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Journal ArticleDOI

Parasitism and developmental plasticity in Alpine swift nestlings

01 Jul 2003-Journal of Animal Ecology (John Wiley & Sons, Ltd)-Vol. 72, Iss: 4, pp 633-639
TL;DR: The present study shows in a wild bird population that nestling hosts can compensate for the effect of parasitism on their phenotype, and emphasizes the need to take the dynamics of parasite populations into account in studies of host-parasite relationships.
Abstract: Summary 1 Development plasticity is a common evolutionary and phenotypic response to poor growth condition, in particular in organisms with determinate growth such as most birds and mammals. Because various body structures can contribute differently to overall fitness, natural selection will adjust the degree of plasticity of each structure to its proportionate contribution to fitness at a given life stage. 2 Two non-mutually exclusive mechanisms can account for plasticity in the growth of offspring to compensate for the effect of parasites. First, if parasite infestation levels fluctuate over the nestling period, parasitized young may show reduced growth until peak parasite infestation, and accelerated growth once the conditions improve (the accelerated growth hypothesis). Secondly, if the period of tissue maturation is not fixed in time, hosts may grow slower than parasite-free hosts but for a longer period of time (the delayed maturation hypothesis). 3 To test whether hosts compensate for the effects of parasites on their development, the load of the blood-sucking louse-fly Crataerina melbae Rondani in the nests of Alpine swifts, Apus melba Linnaeus, was increased or decreased experimentally. Parasite prevalence was 100% in both treatments, but intensity (no. of parasites per nestling) was significantly lower for deparasitized nestlings. In both treatments, parasite intensity increased up to halfway through the rearing period (i.e. 30 days of age) and decreased afterwards. 4 In line with the accelerated growth hypothesis, wings of parasitized nestlings grew at a lower rate than those of deparasitized ones before the peak of parasite infestation, but at a greater rate after the peak. Louse-flies had no significant effect on the growth of body mass. In agreement with the delayed-maturation hypothesis, wings of parasitized nestlings grew for 3 additional days and were of similar size at fledging as in deparasitized birds. 5 In summary, the present study shows in a wild bird population that nestling hosts can compensate for the effect of parasitism on their phenotype. It emphasizes the need to take the dynamics of parasite populations into account in studies of host–parasite relationships, and to investigate the effect of parasites on host development over the entire growing period rather than only at fledging, as employed traditionally.

Summary (1 min read)

Jump to: [Discussion] and [(a)]

Discussion

  • Adaptive developmental plasticity is the process by which an organism alters its growth and maturation to counter the impact of detrimental rearing conditions (Schew & Ricklefs 1998) .
  • Previous studies found that parasites reduce body size or body condition of their hosts (e.g. Richner et al. 1993) , and some studies also.

(a)

  • Reported an increase in the wing growth rate of experimentally parasitized hosts (Saino, Calza & Møller 1998; Szép & Møller 1999) .
  • To their knowledge the present experimental study is the first to investigate developmental plasticity in relation to the intranest population dynamics of parasites.
  • The authors showed that wing growth rate of parasitized hosts decelerated during the peak infestation and accelerated thereafter.
  • Parasitized nestlings were also found to fledge later but at a similar size to deparasitized ones.
  • These findings support the hypothesis that developmental plasticity is not only a strategy to compensate the impact of temporary poor feeding conditions or low ambient temperatures, but also to compensate the effect of parasitism.

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Published in Journal of animal ecology 72, issue 4, 633-639, 2003
which should be used for any reference to this work
1

is usually based on experiments where parasite load
is manipulated early during host development and
the effect measured close to the end (e.g. Møller 1990;
Richner, Oppliger & Christe 1993; Clayton & Tompkins
1995). In species where the effect of parasites on early
growth can be compensated later, the effects of para-
sites may therefore not be detected. Given the poten-
tially long-term fitness consequences of poor early
growth caused by parasites (Gebhardt-Henrich &
Richner 1998), selection will favour such compens-
atory strategies, provided that compensation is not, in
itself, too costly (Metcalfe & Monaghan 2001). Plasticity
in the development may lead to partial or full compensa-
tion, in particular for those body structures where
the long-term costs of suboptimal development are high.
Developmental plasticity as a response to food shortage
or low temperatures is well documented (reviewed in
Schew & Ricklefs 1998; Metcalfe & Monaghan 2001)
but poorly known as a response to parasites.
Two compensatory strategies can be used to face
poor growing conditions. First, after a period with harsh
conditions and poor growth, individuals may show
accelerated growth if condition improves (Fig. 1, curve
II). With parasites, this may occur if populations
fluctuate or if the initial host response is very costly.
Although the population dynamics of ectoparasites
has not attracted much attention, in some species an
increase in population size over the first half of the
host’s rearing period is followed by a decrease (e.g.
Summers 1975; Roulin 1998). Secondly, if the length of
the maturation is not fixed, parasitized individuals
can grow for a longer period of time to compensate for
the parasite-induced reduction in growth rate (Fig. 1,
curve III). The accelerated growth and delayed matura-
tion hypotheses can work in concert, as parasitized
nestlings may simultaneously alter their growth rate in
relation to parasitism and extend the growth period.
Developmental plasticity may therefore help parasitized
individuals to compensate for the effects of parasites
on their development and, as a consequence, to catch
up in size to reach the level of parasite-free individuals
(Fig. 1, curve I). In contrast, if organisms are unable to
perform developmental plasticity or show incomplete
compensatory growth, they will become permanently
stunted at a smaller final size (Fig. 1, curve IV; Richner
1989; Potti & Merino 1996).
The goal of the present study is to examine the effects
of the blood-sucking louse-flies Crataerina melbae on
nestling development in the Alpine swift Apus melba.
This non-passerine bird is suited to examine whether
nestlings alter their growth pattern adaptively in
response to varying levels of parasite infestation
because they reduce growth rate and delay fledging in
prolonged periods of food deprivation, indicating that
development is plastic (Koskimies 1950). When popu-
lations of parasites fluctuate we predict, under the
accelerated growth hypothesis, that experimentally
parasitized nestlings grow less rapidly at the peak of
parasite infestation but more rapidly once this peak has
passed, compared to deparasitized ones. Under the
delayed maturation hypothesis, we predict that experi-
mentally parasitized nestlings grow for a longer time
period. If these two mechanisms allow nestlings to
reduce the cost of parasitism, parasitized nestlings
should fledge with a similar size to deparasitized ones.
Materials and methods
 
The Alpine swift is a 90-g migrant insectivorous
apodiform bird that spends most of its life on the wing,
landing only for breeding purposes. It is socially
monogamous and reproduces in colonies of a few to
several hundred pairs located in holes of cliffs or tall
buildings. One clutch of one to four eggs (mean 2·6) is
produced per year, and both parents incubate for
approximately 20 days (Arn 1960). Offspring fledge at
an age of 5070 days (Arn 1960). Before fledging, nest-
lings lose about 4·5% of their body mass (Arn 1960). At
fledging, parental care ceases and young do not return
to the colony until the following year (P.B. personal
observation; see also Tarburton & Kaiser 2001 for the
common swift Apus apus L.). Body mass and wing/tail
shapes need, therefore, to be particularly fine-tuned
in swifts (Martins 1997). Alpine swifts are sexually
mature in the second or third year, and the oldest
recorded individual was 26 years old (Arn 1960).
Alpine swifts are parasitized by a 7-mm-long blood-
sucking louse-fly C. melbae (Diptera, Hippoboscidae)
that feeds exclusively on this species (Tella et al. 1998).
Larvae develop in the maternal abdomen (viviparity)
until the prepupae stage, when they are released into
the surroundings of the nests and pupate immediately
(Bequaert 1953). Adult parasites emerge slightly before
their nestling hosts hatch. C. melbae is flightless and
can switch hosts rapidly by walking (P.B. personal
Fig. 1. Growth curves of parasitized (II–IV) and parasite-
free (I) individuals. The growth curve I represents the optimal
development of an individual facing no parasites, where A
and M are the optimum asymptotic size and age at maturity.
Although parasites can reduce the growth of their hosts,
parasitized individuals may compensate for their slower
growth by accelerating their development once the population
of parasites decreases (II) or by taking longer (M) to reach
final size (III). If the development of organisms is not plastic,
parasitized individuals become permanently stunted at a
smaller final size (A; IV).
2

observation). Several Hippoboscidae have been shown
to transmit blood parasites to their host (Baker 1967),
but to date this hypothesis has not yet received support
for C. melbae (Tella et al. 1995; P.B. personal observation).
   
Fieldwork was carried out between May and August in
1999, 2000 and 2001 in a Swiss Alpine swift colony
located under the roof of an old building in Solothurn
(47°12 N, 7°32 E) holding about 50 breeding pairs.
At the beginning of each breeding season nests were
visited every other day to determine the date of clutch
completion, and daily around hatching to determine
the hatching date of the first egg (day 0).
To create two groups of nests differing in ectopara-
site load, we transferred ectoparasites from a donor
brood (referred to as ‘deparasitized brood’) to a re-
ceiver brood (‘parasitized brood’). For this purpose,
nests with a similar clutch size (Pearsons correlation,
r = 0·39, N = 50, P = 0·005), hatching date (r = 0·95,
N = 50, P < 0·001), brood size at 10 days after hatching
(r = 0·57, N = 50, P < 0·001) and ectoparasite load at
10 days after hatching (r = 0·45, N = 50, P = 0·001)
were matched in 11, 20 and 19 pairs of nests in 1999,
2000 and 2001, respectively. Manipulations of louse-fly
load started 10 days after hatching because ectopara-
sites are rarely found on offspring before this age
(Roulin et al. 2003). As C. melbae is highly mobile
and deparasitized nests were re-infested frequently by
ectoparasites, we transferred ectoparasites every 5 days
until nestlings were 50 days old. For each pair of nests
we extracted and counted ectoparasites on all nestlings,
and then put all ectoparasites into the parasitized nest
of its pair. At the start of the experiment there were no
differences between treatments in clutch size, hatching
date or brood size and ectoparasite load 10 days
after hatching (all comparisons P > 0·43). Although
we added parasites to nests already infested naturally,
the number of louse-flies per parasitized nestling
remained within the natural range of infestation, as
observed in other Swiss colonies (Roulin et al. 1998;
P. B. personal observation). At each manipulation,
nestling wing length and body mass were measured to
the nearest millimetre and 0·1 g, respectively. After
20 days of age, Alpine swift nestlings start to invade
neighbouring families and are frequently adopted by
foster families (Arn 1960; Bize, Roulin & Richner 2003).
To prevent adoption, we checked all nests daily be-
tween 20 and 50 days after hatching, and returned each
nest-switcher immediately to its natal nest (Bize et al.
2003). Shortly before fledging, nests were visited daily
and nestlings measured as described above. We did
not assess the growth of tarsus in relation to the mani-
pulation of ectoparasite load because, in this species
with very short tarsi (mean 17·6 mm), the tarsus has
already reached its final length at the time when we
started to manipulate ectoparasite load (P.B. personal
observation).

To avoid pseudo-replication the breeding pair was used
as the unit of analysis, and hence if a pair was recorded
in more than one year we included only its first breed-
ing attempt. This restriction reduced our sample to 78
experimental broods (38 of 50 parasitized and 40 of 50
deparasitized broods). For the same reason, statistical
tests were carried out on mean sibling values rather
than on individual nestlings. Only nestlings that
survived up to fledging were included in the analyses.
The number (x) of louse-flies found on nestlings was
log
10
(x + 1) transformed before analyses to fit a normal
distribution. Growth rates (R) of wing length (W)
and body mass (M) between interval t and t + i were
calculated with the formulae: R
W
= (W
t + i
– W
t
)/i, and
R
M
= (M
t + i
– M
t
)/i. Growth rates of wing and body
mass were calculated for intervals between days 10 and
20, 20 and 30, 30 and 40, 40 and 50, and 50 and fledg-
ing. Body condition at fledging was calculated as the
residuals from a linear regression of body mass on wing
length. The effect of experimental manipulation on para-
sites load was analysed using repeated-measures 
with mean number of parasites per nestling and per nest
at 10, 20, 30, 40 and 50 days after hatching as repeats.
Effect of parasite manipulation on growth rate was
analysed using repeated-measures  with wing
growth rate on day intervals 1020, 2030, 3040,
4050 and 50–fledging as repeats. The same procedure
was applied to growth rate of body mass. Mean values
are given ±1 SE, statistical tests are two-tailed and
P-values smaller than 0·05 are considered significant.
Results
   
  
Although parasite prevalence was 100% in both treat-
ments, the experimental manipulation of parasite load
significantly affected mean parasite intensity over the
period of 1050 days after hatching with 7 ± 1 louse-
flies per nestling in deparasitized nests vs. 17 ± 1 per
nestling in parasitized ones (repeated-measures 
with log-transformed louse-fly load on days 10, 20, 30,
40 and 50 as repeats; treatment as factor: F
1,64
= 44·35,
P < 0·0001; Fig. 2). The number of louse-flies per
nestling varied significantly over the rearing period
with a peak of infestation at day 30 (age as factor:
F
4,61
= 74·80, P < 0·0001; Fig. 2). The treatment by
age interaction was also significant (F
4,61
= 12·59,
P < 0·0001), indicating a treatment effect on age-related
dynamics of parasite infestation (Fig. 2).
   
 
Complete brood failure tended to be more frequent
in parasitized than deparasitized broods (eight of 38
3

parasitized broods vs. three of 40 deparasitized broods
failed, 21·1 vs. 7·5%; Fisher’s exact test: d.f. = 1, P = 0·11).
Among successful breeders, brood size at fledging was
not significantly different between the two treatments
(parasitized broods: 1·87 ± 0·12 nestlings at fledging,
N = 30; deparasitized broods: 2·11 ± 0·11, N = 37;
Wilcoxons two-samples test: Z = 1·40, P = 0·16).
    

As expected from the accelerated growth hypothesis,
before the peak of parasite infestation wing growth rate
was lower in parasitized nestlings than deparasitized
ones, but higher thereafter (repeated-measures 
with wing growth rate on day intervals 1020, 2030,
3040, 4050 and 50–fledging as repeats; treatment by
age interaction: F
4,56
= 2·88, P = 0·031, Figs 3a and 4).
Overall, there was no significant difference in wing
growth rate between parasitized and deparasitized
nestlings (treatment as factor: F
1,59
= 1·84, P = 0·18,
Fig. 3a), and in the two treatments wing growth rate
slowed down when wings approached final size (age
as factor: F
4,56
= 175·67, P < 0·0001, Fig. 3a). Growth
rate of body mass did not differ between parasitized
and deparasitized nestlings (repeated-measures 
with growth rate of body mass on day intervals 1020,
2030, 3040, 4050 and 50–fledging as repeats; treat-
ment as factor: F
1,59
= 0·20, P = 0·66; treatment by
age interaction: F
4,56
= 0·81, P = 0·52, Fig. 3b). Growth
rate slowed down until the age of 50 days, followed by
a typical body mass recession (age factor: F
4,56
= 161·73,
P < 0·0001, Fig. 3b).
In agreement with the delayed-maturation hypo-
thesis, parasitized nestlings fledged 3 days later than depara-
sitized ones (Table 1). At the age of 50 days, wings
of parasitized nestlings were significantly shorter
(parasitized nestlings: 200·3 ± 1·9 mm, N = 29 broods;
deparasitized nestlings: 207·8 ± 1·7 mm, N = 37 broods;
Student’s t-test: t = 3·00, P = 0·0038). Combined with
the fact that parasitized nestlings grew their wings at a
faster rate at the end of the rearing period, the longer
time period spent in the nest allowed parasitized nest-
lings to fledge with wing lengths similar to depara-
sitized ones (Table 1). Body mass and body condition at
fledging were similar in parasitized and deparasitized
young (Table 1).
Discussion
Adaptive developmental plasticity is the process by
which an organism alters its growth and maturation to
counter the impact of detrimental rearing conditions
(Schew & Ricklefs 1998). Previous studies found that
parasites reduce body size or body condition of their
hosts (e.g. Richner et al. 1993), and some studies also
Fig. 2. Mean number of louse-flies per parasitized (solid
bars) and deparasitized (open bars) Alpine swift nestlings in
relation to age. Bars represent one standard error.
Fig. 3. Mean growth rate of (a) wing length and (b) body mass of parasitized (hatched bars) and deparasitized (open bars) Alpine
swift nestlings in relation to age. Fledging took place on average at 61 and 58 days after hatching in parasitized and deparasitized
nestlings, respectively. Bars represent one standard error.
(a)
4

reported an increase in the wing growth rate of experi-
mentally parasitized hosts (Saino, Calza & Møller 1998;
Szép & Møller 1999). To our knowledge the present
experimental study is the first to investigate develop-
mental plasticity in relation to the intranest population
dynamics of parasites. We showed that wing growth
rate of parasitized hosts decelerated during the peak
infestation and accelerated thereafter. Parasitized nest-
lings were also found to fledge later but at a similar size
to deparasitized ones. These findings support the
hypothesis that developmental plasticity is not only a
strategy to compensate the impact of temporary poor
feeding conditions or low ambient temperatures, but
also to compensate the effect of parasitism. As devel-
opmental plasticity occurs in nestlings of many species,
such as aerial insectivorous birds (Emlen et al. 1991),
seabirds (Boersma 1986), ducks (Street 1978) and
ptarmigans (Morse & Vohra 1971; Turner & Lilburn
1992), adaptive parasite-induced developmental plasticity
might have been overlooked.
   
The accelerated growth hypothesis predicts that
parasitized nestlings may show reduced growth until
the peak parasite infestation, and accelerated growth
once the conditions improve. Under this scenario,
parasitized hosts adaptively allocate more resources
into physiological processes associated with body
maintenance and parasite resistance during periods of
heavy infestation while favouring physiological processes
associated with growth during less stressful periods. In
line with the accelerated growth hypothesis, parasitized
nestlings grew their wings at slower rates than depara-
sitized nestlings during the first half of the growing
period (i.e. up to peak infestation), and at faster rates
thereafter (i.e. once infestation levels decreased). This
suggests that, as in the barn swallow Hirundo rustica L.
(Saino et al. 1998) and the sand martin Riparia riparia
L. (Szép & Møller 1999), where parasitized young grew
wings at a faster rate than deparasitized ones, wing
growth rate is adjusted adaptively to the level of para-
sitism in the Alpine swift. With respect to growth rate
of body mass, we did not find similar effects of para-
sitism. This may reflect a hierarchy of tissue preservation,
with fat reserves having priority over flight feather
growth. In other words, nestlings cannot afford to
reduce their mass growth because of the high risk of
starvation in case of an upcoming food shortage.
Indeed, Alpine swifts prey solely on aerial insects,
and this food resource shows large and unpredictable
variations over the breeding season. An alternative
explanation is that body mass growth reflects mainly
parental quality (Bize, Roulin & Richner 2002), thereby
masking any weak parasite-induced offspring adjust-
ment of resource allocation between body mass growth
and other functions.
   
The delayed maturation hypothesis states that para-
sitized nestlings can compensate for an initial poor
growth by taking longer to complete development and
maturation. In addition, given that nestling swifts do
not receive parental care and do not roost in the colony
after their first flight (Tarburton & Kaiser 2001; P.B.
personal observation), they should not fledge prema-
turely and should wait until optimal body mass and
shape are reached. Accordingly, our study shows that
the nestling period of parasitized young was prolonged
by 3 days in comparison to deparasitized ones, which
allowed parasitized offspring to fledge with a similar
body mass and wing length. Recaptures of eight depar-
asitized nestlings and four parasitized ones in the sub-
sequent year indicates that their growth was probably
completed at fledging, as there was no significant
Fig. 4. Age-related wing growth rate of parasitized Alpine
swift nestlings (closed symbols) in relation to deparasitized
ones (open symbols). The arrow signals the peak of parasite
infestation.
Table 1. Effects of experimental manipulations of ectoparasite load on fledging age, wing length, body mass and condition
Variable
Parasitized broods Deparasitized broods Student’s t-tests
Mean SE N Mean SE N t-value P-value
Fledging age (day) 61·3 0·9 27 58·1 0·8 36 2·66 0·009*
Fledging wing length (mm) 220·2 0·8 27 221·5 0·7 36 1·22 0·23
Fledging body mass (g) 90·2 1·5 27 91·3 1·3 36 0·54 0·59
Fledging condition (g mm
1
) 0·7 1·5 27 0·1 1·3 36 0·37 0·71
*Also significant after Bonferroni correction for multiple testing.
5

Citations
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Journal ArticleDOI
TL;DR: Evidence suggests that flexibility in immune responses becomes constrained with age through accumulation of memory cells at the expense of naive cells, decreased function of cells involved in adaptive and innate immunity, and programming of HPA-immune interactions.
Abstract: Summary 1. Life history theory predicts that immunity should be plastic and reflect environmental contexts. However, individual variation in immune investment may arise not just because of individual adjustment, but because of developmental, physiological, genetic or immunological constraints which lead to non-adaptive responses by limiting or eliminating flexibility in immune investment. Constraints can arise because organisms are single integrated units with interconnected and interacting components, in which physiological and genetic control mechanisms may limit or constrain immunity. We review some of the key underlying genetic and physiological factors that may constrain the occurrence and intensity of immune responses. 2. A major part of individual variability may rest on variation in genetic background. Genetic-based constraints can limit or influence immune responses, particularly through pleiotropy and epistatic interactions. In addition, genetic variation, an important driver of variation in antigen recognition and immune system polarization, can be constrained through linkage disequilibrium and genetic drift. Epigenetic changes can also constrain or limit immune responses in future generations based on individual experience. 3. The immune system itself can influence individual flexibility in immune investment. Throughout development individuals face tradeoffs within the immune system that favour the expression of one trait at the expense of another. Ontogenetic differences can cause juveniles and adults to produce entirely different immune responses to the same pathogen. T-helper 1 (Th1)/T-helper 1 (Th2) polarization during infection also imposes constraints upon an individual’s immune responsiveness, with the consequence that hosts cannot simultaneously mount strong responses using both Th1 and Th2 cells. In addition, evidence suggests that flexibility in immune responses becomes constrained with age through accumulation of memory cells at the expense of naive cells, decreased function of cells involved in adaptive and innate immunity, and programming of HPA-immune interactions. 4. In summary, selection on a particular immune trait can have effects on other immune components or phenotypic characters, as revealed by artificial selection studies. In particular selection for increased investment in compartments of the immune system leads to decreased investment in other competing life history functions and/or marked changes in other immune components. The role of past experience, even the past experience of parents, may limit and constrain immune responses through influencing the ontogeny of immunity, as well as through epigenetic influences.

109 citations

Journal ArticleDOI
TL;DR: This is the first field experiment demonstrating structural compensatory growth and associated costs in a wild animal population and is consistent with hypothesis 3.
Abstract: Although laboratory and observational studies suggest that many animals are capable of compensatory growth after periods of food shortage, few field experiments have demonstrated structural growth compensation in the wild. Here, we addressed the hypotheses that (i) food restriction can induce structural compensatory growth in free-living animals, (ii) that compensation is proportional to the level of body size retardation and (iii) that compensation induces mortality costs. To test these, wild brown trout (Salmo trutta) yearlings were brought to the lab, tagged individually, subjected to four levels of food deprivation (including a control), released back into the native stream and recaptured after one, five and ten months. Brown trout fully restored condition and partially restored mass within a month, whereas compensation in structure (i.e. body length) was not evident until after five months, supporting hypothesis 1. As the level of growth compensation was similar among the three deprived groups, hypothesis 2 was not supported. A final recapture after winter revealed delayed mortality, apparently induced by the compensatory response in the deprived groups, which is consistent with hypothesis 3. To our knowledge, this is the first field experiment demonstrating structural compensatory growth and associated costs in a wild animal population.

107 citations


Cites background from "Parasitism and developmental plasti..."

  • ...Chicks of the lesser black-backed gulls Larus fuscus restored wing length when feeding conditions were experimentally improved (Royle 2000), as did nestlings of the Alpine swift Apus melba after reduction of the parasite load (Bize et al. 2003)....

    [...]

  • ...Also bird nestlings appear to give priority to structural compensation (Nilsson & Svensson 1996; Royle 2000; Bize et al. 2003)....

    [...]

Journal ArticleDOI
TL;DR: It is recommended that studies aiming to assess parasite impacts on body condition should consider host-parasite biology, choose condition measures that can change during the course of infection, and employ longitudinal surveys or manipulate infection status when feasible.
Abstract: Body condition metrics are widely used to infer animal health and to assess costs of parasite infection. Since parasites harm their hosts, ecologists might expect negative relationships between infection and condition in wildlife, but this assumption is challenged by studies showing positive or null condition-infection relationships. Here, we outline common condition metrics used by ecologists in studies of parasitism, and consider mechanisms that cause negative, positive, and null condition-infection relationships in wildlife systems. We then perform a meta-analysis of 553 condition-infection relationships from 187 peer-reviewed studies of animal hosts, analysing observational and experimental records separately, and noting whether authors measured binary infection status or intensity. Our analysis finds substantial heterogeneity in the strength and direction of condition-infection relationships, a small, negative average effect size that is stronger in experimental studies, and evidence for publication bias towards negative relationships. The strongest predictors of variation in study outcomes are host thermoregulation and the methods used to evaluate body condition. We recommend that studies aiming to assess parasite impacts on body condition should consider host-parasite biology, choose condition measures that can change during the course of infection, and employ longitudinal surveys or manipulate infection status when feasible.

102 citations

Journal ArticleDOI
TL;DR: Interactions between parental melanism and offspring growth rate indicate that individuals display substantial plasticity in response to the rearing environment which is associated with the degree of melanism: at least with respect to nestling growth, phaeomelanic and eumelanic individuals are best adapted to rich and poor environments, respectively.
Abstract: One hypothesis for the maintenance of genetic variation states that alternative genotypes are adapted to different environmental conditions (i.e., genotype-by-environment interaction G×E) that vary in space and time. Although G×E has been demonstrated for morphological traits, little evidence has been given whether these G×E are associated with traits used as signal in mate choice. In three wild bird species, we investigated whether the degree of melanin-based coloration, a heritable trait, covaries with nestling growth rate in rich and poor environments. Variation in the degree of reddish-brown phaeomelanism is pronounced in the barn owl (Tyto alba) and tawny owl (Strix aluco), and variation in black eumelanism in the barn owl and Alpine swift (Apus melba). Melanin-based coloration has been shown to be a criterion in mate choice in the barn owl. We cross-fostered hatchlings to test whether nestlings sired by parents displaying melanin-based colorations to different extent exhibit alternative growth trajectories when raised by foster parents in poor (experimentally enlarged broods) and rich (experimentally reduced broods) environments. With respect to phaeomelanism, barn owl and tawny owl offspring sired by redder parents grew more rapidly in body mass only in experimentally reduced broods. With respect to eumelanism, Alpine swift offspring of darker fathers grew their wings more rapidly only in experimentally enlarged broods, a difference that was not detected in reduced broods. These interactions between parental melanism and offspring growth rate indicate that individuals display substantial plasticity in response to the rearing environment which is associated with the degree of melanism: at least with respect to nestling growth, phaeomelanic and eumelanic individuals are best adapted to rich and poor environments, respectively. It now remains to be investigated why eumelanism and phaeomelanism have a different signaling function and what the lifelong consequences of these melanism-dependent allocation strategies are. This is important to fully appraise the role played by environmental heterogeneity in maintaining variation in the degree of melanin-based coloration.

94 citations


Cites background from "Parasitism and developmental plasti..."

  • ...In swifts, cross-fostered nestlings sired by blacker fathers grew longer wings only when brood size was experimentally enlarged; wing length is a key trait in this species, as it determines age at fledging (an important fitness component in this species) and birds are foraging on their wings (Bize et al. 2003)....

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  • ...…nestlings sired by blacker fathers grew longer wings only when brood size was experimentally enlarged; wing length is a key trait in this species, as it determines age at fledging (an important fitness component in this species) and birds are foraging on their wings (Bize et al. 2003)....

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Journal ArticleDOI
TL;DR: Investigating blood meal size and survival of the ectoparasitic louse fly Crataerina melbae in relation to body condition and cutaneous immune response of their Alpine swift (Apus melba) nestling hosts highlights the fact that giving host immunocompetence primary consideration can result in a biased appraisal of host‐parasite interactions.
Abstract: Numerous host qualities can modulate parasite fitness, and among these, host nutritive resources and immunity are of prime importance. Indeed, parasite fitness increases with the amount of nutritive resources extracted from the host body and decreases with host immune response. To maximize fitness, parasites have therefore to balance these two host components. Yet, because host nutritive resources and immunity both increase with host body condition, it is unclear whether parasites perform better on hosts in prime, intermediate, or poor condition. We investigated blood meal size and survival of the ectoparasitic louse fly Crataerina melbae in relation to body condition and cutaneous immune response of their Alpine swift (Apus melba) nestling hosts. Louse flies took a smaller blood meal and lived a shorter period of time when feeding on nestlings that were experimentally food deprived or had their cutaneous immune response boosted with methionine. Consistent with these results, louse fly survival was the highest when feeding on nonexperimental nestlings in intermediate body condition. Our findings emphasize that although hosts in poor condition had a reduced immunocompetence, parasites may have avoided them because individuals in poor condition did not provide adequate resources. These findings highlight the fact that giving host immunocompetence primary consideration can result in a biased appraisal of host-parasite interactions.

91 citations

References
More filters
Journal ArticleDOI
TL;DR: It is suggested that, although compensatory growth can bring quick benefits, it is also associated with a surprising variety of costs that are often not evident until much later in adult life.
Abstract: Nutritional conditions during key periods of development, when the architecture and modus operandi of the body become established, are of profound importance in determining the subsequent life-history trajectory of an organism. If developing individuals experience a period of nutritional deficit, they can subsequently show accelerated growth should conditions improve, apparently compensating for the initial setback. However, recent research suggests that, although compensatory growth can bring quick benefits, it is also associated with a surprising variety of costs that are often not evident until much later in adult life. Clearly, the nature of these costs, the timescale over which they are incurred and the mechanisms underlying them will play a crucial role in determining compensatory strategies. Nonetheless, such effects remain poorly understood and largely neglected by ecologists and evolutionary biologists.

1,784 citations


"Parasitism and developmental plasti..." refers background in this paper

  • ...Developmental plasticity as a response to food shortage or low temperatures is well documented (reviewed in Schew & Ricklefs 1998; Metcalfe & Monaghan 2001) but poorly known as a response to parasites....

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  • ...Given the potentially long-term fitness consequences of poor early growth caused by parasites (Gebhardt-Henrich & Richner 1998), selection will favour such compensatory strategies, provided that compensation is not, in itself, too costly ( Metcalfe & Monaghan 2001 )....

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  • ...Adaptive compensatory growth and delayed fledging may carry significant costs for nestlings and their parents, although such costs are as yet poorly documented, and also supposed to occur later in life ( Metcalfe & Monaghan 2001 )....

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  • ...Given the potentially long-term fitness consequences of poor early growth caused by parasites (Gebhardt-Henrich & Richner 1998), selection will favour such compensatory strategies, provided that compensation is not, in itself, too costly (Metcalfe & Monaghan 2001)....

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  • ...Adaptive compensatory growth and delayed fledging may carry significant costs for nestlings and their parents, although such costs are as yet poorly documented, and also supposed to occur later in life (Metcalfe & Monaghan 2001)....

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Book
01 Jan 1980
TL;DR: In this paper, Peter Price integrates the biological attributes that characterize parasites ranging from such diverse groups as viruses, bacteria, protozoa, and fungi, to helminths, mites, insects, and parasitic flowering plants.
Abstract: In spite of the fact that parasites represent more than half of all living species of plants and animals, their role in the evolution of life on earth has been substantially underestimated. Here, for the first time within an evolutionary and ecological framework, Peter Price integrates the biological attributes that characterize parasites ranging from such diverse groups as viruses, bacteria, protozoa, and fungi, to helminths, mites, insects, and parasitic flowering plants. Synthesizing systematics, ecology, behavioral biology, genetics, and biogeography, the author outlines the success of parasitism as a mode of life, the common features of the wide range of organisms that adopt such a way of life, the reasons for parasites' extraordinary potential for continued adaptive radiation, and their role in molding community structure by means of their impact on the evolution of host species. In demonstrating the importance of parasitic interactions for determining population patterns and geographical distributions, Dr. Price generates further discussion and suggests new areas for research.

1,235 citations

Journal ArticleDOI
TL;DR: A trade-off between quality and number of offspring is feasible only in the absence of the parasitic hen flea, and in parasite-free broods fitness can potentially be gained through offspring quality or number or both, whereas in infested broods it can be gain through offspring quantity only.
Abstract: 1. The effect of a haematophageous ectoparasite, the hen flea, on quality an number of offspring was experimentally investigated in the great tit. The experiment consisted of a controlled infestation of a random sample of nests with the parasitic flea and of a regular treatment of control nests with Microwaves in order to eliminate the naturally occurring fleas. 2. To assess the effects of fleas on variables related to offspring number, we considered the number of hatchlings and fledglings, the mortality between hatching and fledging, and the hatching and fledging success. For assessment of offspring quality, we measured body mass, tarsus and wing length, and calculated the nutritional condition of, nestlings as the ratio of body mass to tarsus length. A physiological variable, the haematocrit level, was also measured. 3. Hatching success and hatchling numbers did not differ between the two experimental groups. Offspring mortality between hatching and fledging was significantly higher in the infested broods (xBAR = 0.22 chicks dead per day) than in the parasite-free broods (xBAR = 0.07 dead per day). Fledging success was 83% in the parasite-free broods, but only 53% in the infested ones. The number of fledglings in infested broods (xBAR = 3.7 fledglings +/-2.1 SD) was significantly lower than in the parasite-free (xBAR = 4.9 +/- 1.1 SD) broods. 4. Body mass of chicks in the infested broods was significantly smaller than in the parasite-free broods both 14 days and 17 days after hatching. The chicks in the infested broods reached a significantly smaller tarsus length than the ones in the parasite-free broods. Close to fledging, the nutritional condition of chicks was significantly lower in infested broods. Haematocrit levels were significantly lower in the infested broods. 5. Brood size correlated differently with body mass and condition of chicks in infested and parasite-free nests. In parasite-free broods both body mass and condition of chicks at age 17 days, i.e. close to fledging, were significantly higher in small broods than in large ones. However, in the infested broods chicks were of the same body mass and condition in large as in small broods. Therefore, in parasite-free broods fitness can potentially be gained through offspring quality or number or both, whereas in infested broods it can be gained through offspring quantity only. In other words, a trade-off between quality and number of offspring is feasible only in the absence of the parasitic hen flea. 6. These results emphasize the need to study the effects of ectoparasites on ecological, behavioural and evolutionary traits of their bird hosts. A knowledge of these effects is essential for the understanding of population dynamics, behaviour and life-history traits of the hosts.

317 citations

Journal ArticleDOI
TL;DR: In this paper, the authors showed that decreasing the daylength of moulting in European starlings reduced the duration of moult from 103 +/- 4 days to 73 +/- 3 days (p < 0.0001).
Abstract: Life-history theory proposes that costs must be associated with reproduction. Many direct costs are incurred during breeding. There is also evidence for indirect costs, incurred after breeding, which decrease survival and future reproductive success. One possible indirect cost identified in birds is that breeding activity in some way compromises plumage quality in the subsequent moult. Here we propose a mechanism by which this could occur. Breeding activity delays the start of moult. Birds that start to moult later also moult more rapidly--an effect of decreasing daylength. Could this result in poorer quality plumage? We kept two groups of male European starlings, Sturnus vulgaris, one on constant long days and the other on decreasing daylengths from the start of moult. Decreasing daylengths reduced the duration of moult from 103 +/- 4 days to 73 +/- 3 days (p < 0.0001). Newly grown primary feathers of birds that moulted fast were slightly shorter, weighed less (p < 0.05) and were more asymmetrical. They had a thinner rachis (p < 0.005), were less hard (p < 0.01) and less rigid (p < 0.05). They were also less resistant to wear so that differences in mass and asymmetry increased with time. There was no difference in Young's modulus. Poorer quality plumage will lead to decreased survival due to decreased flight performance and increased thermoregulatory costs. Thus, reproduction incurs costs through a mechanism that operates after the end of breeding.

307 citations


"Parasitism and developmental plasti..." refers background in this paper

  • ...For instance, in parasitized offspring fast growth of flight feathers might reduce the quality of their wings (Dawson et al. 2000), and profoundly penalize juveniles on the wing and during long-distant migration....

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Journal ArticleDOI
01 Dec 1990-Ecology
TL;DR: Barn Swallows regularly reuse old nests, but avoid old nests with mites as demonstrated by experimental manipulation of mite loads, suggesting that new nests are not primarily infected from old nests harboring large mite populations.
Abstract: I studied the effect of the parasitic haematophagous tropical fowl mite (Or- nithonyssus bursa, Macronyssidae, Gamasida) on the reproduction of the Barn Swallow (Hirundo rustica, Hirundinidae, Passeriformes). Barn Swallows regularly reuse old nests, but avoid old nests with mites as demonstrated by experimental manipulation of mite loads. An equally large proportion of nests was infected with mites in experimental colonies, where all old Barn Swallow nests were removed, as in control colonies without such removal. Furthermore, the estimated number of mites per nest did not differ between experimental colonies, where all old nests were removed, and control colonies. These results suggest that new nests are not primarily infected from old nests harboring large mite populations. Mite population density per nest after fledging was significantly positively related to mite pop- ulation density on adult Barn Swallows upon arrival at the breeding site in early spring the same year. Mate choice may significantly affect levels of ectoparasitism, if parasite loads of nests originate from inoculates provided by adult Barn Swallows. In order to mimic the effects of choice of a mate with few or many mites, respectively, I manipulated mite loads of newly built first clutch nests during the egg-laying period of Barn Swallows by either spraying nests with a pyrethrin solution or introducing an inoculate of 50 mites, or nests were simply kept as controls. Addition of mites to nests decreased reproductive success of the birds measured in terms of number of independent fledglings of first clutches and in terms of clutch size, brood size, and number of independent fledglings of second clutches. Barn Swallow nestlings in nests with mites had lower body mass but similar body size compared with nestlings in sprayed nests. Incubation periods were longer and nestling periods shorter for nests with added mites. Interclutch intervals were significantly shorter in the group of sprayed nests, mainly because more such nests were reused for second clutches and because adult swallows suffered less from mite infestations. Slightly fewer Barn Swallows had second clutches during the same breeding season if their nests held many mites. Fitness of adult Barn Swallows is thus directly related to their own mite infection level and that of their mate.

242 citations


"Parasitism and developmental plasti..." refers background in this paper

  • ...…et al. © 2003 British Ecological Society, Journal of Animal Ecology , 72 , 633–639 is usually based on experiments where parasite load is manipulated early during host development and the effect measured close to the end (e.g. Møller 1990; Richner, Oppliger & Christe 1993; Clayton & Tompkins 1995)....

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Q1. What are the future works in this paper?

Therefore, future studies on host–parasite relationships should consider parasite fluctuations and assess the effects of parasites at different stages in host development.