Energy costs of blood digestion in a host-specific haematophagous parasite
1 Ramon Science Center and Mitrani Department of Desert Ecology, Jacob
Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev,
Mizpe Ramon 80600, Israel
2 Albert Katz International School for Desert Studies, Jacob Blaustein
Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer
Campus, Israel
3 Desert Animal Adaptations and Husbandry, Wyler Department of Dryland
Agriculture, Jacob Blaustein Institutes for Desert Research, Ben-Gurion
University of the Negev, Beer Sheva 84105, Israel
4 Science Division, Truman State University, Kirksville, MO 63501,
USA
* Author for correspondence (e-mail: krasnov{at}bgumail.bgu.ac.il)
Accepted 4 May 2005
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Summary |
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Key words: CO2 emission, digestion, flea, host specificity, metabolic cost, Acomys cahirinus, Gerbillus dasyurus
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Introduction |
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Cost/benefit analyses for foraging decisions that take into account the
energetic outlay for digestion have been done extensively for various
vertebrates such as reptiles (Segor and
Nagy, 1994), birds (Piersma et
al., 2003
; van Gils, 2005) and mammals
(Williams et al., 2004
).
However, this is not the case for invertebrates, where only few studies have
been made (Beiras and Camacho,
1994
; Yang and Joern,
1994
). Furthermore, energetic components of digestive physiology
have been examined only rarely in parasitic organisms, although parasites form
a large proportion of the diversity of life. Parasitism is suggested 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.
Different aspects of digestive physiology of parasites, especially
haematophagous arthropods such as mosquitoes
(Pascoa et al., 2002;
Briegel, 2003
), fleas
(Richards and Richards, 1968
;
Vatschenok et al., 1976
) and
ticks (Coons et al., 1986
;
Rechav and Fielden, 1995
),
have been reported. In particular, different ectoparasitic arthropods have
been shown to increase their metabolic rate during blood digestion (Fielden et
al., 1999
,
2004
;
Gray and Bradley, 2003
).
However, the energetic costs of digestion of a food resource (e.g. blood)
extracted by a parasite from different hosts have never been studied. These
costs would include secretion of enzymes, the metabolism of the blood
components, the excretion of the toxic by-products and the heat increment of
feeding (see Clements, 1992
for
a review).
Differential energy costs of digestion of food obtained by a parasite from different hosts may have important ecological and evolutionary implications. A lower energy cost for resource processing would allow a parasite to allocate more energy for other competing requirements of an organism (host location, mating, oviposition). This would supposedly increase fitness reward stemming from selection of an appropriate host and, thus, can shape the coevolutionary process between hosts and parasites. At the evolutionary level, differences in the energy cost of digestion of a resource extracted by a parasite from one host species rather than from another host species may reflect specific adaptations of a parasite to exploit successfully a particular host species. Specific adaptations to this host species were favoured by natural selection due to differential fitness rewards between hosts. Thus, energy expended by a parasite to process food obtained from a host may be an indicator of evolutionary success of a parasite in the exploitation of a host species.
We examined energy expenditure, as determined by measurement of
CO2 emission, of the flea Parapulex chephrenis Rothschild
after feeding on blood of different hosts. Fleas (Siphonaptera) are
holometabolous, blood-sucking, ectoparasitic insects that exploit higher
vertebrates, being most abundant and diverse on small to medium-sized mammal
species (Marshall, 1981). The
larvae of fleas are not usually parasitic and feed on organic debris and
materials found in the nest of the host. After emergence from the pupa and
cocoon, adult fleas must locate a suitable host to complete their life cycle.
Fleas vary in the degree of association with their host species from being
highly host-specific to being host-opportunistic
(Marshall, 1981
).
P. chephrenis is a highly host-specific parasite associated with
the Egyptian spiny mouse Acomys cahirinus Wagner
(Krasnov et al., 1997). A.
cahirinus is a specialized rock-dweller that co-exists in rocky habitats
with the gerbil Gerbillus dasyurus Wagner, from which P.
chephrenis is absent. When A. cahirinus was recorded
occasionally in other habitats, it was also parasitized by P.
chephrenis. Moreover, P. chephrenis was able to discriminate
between different host species, selecting A. cahirinus over G.
dasyurus in host-choice experiments
(Krasnov et al., 2002a
). In
the laboratory experiments, P. chephrenis was shown to be able to
survive and reproduce on G. dasyurus
(Krasnov et al., 2002a
).
However, the egg production of P. chephrenis fed on this host was
almost six times less than when it fed on A. cahirinus
(Krasnov et al., 2002a
).
Physical and chemical properties of blood are important characteristics of
a host to which a host-specific ectoparasite is expected to be adapted
(Marshall, 1981). However,
studies of the effect of feeding ectoparasites on different host species are
scarce and indirect (e.g. Prasad,
1969
). Moreover, in most laboratory studies of the rate of blood
digestion, ectoparasitic arthropods were fed on laboratory animals rather than
on their natural hosts. For example, wild rodents were used as hosts in only
eight of 27 studies on fleas while the others used mainly laboratory mice,
rats, hamsters and guinea pigs (cited by
Vatschenok, 1988
).
We hypothesized that different host species exert different energetic costs on the digestion of blood by a flea. To test this hypothesis, we studied CO2 emission during digestion of a single blood meal extracted by a host-specific P. chephrenis from a preferred (A. cahirinus) and non-preferred (G. dasyurus) host. We predicted that the energy costs of digestion would be lower for digesting blood from A. cahirinus than blood from G. dasyurus.
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Materials and methods |
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Progenitors of the rodent colonies were captured at the Ramon erosion
cirque, Negev Highlands, Israel (30°35' N, 34°45' E). The
rodents were maintained in glass cages (60x50x40 cm) at 25°C
with a photoperiod of 12 h:12 h(L:D), using dried grass as bedding material.
They were offered millet seeds and alfalfa (Medicago sp.) ad
libitum and commercial cat chow or larvae of flour beetles once a week.
No water was available to the rodents as alfalfa supplied enough for their
needs. The infestation level of fleas on rodents in our colonies comprised
approximately 75% of the natural level of flea infestation (68 fleas
per rodent; see Krasnov et al.,
1997). No adverse effects on body mass and food intake of infested
rodents were observed. The experimental protocol met the requirements of the
1994 Law for the Prevention of Cruelty to Animals (Experiments on Animals) of
the State of Israel by the Ben-Gurion University Committee for the Ethical
Care and Use Animals in Experiments (License IL-19-04-2001). Details on
maintenance of fleas and rodents were published elsewhere (Krasnov et al.,
2002a
,
2003
).
Experimental design
Feeding of fleas on rodents was carried out at a room temperature of
25°C and relative humidity of 70%. We used A. cahirinus and
G. dasyurus; 10 male adults of each species. Each rodent (A.
cahirinus or G. dasyurus) was placed in a wire mesh (5x5
mm) tube (10 cm length and 2 cm diameter) that limited movement and did not
allow self-grooming. To avoid the potential effect of acquired resistance
(Willadsen, 1980), rodents
were subjected to P. chephrenis parasitism 35 times (once
daily) prior to experiments. Each tube with a rodent was placed in an
individual white plastic pan, and 20 male or female fleas were placed on each
rodent. Fleas were collected after 2 h. Groups of fleas
(N=510) were weighed to the nearest 0.01 mg (Precisa Balance,
model 290 SCS; Precisa Instruments AG, Dietikon, Switzerland) prior and after
feeding and the difference was calculated as blood consumed. Fleas with high
midgut engorgement (see below) only were weighed after feeding.
We assessed the level of flea midgut engorgement by examination of each flea under a light microscope (without dissection) and by using the following classification: (a) low (less than 30% of midgut is filled with blood); (b) medium (3070% of midgut is filled with blood); and (c) high (more than 70% of midgut is filled with blood). We selected fleas with high midgut engorgement, weighed them in groups (N=5) and placed them individually into 20 ml glass vials covered by a 5x5 cm nylon screen. Then, vials were placed in refrigerated incubators (FOC225E; Velp Scientifica srl, Milano, Italy) and maintained at 25°C and 92% relative humidity.
We measured CO2 emission in newly emerged, unfed fleas as well
as in fed fleas at different stages of blood digestion. Classification of the
stages of blood digestion was modified from a classification of Ioff
(1941) and has been used in
our previous studies (Krasnov et al.,
2002b
). We distinguished the following stages: (1) early
midgut stretched and fully filled with light scarlet or dark red blood;
(2) middle the contour of the midgut is jagged and the
content is dark brown or black; and (3) late midgut contains only
remnants of digested blood or is empty. The duration of each stage of blood
digestion in P. chephrenis fed on A. cahirinus or G.
dasyurus is reported elsewhere
(Krasnov et al., 2003
). In
brief, the first, second and third stages of digestion of the first blood meal
lasted 78, 910 and 1415 h, respectively, when a flea fed
on A. cahirinus, and 89, 1213 and 1011 h,
respectively, on G. dasyurus. We measured CO2 emission
after 3, 12 or 24 h post-feeding. Prior to a measurement, we examined the
midgut of each flea under light microscopy to verify the blood digestion
status. Treatments, therefore, differed in host species (A. cahirinus
or G. dasyurus), flea sex (male or female) and stage of blood
digestion (1st, 2nd or 3rd). Each treatment (610 fleas) was replicated
10 times, totalling two hosts x two sexes x three stages of
digestion x 10 replicates + 10 measurements of CO2 emission
of unfed fleas=130 experiments. Fleas were assigned to different treatments at
random.
Respirometry
A flow-through respirometry system was used to measure CO2
emission. Incurrent air was scrubbed of CO2 and H2O
vapour by Drierite (700 ml volume) and Ascarite (25 mlvolume) columns,
respectively, and was pumped through a respirometer chamber made of tygon
tubing (6.5 mm internal diameter, 3 ml volume) at a flow rate of 50 ml
min-1. Flow rate was controlled by a mass flow controller (model
FC-260; Tylan, Rancho Dominquez, CA, USA). This dry, CO2-free air
constituted the baseline measurements for all flow-through measurements.
Carbon dioxide content (p.p.m.) of air exiting the respirometer chamber,
measured by a CO2 analyzer (model 6262; LI-COR, Lincoln, NE, USA)
in conjunction with data-acquisition software (Datacan V; Sable Systems,
Henderson, NV, USA), was sampled every 2 s. Tygon tubing (3.3 mm internal
diameter) was used to plumb the system. A stable temperature for the air
inside the respirometer tubing (25°C) was regulated by placing the chamber
and preceding 6 m of incurrent tygon tubing into a water bath (model 1013S;
Fisher Scientific, Pittsburgh, PA, USA). Carbon dioxide emission for fleas was
recorded for 1 h. Baseline measurements were made before and after each
recording to determine zero CO2 and to correct for instrument
drift. Fleas were measured in groups (N=610) since
CO2 emission of individuals was very low and only slightly above
baseline levels. Before being placed in the respirometer chamber, groups of
fleas were weighed to the nearest 0.01 mg. Details of the protocol as well as
details on the repeatability of the measurements can be found elsewhere
(Fielden et al., 2004;
Krasnov et al., 2004a
).
Data analysis
The effect of host species and flea sex on the amount of blood consumed by
a flea per individual and per unit body mass of unfed flea was analyzed using
two-way analysis of covariance (ANCOVA; with body mass as a covariate because
of sexual size dimorphism) and two-way analysis of variance (ANOVA),
respectively.
All computerized CO2 emission recordings were processed using
the analysis package of Datacan V. Each recording was converted from p.p.m. to
µl CO2 h-1. We analyzed both mass-specific (per unit
body mass) and mass-independent metabolic rate of CO2 emission.
Distribution of all dependent variables did not deviate significantly from
normal (KolmogorovSmirnov's tests; non-significant), so parametric
statistics were applied. We analyzed mass-specific rates of CO2
emission of fed fleas using three-way ANOVA with host species, flea sex and
stage of blood digestion as independent variables. These variables were also
used in ANCOVA of mass-independent rate of CO2 emission with body
mass as a covariate (Packard and Boardman,
1999). In addition, we analyzed mass-specific and mass-independent
rate of CO2 emission in newly emerged versus adult fleas
using one-way ANOVAs and ANCOVAs (with body mass as a covariate),
respectively, with flea feeding state (unfed and three stages of digestion) as
an independent variable separately for male and female fleas fed on each host
species. We used Tukey's HSD test for multiple comparisons. This test is
highly conservative (Winer et al.,
1991
).
We also calculated mass-specific energy cost of a flea for digestion of 1
mg of blood of A. cahirinus or G. dasyurus during one hour
of the first, second or third digestion stages. We refer to the energy
expended to digest 1 mg of blood as specific dynamic effect (SDE), as
suggested by Withers (1992).
Withers (1992
) defined SDE as
reflecting `...the energetic requirements of many processes that occur as a
consequence of food digestion, including mechanical processing, energy
exchange through catabolic and anabolic biochemical pathways and amino acid
deamination and nitrogen excretion' (p.
108). First, we calculated the mean volume of CO2 emitted
per hour per mg of body mass of newly emerged unfed fleas (no sexual
difference in this parameter was found in P. chephrenis; see
Results). Then, we used this value to calculate the difference in the
mass-specific volume of emitted CO2 between a digesting flea and
that of an unfed flea for each respirometric replicate. Difference in body
mass of fleas before and after feeding (reduced to 1 mg of body mass before
feeding) was considered to be equal to the mass-specific amount of blood
consumed. The quotient of mass-specific difference in the volume of emitted
CO2 between digesting and unfed fleas and mass-specific amount of
consumed blood was considered as a mass-specific indicator of SDE (energy
expended for digestion of 1 mg of blood) during the first, second or third
digestion stage. To convert metabolic rate measured as the rate of
CO2 emission to an energy equivalent, we assumed a respiratory
quotient (RQ) of 0.8. This was determined previously for unfed females of the
tick Amblyomma marmoreum by Lighton et al.
(1993
) and seemed a reasonable
assumption for haematophagous arthropods. An RQ of 0.8 gives an energy
equivalent of 24.5 J ml-1 CO2
(Schmidt-Nielsen, 1990
). SDE
of a whole flea was calculated in a similar way. These values were used to
calculate the energy cost of blood digestion and were analyzed using three-way
ANOVA and three-way ANCOVA (with initial body mass as a covariate),
respectively, between host species and flea sexes and among digestion
stages.
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Results |
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Mass-specific rate of CO2 emission of fed fleas was higher than that of unfed fleas (ANOVA; males, F1,38=13.9 if fed on A. cahirinus and F1,38=12.2 if fed on G. dasyurus; females, F1,38=7.2 if fed on A. cahirinus and F1,38=16.4 if fed on G. dasyurus; P<0.005 for all; Table 1). The same was true for mass-independent rate of CO2 emission (ANCOVA with body mass as a covariate; ANOVA; males, F1,37=12.7 if fed on A. cahirinus and F1,37=6.9 if fed on G. dasyurus; females, F1,37=13.8 if fed on A. cahirinus and F1,37=4.8 if fed on G. dasyurus; P<0.05 for all; Table 1).
|
Both mass-specific and mass-independent rates of CO2 emission differed significantly among stages of blood digestion and were affected significantly by host species and flea sex, being, in general, higher (1) when digesting G. dasyurus than A. cahirinus blood and (2) in females than in males (Table 2). However, significance of the interaction terms indicated that differences in CO2 emission among stages of digestion were manifested differently in male and female fleas fed on different hosts. Indeed, mass-specific rate of CO2 emission did not differ between consecutive stages of blood digestion in both male and female fleas fed on A. cahirinus (Tukey's HSD tests; P>0.1 for all; Table 1). By contrast, male and female fleas fed on G. dasyurus demonstrated significantly higher mass-specific rates of CO2 emission during the 1st and 2nd digestion stages than during the 3rd stage (Tukey's HSD tests; P<0.05; Table 1). The same was true for mass-independent rates of CO2 emission (Table 1). In addition, mass-independent rates of CO2 emission in females fed on G. dasyurus were significantly lower during the 2nd digestion stage than the 1st stage (Tukey's HSD tests; P<0.05; Table 1).
|
Mass-specific SDE of fleas showed a significant effect of host species (F1,108=58.9; P<0.001); fleas expended significantly more energy digesting blood of G. dasyurus than blood of A. cahirinus (Fig. 1). The difference between digestion stages in SDE was marginally significant (F2,108=2.9; P=0.06) whereas SDE was similar in males and females (F1,108=0.7; P>0.3). The only significant interaction was between host species and digestion stage factors (F2,108=3.6; P<0.03). This was manifested in lower SDE during the third stage of digestion than the second stage for males or the two first stages for females when fleas fed on G. dasyurus (Fig. 1).
|
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Discussion |
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Effect of host species
Besides the lower energy costs of P. chephrenis to digest blood of
A. cahirinus than blood of G. dasyurus, it took P.
chephrenis less time to digest the A. cahirinus blood
(9.1±0.6 versus 15.4±0.9 h for the 2nd stage of
digestion; Krasnov et al.,
2003). This between-host difference in digestion time could be due
to between-host variability in the resistance of blood cells (both red and
white) to haemolytic activity of the flea digestive system
(Vatschenok, 1988
).
Consequently, a blood meal from A. cahirinus would probably produce a
higher fitness reward for P. chephrenis than a blood meal from G.
dasyurus. Indeed, a previous study showed that female P.
chephrenis produced 46 times more eggs when fed on A.
cahirinus than on G. dasyurus
(Krasnov et al., 2002a
). A
reduction in egg production and viability for parasites fed on a non-preferred
host has been reported for other species. As early as the beginning of the
twentieth century, Goeldi
(1905
) recognized that
mosquito egg production was affected by host blood. The rat fleas
Xenopsylla cheopis and Xenopsylla astia failed to reproduce
when they fed on humans (Seal and
Bhattacharji, 1961
), and fecundity and egg hatchability in X.
cheopis were higher when the fleas fed on Rattus rattus than on
Bandicota bengalensis (Prasad,
1969
). Moreover, flea species that are commonly believed to be
host opportunistic demonstrate differential reproduction output, dependent on
host species. Xenopsylla conformis produced three times the number of
eggs when exploiting the jird Meriones crassus than the gerbil
Gerbillus dasyurus (Krasnov et
al., 2004b
).
Differential fitness reward of a haematophagous ectoparasite according to
host species suggests that ectoparasites can adapt to feed on blood with host
species-specific physiological and biochemical parameters (viscosity, protein,
glucose, lipid content). However, little information is available on host
blood characteristics that could account for preferences in haematophagous
parasites. Host preferences shown by tsetse flies for certain mammals do not
appear to be based on the nutritional value of the blood
(Moloo et al., 1988), whereas
some species of mosquitoes show a preference for human blood over mouse blood
based on amino acid composition, specifically isoleucine content
(Harrington et al., 2001
).
The energy cost of digestion is not the only parameter that determines
energetic efficiency of foraging and, ultimately, of host selection by a
parasite. Other expenditures associated with foraging activities include
searching for the host, feeding site selection for piercing the skin of the
host and obtaining a blood meal, time required for a blood meal and surviving
anti-parasitic grooming effort of a host. For example, hosts can differ in
abundance and spatial distribution and, thus, in their availability for a
parasite. The difference in feeding rate of a haematophagous parasite on
different hosts could be a result of the morphology of the mouthparts that can
penetrate the skin of some hosts but not others
(Marshall, 1981). Previous
studies on the patterns of flea foraging demonstrated that these costs are
usually lower for a preferred host than for other hosts. For example, time
from contact with the host to the beginning of feeding, which can be
considered the latency of foraging decision, was less in P.
chephrenis feeding on A. cahirinus than on G. dasyurus
(Krasnov et al., 2003
).
Digestion and metabolic rate
Higher CO2 emission in fed versus unfed fleas supports
our previous findings on Xenopsylla ramesis that fleas that had a
blood meal had significantly higher metabolic rates than newly emerged unfed
fleas (Fielden et al., 2004).
This difference in energy expenditure is mainly a consequence of the energy
costs of consuming, processing and digesting blood by the haematophagous
arthropods. In addition, feeding may stimulate some physiological process that
causes differential metabolic responses in starving fed and unfed
haematophagous arthropods such as sperm or egg production
(Gray and Bradley, 2003
).
In fleas fed on G. dasyurus, energy costs generally decreased at
the third stage of digestion. This decrease of energy expenditure may be
associated with the absence of a digestive process per se at the
third stage of digestion (Vatschenok and
Solina, 1969). Indeed, the earlier stages of digestion in fleas
include haemolysis and digestion of blood to haematin (the final product of
blood digestion; Vatschenok,
1988
), whereas the third stage seems to reflect mechanical
(release of the undigested remnants and final products) rather than
biochemical processes (Vatschenok and
Solina, 1969
; Brukhanova et
al., 1978
). The lack of differences in energy cost of different
digestion stages in fleas fed on A. cahirinus can be related to
overall low energy expenditure during this process and, thus, possible
undetectability of these differences by our equipment.
Sexual difference
Female fleas invested more energy for digestion of blood of a non-preferred
host than did males. In addition, time required for digestion of G.
dasyurus blood has been found to be longer in females than in males
(Krasnov et al., 2003, but see
Vatschenok et al., 1976
for
X. cheopis). This suggests a strong female-biased sexual difference
in the total amount of energy spent for digestion of a blood meal from a
non-preferred host.
This difference between sexes can be related to the unpredictability of
host finding by a flea and to the association of flea reproduction with blood
feeding. Adult fleas alternate periods on the host with periods in the burrow
or nest (Ioff, 1941). Since a
host may not always return in a regular or predictable manner to its nest or
resting area, survival of fleas depends in part on their ability to use other
host species. Indeed, female P. chephrenis can survive and reproduce
when fed on G. dasyurus, although its fecundity decreases drastically
when exploiting this host (Krasnov et al.,
2002a
). Furthermore, blood feeding in fleas triggers sperm
transfer, mating behaviour, egg maturation and oviposition
(Iqbal and Humphries, 1970
;
Hsu and Wu, 2001
;
Dean and Meola, 2002
). Male
fleas are able to mate after a single blood meal
(Iqbal and Humphries, 1976
),
but females of most flea species have to feed repeatedly for their eggs to
mature (Vatschenok, 1988
).
Consequently, the urgency of a blood meal is more critical for females than
for males. As a result, females would benefit from investing energy in
digesting blood from a strange host, especially given that the location and
successful attack of a preferred host is not guaranteed. Another, not
necessarily alternative, explanation of the sexual differences in the
digestion of blood of a non-preferred host is related to the fact that, during
digestion, fleas essentially transform host blood into eggs or sperm.
Vitellogenesis or oogenesis may be more energy costly than spermatogenesis,
especially when food with biochemical components that differ in some way from
that of the specific host is consumed.
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Acknowledgments |
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