J Ornithol (2008) 149:193–197
DOI 10.1007/s10336-007-0259-5
ORIGINAL ARTICLE
Blow fly Trypocalliphora braueri parasitism on Meadow Pipit
and Bluethroat nestlings in Central Europe
Václav Pavel Æ Bohumı́r Chutný Æ Tereza Petrusková Æ
Adam Petrusek
Received: 4 April 2007 / Revised: 30 September 2007 / Accepted: 8 November 2007 / Published online: 2 December 2007
Ó Dt. Ornithologen-Gesellschaft e.V. 2007
Abstract The larvae of blow fly (Trypocalliphora braueri) are known to cause a subcutaneous myiasis in bird
nestlings mainly in Nearctic species, while only a few
records are available from the Palaearctic. Here, we report
on infestations of this insect ectoparasite in two passerine
species, Meadow Pipit (Anthus pratensis) and Bluethroat
(Luscinia svecica), breeding in the Central European
mountain range Krkonoše. The infestation of T. braueri
parasite was relatively low in studied bird species (3.0% of
infested nests in Meadow Pipit and 4.2% in Bluethroat) but
varied strongly between years (0–33% of infested nests/
year/species). The presence of the parasitic blow fly larvae
was apparently controlled by temperature; they were found
only during warm summers. The combination of parasite
infection and heavy rainfalls in a critical period significantly reduced nestling survival.
Keywords Trypocalliphora braueri Blow fly Meadow pipit Bluethroat Nestling survival
Communicated by F. Bairlein.
V. Pavel (&)
Laboratory of Ornithology, Palacký University in Olomouc,
tř. Svobody 26, 77146 Olomouc, Czech Republic
e-mail: [email protected]
B. Chutný
Malinová 27, 10600 Prague 10, Czech Republic
T. Petrusková A. Petrusek
Department of Ecology, Faculty of Science,
Charles University in Prague, Prague, Czech Republic
Introduction
Nestlings of many bird species have been reported to be
parasitised by obligate hematophagous larvae of bird blow
flies of closely related genera Protocalliphora and Trypocalliphora. Larvae of most blow flies are intermittent
ectoparasites that live in nesting material and only feed
(suck the blood) of the nestlings. Trypocalliphora braueri
(Hendel 1901; syn. Protocalliphora braueri) is unusual, as
its larvae burrow into the skin of the bird nestlings, causing
a subcutaneous myiasis that persists throughout the larval
stage. The larvae mature, leave the hosts before the nestlings fledge, and pupate in the nest substrate to complete
the blow fly life cycle (Sabrosky et al. 1989; Howe 1992).
T. braueri is well known in the Nearctic region, parasitising a variety of North American bird species (e.g.
Garrison et al. 1986; Sabrosky et al. 1989; Howe 1991,
1992; Warren 1994). However, there are only limited
records of T. braueri infesting Palearctic bird species. The
species was first described in the literature from the western Palaearctic by Rognes (1985). The most complete data
on the presence of T. braueri in Europe exist from
Fennoscandia (Rognes 1991), but occasional records have
also been reported from Ukraine and Russia as well as from
several Central European countries, including Austria,
Czech Republic, Slovakia, Germany, Hungary, Poland and
Switzerland (Rognes 2004). Records from more southerly
latitudes are missing, with the exception of Corsica
(Rognes 2004) and a recent find in Italy (Raffone 2006).
Host range of T. braueri in Fennoscandia includes over
ten ground- and hole-nesting passerine species, including
the Meadow Pipit (Anthus pratensis) and the Bluethroat
(Luscinia svecica) (Rognes 1991; Åkesson et al. 2002). In
Central Russia, the parasite was found in nests of 14 species of passerines breeding on or close to the ground
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(Gaponov and Truchanova 1995). Krištı́n and Exnerová
(1994) described a lethal infestation by blow fly larvae
(misidentified as Ornithomyia sp.) causing a subcutaneous
myiasis in the nestlings of Tree Pipits (Anthus trivialis)
breeding in a mountain locality in Slovakia.
In this study, we report on the infestation of T. braueri
larvae on the nestlings of two passerine species breeding in
mountain habitats in Central Europe. During our study of
reproductive behaviour of Meadow Pipits and Bluethroats,
we collected detailed information about the prevalence and
intensity of parasitism of T. braueri, and we analysed the
effect of environmental conditions on the occurrence of
parasitism and the effect of parasites on host nestlings.
Methods
Our study was conducted on Meadow Pipits and Bluethroats breeding in the Krkonoše Mountains (= Giant
Mountains, Czech Republic; 50°44–470 N, 15°32–430 E;
1,320–1,450 m above sea level) between 2001 and 2007.
Both studied species are altricial ground-nesting passerines
of body weight ca. 18–19 g. In the Krkonoše Mountains,
they breed on alpine meadows with peat bogs partially
covered by scrub (Pinus mugo, Picea abies, Sorbus aucuparia, Salix sp.); the Meadow Pipit is the most abundant
bird species breeding there (with a density approx. 1 pair/
ha). Both species incubate eggs for 13–14 days and the
hatched chicks fledge after 10–14 days. Fledglings are
cared for and fed by both parents for 1–2 weeks (Hötker
and Sudfeldt 1982; Cramp 1988; own unpublished data).
From mid-May to end-July, as a part of larger study, we
followed the basic breeding biology of both species. We
located nests and checked them every 2–3 days until the
nesting attempt finished. After the nestlings had reached
8–10 days of age, they were ringed and carefully checked
for ectoparasites. The larvae of T. braueri are visible on the
parasitised nestlings only for 3–5 days (Howe 1992;
Eastman et al. 1989); this corresponds to the nestling age of
8–10(12) days. When we found blow fly larvae burrowed
into the subcutaneous tissues of the nestlings (myiases), we
waited until the nestlings reached the age of 10 days (larvae matured and our manipulation did not bias the survival
of nestlings). Afterwards, we counted the larvae, recorded
their locations on the nestling bodies and collected some
larvae from infested nestlings. To facilitate identification,
larvae were reared to adults in a screen-covered plastic
container filled with cotton wool.
During June and July, when nestlings of studied bird
species were present in the nests, meteorological conditions
(air temperature and precipitation) were measured on the
study plots. Mean daily air temperature and sum of daily
precipitation was compared between years using analysis
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J Ornithol (2008) 149:193–197
of variance. Survival of nestlings (proportions of fledglings
to hatchlings) in infested and uninfested nests, in which the
nestlings reached the age of 8 days and were not predated
until fledging, was compared using the logistic regression
model (PROC GENMOD; SAS Institute 2000). All tests
were two-tailed.
Results
In total, 234 nests of Meadow Pipits and 71 nests of
Bluethroats were checked in the Krkonoše Mountains
between 2001 and 2007 after the nestlings reached 8 days
of age. We found only a single ectoparasitic insect species
living in the nests of the studied bird species; the parasitic
larvae of T. braueri were found in seven nests of Meadow
Pipit (3.0%) and in three nests of Bluethroat (4.2%;
Table 1). T. braueri larvae were found in the years 2002,
2003, 2006 and 2007, but not in 2001, 2004 and 2005. The
years with T. braueri occurrence were characterised by
elevated mean daily temperatures during the nesting season
(June and July; Fig. 1a), with afternoon temperatures frequently exceeding 18°C.
The larvae parasitising on the nestlings were found
burrowed mainly in the subcutaneous tissues on the head,
neck, wings and flanks; the parasitised young had perforations of the skin on the infested areas. All nestlings in
infested nests were parasitised (28 nestlings of Meadow
Pipit, 11 nestlings of Bluethroat), the numbers of larvae per
nestling varied between 5 and 22 (nnestlings = 34, mean ±
SE = 9.15 ± 0.75). The age of nestlings when parasitic
larvae were registered was 7–11 days (nnests = 9, median = 10 days). All infestations occurred between 18 June
Table 1 The numbers of nests of Meadow pipit (Anthus pratensis)
and Bluethroat (Luscinia svecica) that were checked after the nestlings reached 8 days of age (including the nests predated before
fledging) and numbers of nests infested by larvae of Trypocalliphora
braueri
Year
Meadow pipit
(Anthus pratensis)
Nests
checked
Infested
Bluethroat
(Luscinia svecica)
(%)
Nests
checked
Infested
(%)
2001
25
0
0
12
0
0
2002
43
3
7.0
13
1
7.7
2003
44
2
4.5
9
0
0
2004
59
0
0
14
0
0
2005
25
0
0
7
0
0
2006
19
2
10.5
10
0
0
2007
19
0
0
6
2
33.3
234
7
3.0
71
3
4.2
2001–2007
J Ornithol (2008) 149:193–197
Fig. 1 a Comparisons of temperature and precipitation in the
Krkonoše Mountains (1,400 m a.s.l.) in the nesting seasons 2001–
2007. Mean daily temperature and sum of daily precipitation for June
and July are presented (mean ± SE). Both temperature (ANOVA:
F = 7.09; df = 6; P \ 0.001) and precipitation (F = 3.72; df = 6;
P = 0.001) showed significant differences between years. b Survival
of nestlings (proportions of fledglings to hatchlings; least square
means ± 95% confidence limits) in the studied Meadow Pipit (Anthus
pratensis) nests (uninfested nests in 2001–2007 are shown separately
and the nests infested by T. braueri in 2002, 2003 and 2006 are
pooled). Numbers of nests are indicated below the error bars. Only
the nests potentially influenced by T. braueri infestation—those
where the nestlings reached 8 days of age (critical nesting period)—
and were not predated until fledging were included in the analysis.
and 23 July (dated for the infested nestling’s age 10 days),
late nests were more affected by the parasite than early
nests (the mean hatching date in infested nests was higher
than in uninfested nests in the infestation years 2002, 2003,
2006: 23 June vs. 13 June; Mann–Whitney U test:
ninfested = 7, nuninfested = 96, exact P = 0.05).
Survival of Meadow Pipit nestlings (proportion of
fledglings to hatchlings) was negatively influenced by
infestation of T. braueri and significantly differed between
years. During the infestation years (2002, 2003 and 2006),
it was significantly reduced in the nests parasitised by
larvae of T. braueri (Logistic regression: infestation
F1,99 = 7.54, P = 0.007; year F2,99 = 5.01, P = 0.009;
Fig. 1b). The nestling survival in infested Meadow Pipit
nests was further negatively influenced by weather conditions (in particular, by high precipitation) during the
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Fig. 2 The relationships between survival of nestlings (proportions
of fledglings to hatchlings) in infested nests of the Meadow Pipit and
weather conditions during the days when the nestlings mature
(average daily temperature and sum of daily precipitation during the
days 8–10 of the nestling’s age). The dashed lines represent logistic
regression, points represent infested nest.
critical nestling period, i.e., the days when the nestlings
mature and simultaneously the developed larvae have the
highest detrimental influence (logistic regressions of nestling survival versus average daily temperature and sum of
daily precipitation during the days 8–10 of the nestlings
age; temperature F1,5 = 0.08; P = 0.79; precipitation
F1,5 = 6.69; P = 0.049; Fig. 2). In contrast, the weather
conditions did not seem to markedly influence survival of
Meadow Pipit nestlings in uninfested nests during the
critical nesting phase; the survival of nestlings, although
significantly differing between years (Logistic regression:
year F6,215 = 3.94, P \ 0.001), did not correspond to more
severe weather conditions (Fig. 1a, b), This suggests that
the separated effect of the weather had only a minimal
influence on nestling survival during this critical phase.
Survival of Bluethroat nestlings was also negatively
influenced by the T. braueri infestation: nestlings from two
of the three parasitised nests (7 out of 11 parasitised nestlings recorded) did not survive the combination of
infestation and heavy rainfalls. Due to small sample size,
however, we analysed in detail only the influence of
infestation on survival of Meadow Pipit nestlings.
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Discussion
Our results suggest that the overall infestation rate of
T. braueri larvae on Meadow Pipit and Bluethroat nestlings
is low in the Krkonoše Mountains and that the infestation
occurs only during warm summers. These findings correspond to the results of other studies describing natural
history of this parasitic blow fly and its hosts (Eastman
et al. 1989; Howe 1992; Gaponov and Truchanova 1995).
Studies of natural populations of T. braueri indicated
that densities of this blow fly are usually too small to
seriously reduce the host bird populations (they usually
parasitise less than 3% of nests in most bird species;
Whitworth and Bennett 1992; Warren 1994; Gold and
Dahlstein 1983). However, there are also studies describing
relatively high infestation rates (up to 39% of nests; e.g.
Eastman et al. 1989; Gaponov and Truchanova 1995;
Åkesson et al. 2002), which may have a detrimental effect
on the hosts.
Important factors that might influence abundance of this
insect ectoparasite are environmental conditions, especially
the temperature (e.g. Merino and Potti 1996). Temperature
has been shown to have a critical influence on the activity,
growth and development of insect ectoparasites, especially
in species which do not live permanently on their hosts
(Marshall 1981; Merino and Potti 1996). Females of parasitic T. braueri overwinter as imagines and lay their eggs
in nests of bird host species. Blow fly adults start activity at
the threshold temperature of 15.5°C and reach full flight
capability at 17.5°C (Gold and Dahlsten 1989; Bennett and
Whitworth 1991). The parasitic T. braueri larvae were
found in the Krkonoše Mountains only in warmer years
when June and July afternoon temperatures frequently
exceeded 18°C. The severe mountain climate with variable
temperature conditions may therefore explain both the
overall low infestation rate of T. braueri in the studied area
and its between-year variation.
It has been shown that ectoparasites in bird nests may
have detrimental effects on parasitised nestlings. The
infestation by blow fly larvae causes loss of blood and
anaemia in nestlings (Johnson and Albrecht 1993; O’Brien
et al. 2001), with deleterious effect on their mass (Simon
et al. 2003), immunity, and health (Howe 1992; Warren
1994; O’Brien et al. 2001). Parents might compensate the
negative effect of parasites by increasing their feeding rates
(Hurtrez-Boussès et al. 1998), but this strategy is unsuccessful when the effect of ectoparasites is combined with
other negative effects, such as adverse weather conditions
(de Lope et al. 1993; Merino and Potti 1996).
Our results showed that the survival of Meadow Pipit
nestlings in the Krkonoše Mountains was reduced in the
nests infested by larvae of T. braueri. The prevalence of the
parasite and its negative influence on the nestlings was
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J Ornithol (2008) 149:193–197
more evident during the years when warm periods
(important in the life cycle of parasite) were combined with
high precipitation during the days of nestling maturation
(in rainy periods, nestlings weakened by infestation may
die due to secondary infections or exhaustion). The finding
that T. braueri infestation affects the nesting success of the
studied species in Central European alpine habitats during
warmer seasons is especially relevant in the view of
potential future climate changes, either towards warming or
more continental climate.
Zusammenfassung
Parasitismus der Schmeißfliege Trypocalliphora braueri
bei Nestlingen von Wiesenpieper und Blaukehlchen in
Zentraleuropa
Es ist bekannt, dass die Larven der Schmeißfliege Trypocalliphora braueri subkutane Myiasis bei Nestlingen
vorwiegend nearktischer Vogelarten verursachen, während
es nur wenige Nachweise aus der Paläarktis gibt. Hier
berichten wir über den Befall mit diesem ektoparasitischen
Insekt bei zwei Sperlingsvogelarten, dem Wiesenpieper
Anthus pratensis und dem Blaukehlchen Luscinia svecica,
die im zentraleuropäischen Gebirgszug Krkonoše brüten.
Der Befall mit T. braueri-Parasiten war bei den untersuchten Vogelarten relativ niedrig (3% infizierter Nester
beim Wiesenpieper und 4.2% beim Blaukehlchen), variierte
jedoch stark zwischen Untersuchungsjahren (0–33%
infizierter Nester pro Jahr pro Art). Die Anwesenheit
parasitischer Schmeißfliegenlarven wurde offensichtlich
über die Temperatur kontrolliert; sie wurden lediglich in
warmen Sommern gefunden. Die Kombination von Parasitenbefall und starken Regenfällen während eines kritischen
Zeitraums führte zu einer signifikanten Reduktion im
Überleben der Nestlinge.
Acknowledgments We are very grateful to Správa KRNAP, Lučnı́
Bouda and Labská Bouda for their help in arranging our stay in the
Krkonoše Mountains. We thank Petr Kovařı́k and Aleš Svoboda for
assistance in the field, Jan Vaněk, Dalibor Povolný and František
Gregor for help with identification of blow fly larvae, and Arild
Johnsen, Tomáš Koutný, Karel Weidinger, and two anonymous
reviewers for helpful comments on the manuscript. This work was
supported by grants from the Czech Science Foundation (GAČR 206/
02/P074) and the Czech Ministry of Education (MSM6198959212
and MSM0021620828), and complies with all the current laws of the
Czech Republic.
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