Ecology of flea locomotion
The locomotory patterns of fleas reflect their way of life as parasites of fur- or feather-covered hosts. Fleas are able to move through dense host pelage and withstand the host's anti-parasitic grooming. They also are able to jump, to move through the substrate of a host's burrow or nest and to move on vertical surfaces (e.g. fleas parasitic on bats). Here, I briefly review the morphological and physiological aspects of flea locomotory features that facilitate the successful exploitation of hosts.
8.1 On-host locomotion
Flea locomotion in host pelage or feathers differs from that of other mammal and bird ectoparasites. For example, Nycteribiidae (bat flies) have a compressed dorsoventral body and long, spider-like legs (Dick & Patterson, 2006). They are capable of fast sliding movements above the fur of the host. In contrast, the laterally compressed body, high and narrow head capsule and flexible joints of the thorax and abdomen of fleas allow them to move through host pelage by dividing the hair during forward movement.
The flea thorax consists of three separate modified segments (pro-, meso- and metathorax), whereas the abdomen consists of 10 segments. The posterior margins of each segment form collars that overlie the anterior margins of the next segment. As a result, these segments are able to 'squeeze' into each other. In contrast to most winged insects, separation of the mesothorax and metathorax in fleas leads to the absence of a pterothorax which is characteristic of other holometabolous insects. It has been suggested that flea ancestors also did not possess a pterothorax (Medvedev, 2003a, 2005). This lack could be considered as a pre-adaptation to ectoparasitism on fur-covered hosts (see Chapter 4). Separation of the thoracic segments, possession of movable between-thoracic sclerites and highly developed phragmata are features that allow high flexibility of the flea body.
In contrast to other Holometabola, the flea prothorax is not reduced but is tightly connected with the head. The lower part of the prothorax (pleuroster-num) is strongly elongated, exceeding at least two times the length of the pronotum. The pleurosternum protrudes anterior to the notum and envelops the posterior part of the head from beneath. As a result, the head and prothorax together constitute a frontal complex which is movable relative to other thoracic segments (Medvedev, 2003a, b). Structures of this complex also include maxillary plates (first segments of the maxilla that possess highly developed collars) and fore coxae. Due to an elongated pleurosternum, fore coxae are situated anterior to the notum. The maxillary plates are broad in the middle, but narrow at the bases and apices. As a result, the anterior frontal complex of a flea is shaped like a keel which divides the host's hairs or feathers or particles of the substrate of its burrow/nest during flea movement. In addition, the frontal and occipital regions of some fleas are covered with basiconic sensilla and large numbers of pores (Amrine & Lewis, 1978; de Albuquerque Cardoso & Linardi, 2006). These pores are openings for the epidermal glands and exude oily substances onto the cuticular surface of a flea facilitating movements among the host hairs (Rothschild & Hinton, 1968; but see Smith & Clay, 1985 and de Albuquerque Cardoso & Linardi, 2006).
8.2 Off-host locomotion 8.2.1 Mechanics of a flea jump
The jump is the most conspicuous characteristic of fleas. For example, Pulex irritans can leap a distance of 33 cm, about 200 times the length of their bodies (Rothschild et al., 1972), and the stick-tight flea Hectopsylla narium jumps as far as 25 cm (Blank et al., 2007). The recorded heights of flea jumps are no less impressive, attaining, for example, 16.5 cm in Echidnophaga myrmecobii (Mules, 1940) and 33 cm in P. irritans and Ctenocephalides felis (Rothschild et al., 1972, 1975). Jumping allows these wingless blood-sucking insects to attack their hosts successfully, although their major type of locomotion remains walking (Marshall, 1981a).
Enthralled by fleas' jumping abilities, several scientists have asked what are the morphological and physiological mechanisms that allow fleas to accomplish these leaps (e.g. Bennet-Clark & Lucey, 1967; Rothschild et al., 1973; Bossard,
2002; Krasnov et al., 2003a, 2004b). Sometimes this interest has even resulted in humiliating mockeries from the public media (Abrahams, 2004; O'Hare, 2005). Undoubtedly, the major credit in unveiling flea jump mechanisms belongs to Miriam Rothschild and her collaborators who defined this locomotion as a 'flying leap' (Rothschild et al., 1973) and fleas as 'insects which fly with their legs' (Rothschild & Neville, 1967). In their classical series of papers, Rothschild and coauthors (Rothschild et al, 1973, 1975; Rothschild & Schlein, 1975) reported that the main sources of flea saltatorial power are the muscles of the hind legs and a rubber-like protein (resilin) located in the pleural arch. The resilin pad is homologous with the wing-hinge ligaments in flying insects. After being stretched and then released, resilin yields about 97% of its stored energy (Rothschild et al., 1975). An additional advantage of resilin is that the release of energy stored in this elastic structure seems to be a purely physical process and, unlike the chemically controlled release of energy during muscle contraction, does not depend strongly on air temperature (Rothschild et al., 1973).
The jump of the rat flea Xenopsylla cheopis was described in detail by Rothschild et al. (1973, 1975). When a flea prepares to jump, it squats down and contracts its body. It orients its hind femurs almost upright, so that only its hind trochanters and tibiae are in contact with the substrate. Contraction of epipleural and trochanteral depressor muscles squeezes the resilin in the pleural arch. Thoracic and coxa-abdominal catches are engaged. Upon the jump, the levator and the ventral longitudinal muscles relax which causes the femur to descend and the catches to be released. The energy stored in the resilin and the arched pleural and coxal wall is freed and rapidly transferred to the legs providing an acceleration of about 150 g in about 1 millisecond. During the jump, the flea arranges its middle or hind legs in an upright position to be able to hook into a host pelage or feathers. During descent, the flea spreads its legs widely sideways and thus controls its landing.
8.2.2 Jumping capacity, sexual size dimorphism and morphology
The ability to make long and high jumps varies greatly among flea species (Cadiergues et al., 2000). Rothschild et al. (1975) argued that this ability and the development of the pleural arch are related. Indeed, pleural arches and resilin protein are well developed in fleas with high jumping capacity such as P. irritans, parasitic on medium and large mammals, and Ceratophyllus styx, parasitic on birds (Bates, 1962; Rothschild et al., 1975), but are absent or greatly reduced in poor jumpers such as specific bat fleas Ischnopsyllidae and sessile Tunga (Traub, 1972a; Rothschild et al., 1973). However, some fleas with extremely low jumping ability have well-developed pleural arches (e.g. Jordanopsylla allredi: Hastriter et al., 1998). Nevertheless, the idea that the size of certain parts of the locomotory apparatus can be indicative of jumping capacity, and thus can be used for comparisons among individuals, between genders and among species, has been suggested. Inspired with this idea, Tripet et al. (2002a) measured pleural height in preserved flea specimens to be used as indicators of flea mobility for broad comparisons among species of bird fleas from different geographical and host ranges. They found a negative correlation between flea mobility (expressed via measurements of pleural height) and the degree of host colonialism and a positive correlation between flea mobility and their host range. Nonetheless, these conclusions are valid only if pleural height and jumping capacity are indeed correlated.
Furthermore, Rothschild et al. (1975) studied gender differences in jumping capacity in X. cheopis, Spilopsyllus cuniculi and Nosopsyllus fasciatus. This study demonstrated that, on average, males jumped a shorter distance than females, which is not surprising due to obvious sexual size dimorphism in fleas, with males smaller than females (see Chapter 7). However, the data were not corrected for body size dimorphism and, thus, it was unclear whether size was the only source of gender difference in locomotory performance or other factors were also involved.
The only experimental study with simultaneous measurements of jumping performance among individuals within species, between genders and among species of fleas was carried out by Krasnov et al. (2003a) who searched for correlates between jumping performance and morphometrics of the locomotory apparatus in seven flea species. A flea was allowed to jump, and the jump length was measured. Then, the flea was anaesthetized and measured. Maximal body length was used as a trait describing body size, whereas the pleural height and the length of coxa, femur and tibia of the left hind leg reflected the mor-phometrics of the locomotory apparatus. Surprisingly, this study demonstrated that morphometrics of the jumping apparatus did not correlate with jumping capacity; no correlation was found between jumping performance and any measure of the locomotory system either among individuals, between genders or among species.
In addition, it was found that interspecific differences in jumping capacity were not related to interspecific differences in body size and locomotory mor-phometrics (Fig. 8.1; compare with Fig. 7.1a). These results hold also when controlling for the confounding effect of phylogeny. Furthermore, females were generally better jumpers than males, even when accounting for sexual size dimorphism (Fig. 8.1) (Krasnov et al., 2003a). However, males and females of Stenoponia tripectinata demonstrated similar jumping ability despite body size
Table 8.1 Absolute female: male jumping performance ratio and the fraction of performance dimorphism explained by size dimorphism in six flea species
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