Atriplex halimus, and Noaea mucronata. Holot Agur and Holot Halutza are sandy regions situated in the western Negev desert. The landscape is represented by linear stabilized dunes, often with mobile ridges, covered by Artemisia monosperma, Echiochilon fruticosum and R. raetam. Average annual rainfall in the area is 108 mm, whereas mean daily air temperature during July is 25C and that during January is 11.1C.
easily accessible for self-grooming. The body surface of a rodent was calculated as that of a cylinder (TB-TL-GSL)BDp, where TBL is the average total body length from the tip of the snout to the tip of the tail, TL is the average tail length, GSL is the average greatest anterior-posterior length of the skull, BD is the diameter of the body, and p=3.14. Linear measurement of living animals does not allow accurate estimates to be made. Consequently, we used average values calculated for each species. We conducted measurements of TBL, TL, GSL and BD (€1 mm) on dead adult animals of each species and found low individual within-species variation in body surface. Coefficient of variation of body surface was 3.1% for M. crassus (n=20), 4.2% for G. dasyurus (n=69), 3.8% for G. a. allenbyi (n=26) and 2.9% for G. pyramidum (n=9). In total, 944 rodents were captured and 4,428 fleas were collected.
Flea species
Isodar analysis
X. conformis and X. ramesis are common ectoparasites of gerbils and birds throughout the Middle East. These two species have a parapatric distribution in the Ramon cirque in that X. conformis is displaced by X. ramesis on M. crassus and G. dasyurus from eastern (drier) to western (more mesic) habitats (Krasnov et al. 1997, 1998). Both species are active throughout the year, although their abundances in winter are low (Krasnov et al. 1997, 2002a). N. i. theodori and S. t. medialis are winter fleas. No imago has been found from April until December (Krasnov et al. 1997, 2002a). S. c. pyramidis is widely distributed in Israel and is characteristic of sand-dwelling gerbils (Theodor and Costa 1967; Krasnov et al. 1999). This flea is active throughout the year and does not demonstrate high seasonal variation in abundance (B. R. Krasnov and G. I. Shenbrot, unpublished data). All these flea species occur also on other rodents in the area (Krasnov et al. 1997, 1999). However, extremely low abundances and sporadic occurrence of these fleas on rodents other than M. crassus, G. dasyurus, G. a. allenbyi and G. pyramidum suggest that other rodents have little effect on the host selection process.
Interpretation of the isodar analysis follows Morris (1987a, 1987b, 1988). Situations where habitats differ quantitatively only, result in isodars with a non-zero intercept and slope equal to 1.0 (parallel population regulation), whereas situations where habitats differ qualitatively only, result in isodars with zero intercept and a slope >1.0 (divergent population regulation). If habitat 1 is qualitatively and quantitatively more suitable than habitat 2, the resulting isodar has a non-zero intercept and a slope >1.0 (divergent population regulation maintained) (Morris 1988). If a quantitatively superior habitat is also the one with the lower foraging efficiency, the slope of the fitness function with density is steeper in the habitat with the greater resource, and the fitness curves can cross (Morris 1988). This situation produces an isodar with a non-zero intercept and a slope
