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B I O L O G I CA L C O N S E RVAT I O N
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Short communication
Effects of the introduced parasite Philornis downsi
on nestling growth and mortality in the medium
ground finch (Geospiza fortis)
Sarah K. Huber*
Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts, 319 Morrill Science Center,
Amherst, MA 01003, USA
A R T I C L E I N F O
A B S T R A C T
Article history:
Invasive species have the potential to detrimentally affect native ecosystems by out com-
Received 27 May 2007
peting or directly preying upon native organisms, and have been implicated in the extinc-
Received in revised form
tion of endemic populations. One potentially devastating introduced species in the
13 November 2007
Galápagos Islands is the parasitic fly Philornis downsi. As larvae, P. downsi parasitize nestling
Accepted 25 November 2007
birds and have been associated with high nestling mortality and reduced growth rates.
Available online 31 January 2008
Here I document nestling growth and mortality in a bimodal population of the medium
Keywords:
iable ecological conditions. Annual parasite prevalence in nests ranged from 64% to 98%,
Darwin’s finches
and nestling mortality in nests with parasites ranged from 16% to 37%. Parasite load and
Muscidae
parasite load per nestling follow a skewed distribution with many nests having relatively
Ectoparasite
few parasites, and few nest having many. Parasite load, however, was not correlated with
Nestling mortality
onset of breeding, clutch size, the number of nestlings, nestling survival or fledgling suc-
Growth rate
cess. Parasite load per nestling, on the other hand, was correlated with clutch initiation
Galápagos Islands
date and the proportion of nestlings that died in parasitized nests. Neither nestling size
ground finch, Geospiza fortis. Observations were conducted over three years, and under var-
nor growth rate differed between parasitized and unparasitized nests. In addition, male
and female beak morphology was not correlated with parasite load, breeding variables or
nestling survival. Thus, while overall mortality due to parasitism is high, ecological conditions and possible host defenses may potentially counter some of the detrimental affects of
P. downsi on nestling size and growth. These results taken together suggest that parasitism
of P. downsi larvae on nestling G. fortis has the potential to lead to large population declines.
Ó 2007 Elsevier Ltd. All rights reserved.
1.
Introduction
The ecological and evolutionary impacts of invasive species
on native organisms has been a major emphasis of recent research in conservation biology (Sakai et al., 2001; Mooney and
Cleland, 2001; Snyder and Evans, 2006; Strayer et al., 2006;
Weinig et al., 2007). Invasive species often out-compete or
prey on native species, and have been implicated in extinctions of native organisms (Warner, 1968; Van Riper et al.,
1986, 2002; Vitousek et al., 1987; Mack et al., 2000). Island
* Present address: Department of Biology, University of Utah, 257 South 1400 East Salt Lake City, UT 84112, USA. Tel.: +1 413 695 7069.
E-mail address: [email protected].
0006-3207/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2007.11.012
602
B I O L O G I C A L C O N S E RVAT I O N
biotas are thought to be particularly vulnerable to the negative impacts of invasive species, in part, because island habitats have lower species diversity, with fewer niches exploited
by native fauna, and they tend to support small population
sizes of endemic organisms (Diamond, 1984; Dobson and
McCallum, 1997; Dobson and Foufopoulos, 2001; Altizer
et al., 2001; Vitousek, 2002).
The Galápagos Islands of Ecuador have served as an excellent model system for the study of ecology and evolution
(Grant, 1999; Wikelski, 2005; Arbogast et al., 2006). However,
an increasing number of invasive species are threatening native biotas (Wikelski et al., 2004; Causton et al., 2006; Parker
et al., 2006), with a recent count estimating the number of
exotic species to be over 800 (Bensted-Smith et al., 2000).
One potentially devastating invasive species is the fly Philornis
downsi, which in the larval stage is a hematophagous parasite
of nestling birds. In 1964 several specimens of P. downsi were
collected in the Galápagos Islands (Causton et al., 2006). Additional collections were made in 1981; however, the presence
of P. downsi went relatively unnoticed until 1997, when larvae
were discovered in the nests of land birds (Fessl et al., 2001).
To date, P. downsi has been found to parasitize at least 12 bird
species in the Galápagos Islands (Fessl and Tebbich, 2002),
and has been recorded from 13 to 15 major islands (Wiedenfeld et al., 2007). Philornis downsi has been implicated in the
decline of populations of the mangrove finch, Cactospiza heliobates, and the warbler finch, Certhidea olivacea (Dvorak et al.,
2004; Grant et al., 2005).
Flies of the genus Philornis are common throughout the
Neotropics (Dodge, 1955, 1963, 1968; Dodge and Aitkin, 1968;
Couri, 1984, 1986). Females presumably lay their eggs directly
on nestlings (Meinert, 1890; Dodge, 1971; Arendt, 1985), and
larvae feed on the blood and fluid of nestlings. The early instars will often burrow in the nostrils of nestlings, causing
long term morphological damage (Fessl et al., 2006a). Later instars live in the nesting material and surface at night to feed
on nestlings. Philornis downsi parasitism has been correlated
with a reduction in nestling survival in several species of Darwin 0 s finches, including the woodpecker finch (Cactospiza pallida), small tree finch (Camarhynchus parvulus), warbler finch (C.
olivacea), small ground finch (Geospiza fuliginosa), and medium
ground finch (Geospiza fortis) (Fessl and Tebbich, 2002; Fessl
et al., 2006b). Parasitism by P. downsi also has been found to
impact negatively nestling growth rates in a combined analysis of small ground finches and medium ground finches (Fessl
et al., 2006b), and result in reduced hemoglobin and immature
red blood cell counts in the small ground finch (Dudaniec
et al., 2006).
This study documents the impacts of P. downsi parasitism
on nestling survival and growth in the medium ground finch,
G. fortis, at El Garrapatero, Santa Cruz Island, Galápagos
(Fig. 1). Interestingly, the population of G. fortis at El Garrapatero is bimodal with respect to beak morphology, with birds
falling mainly into large and small beak size classes with relatively few intermediates (Hendry et al., 2006; Huber and Podos, 2006). As in other populations of G. fortis (Grant and
Grant, 2006; Grant, 1999; Price, 1987; Keller et al., 2001), beak
size variation likely has a strong additive genetic basis and reflects selection imposed by variation in the size and hardness
of seeds. The bimodality is likely due to specialization by the
1 4 1 ( 2 0 0 8 ) 6 0 1 –6 0 9
A
91°
90°
Pinta
Marchena
0°
50 km
Genovesa
0°
Santiago
Santa
Cruz
Fernandina
Isabela
1°
San Cristobal 1°
Floreana
Espanola
91°
90°
B
El Garrapatero
Academy
Bay
10 km
Fig. 1 – (A) Map of Galápagos Islands. Field work was
conducted at (B) El Garrapatero, Santa Cruz Island.
two morphs on different food types, perhaps coupled with intra- or inter-specific competition. Indeed, intermediate birds
survive at lower rates between years in comparison to large
and small morphs (A.P. Hendry et al., unpublished data). In
addition to determining the effects of P. downsi parasitism
on nestling growth and mortality, I will test whether beak size
confers a selective advantage with respect to parasitism.
2.
Materials and methods
2.1.
Parasite prevalence and nestling mortality
Research was conducted at El Garrapatero, Isla Santa Cruz,
Galápagos, Ecuador (Fig. 1, GPS coordinates S 00°40 0 20 0 0 –
41 0 20 0 0 ; W 90°13 0 10 0 0 –14 0 40 0 0 ). Nests of G. fortis were observed
from January to April 2004, January to May 2005, and January
to March 2006. The average monthly rainfall during these
periods was collected by weather stations at the Charles Darwin Research Station in Academy Bay (Fig. 1).
In 2004, the fate of each nest was recorded as ‘‘successful’’
(nestlings fledged) or ‘‘failed’’ (nestlings were predated or
found dead in the nest). No data was collected on rates of predation or parasitism; however, dead nestlings were examined
for P. downsi larvae and the presence of lesions associated
with larval feeding.
In 2005, nests were located, and checked every 3–4 days
during the breeding season. During each nest check the
B I O L O G I C A L C O N S E RVAT I O N
number of eggs or nestlings was recorded, and nestlings were
inspected for external signs of parasites (e.g., lesions on the
body). A decrease in the number of eggs or nestlings from
one visit to the next was presumed to be the result of predation. Predators of Darwin 0 s finches include mockingbirds,
owls, and in some cases rats (Grant, 1999). There is no evidence to suggest that eggs are ejected by Darwin 0 s finch
adults or nestlings, and visual inspection of the ground under
predated nests in this study failed to recover any eggs. When
nests were no longer active (e.g., due to predation, the death
of nestlings, or fledging), nests were collected and the number
of P. downsi larvae and pupae per nest were recorded. Because
larvae feed at night, it was not possible to determine the
number of parasites infecting a given nestling within a nest.
Therefore, to determine parasite load per nestling, I divided
the total number of parasites by the number of nestlings in
the nest. In summary, I recorded for each nest: clutch initiation date, clutch size, the number of eggs predated, the number of nestlings predated, the number of nestlings dead in the
nest, the number of nestlings fledged, the parasite load, and
the parasite load per nestling.
In 2006, nests were checked every other day and the number of eggs and nestlings recorded. Birds were again examined
for the presence of lesions associated with P. downsi larval
feeding. I recorded for each nest: clutch initiation date, clutch
size, the number of eggs predated, the number of nestlings
predated, the number of nestlings dead in the nest, the number of nestlings fledged, and whether parasites were present
or absent. The number of nests with P. downsi larvae was recorded, but the number of larvae per nest (parasite load)
was not determined.
Observations of nestling survival were terminated prior to
the end of the breeding season in 2005 and 2006. At the end of
the observation period in 2005, the fate of 12 nestlings from
four nests was unknown. At the end of the observation period
in 2006, the fate of 10 nestlings from five nests was unknown.
These 22 nestlings were removed from further analyses.
2.2.
Nestling size and growth rate
Data on nestling size and growth rate was collected in 2006
only. Individual nestlings within a nest were marked with a
unique colored plastic leg band, or by coloring a toenail with
non-toxic paint. Nestlings were measured every other day,
and measurements included: mass, tarsus, gape, beak length,
beak width, and beak depth.
For measures of both size and growth rate the mean value
of nestlings within a nest was used for statistical analysis.
This is because siblings are genetically similar, and thus statistically non-independent. The mean size of nestlings within
a nest was determines for each day post hatching (1 day old,
2 days old, etc.). Nestlings hatch asynchronously, and so measurements were collected at days one, three, five, etc., for
some nestlings within a nest, and days two, four, six, etc.,
for other nestlings within the same nest. Because nestling
mortality was high, in some nests only a single nestling was
measured at given age.
The size of parasitized nestlings at each age was then plotted against the size of unparasitized nestlings of the same age
for all morphological variables. To determine the size and
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603
growth trajectories of nestlings from parasitized to unparasitized nests, I used reduced major axis regression (RMA). A RMA
that results in a regression line with a slope of one would indicate that size at a given age is not statistically different between parasitized and unparasitized nestlings.
Growth rates were determined for individual nestlings by
calculating the average change in a variable per day. Growth
rates were then averaged across all nestlings in a nest. Due
to high nestling mortality, growth rates could be calculated
for two unparasitized nests and seven parasitized nests. A
Kruskal–Wallis test was used to compare median growth
rates between parasitized and unparasitized nests for each
variable.
2.3.
Adult beak morphology
Adult birds were captured in mist nets and banded with unique combinations of one metal and three color bands. The
following measurements were taken from each bird, as in
Grant et al. (1985): beak length, beak depth, and beak width.
The first axis of a principle component analysis (PC1) that included beak length, beak depth, and beak width was used in
future analyses of adult beak morphology. Birds were classified into three beak sizes classes (small, intermediate, and
large) based on an hierarchical cluster analysis of PC1 (for
methods see Huber et al. (2007)). A v-square test was used
to determine if the beak size of breeding birds was representative of the population as a whole.
To test for the influence of parental beak morphology on
nestling mortality and parasite loads I correlated male and female beak PC1 scores from 2005 with clutch initiation date,
clutch size, number of nestlings, number of dead nestlings
in nests with parasites, proportion of dead nestlings in nests
with parasites, number of nestlings fledged, proportion of
nestlings fledged, parasite load, and parasite load per nestling. Male and female beak PC1 scores from 2006 were correlated with clutch initiation date, clutch size, and number of
nestlings. Sample sizes were too low in 2006 to correlate beak
morphology with the number of dead nestlings in nests with
parasites (n = 3 nests), the proportion of dead nestlings in
nests with parasites (n = 3 nests), the number of nestlings
fledged (n = 1 nest), or the proportion of nestlings fledged
(n = 1 nest). In 2006, parasite load was not determined. Rather,
the presence or absence of parasites was assessed. A logistic
regression was used to determine if beak morphology was a
predictor of parasite presence or absence.
The collection of data in this study was done in concordance with animal use protocols approved by the University
of Massachusetts Amherst.
3.
Results
3.1.
Parasitism and nestling mortality
High nestling mortality occurred in all three years of this
study. In 2004, 100% of nests failed: all nestlings were predated or were found dead in the nest. Dead nestlings had lesions indicative of larval feeding by P. downsi, and larvae or
pupae were found in the nesting material of all nests with
dead nestlings. In 2005, nestling mortality associated with
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B I O L O G I C A L C O N S E RVAT I O N
parasitism was high, though not as high as predation rates,
and larvae and pupae of P. downsi were found in all nests that
contained dead nestlings (Table 1). Larvae were frequently
found feeding inside the head and body cavity of dead nestlings. In 2006, fewer nestlings died in nests with parasites
(Table 1). However, many nestlings that were ultimately predated also showed signs of P. downsi parasitism (e.g., lesions
on body and/or larvae and pupae in empty nest).
Parasite load per nest follows a skewed distribution, common in many parasite systems (Fig. 2a), even when standardized for the number of nestlings per nest (Fig. 2b). However,
parasite load was not a significant predictor of any breeding
variables, nestling mortality, or fledging (Table 2). Parasite
load per nestling was significantly correlated with clutch initiation date (Table 2). Nests earlier in the breeding season had
significantly more parasites per nestling than did nests later
in the breeding season. This is likely because clutch initiation
date has a significant, positive relationship with clutch size
(F = 39.66, R = 0.76, p < 0.001); clutch sizes were higher later
in the breeding season. Parasite load per nestling also was significantly correlated with the proportion of nestlings in a nest
that died; nests with a higher number of parasites per nestling had a larger proportion of nestlings die (Table 2).
Table 1 – Summary of parasite prevalence and nestling
mortality in G. fortis
Number of nests
Number of nests with nestlings
Number of nests with parasites
Number of nestlings
Number nestlings predated
Number dead nestlings in
nests with parasites
Number fledged
2005
2006
47
44 of 45 (98%)
129
71 (55%)
48 (37%)
16
9 of 14 (64%)
32
25 (78%)
5 (16%)
10 (8%)
2 (6%)
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3.2.
Nestling size and growth rate
Nestlings from parasitized and unparasitized nests were
similar in size throughout the nestling period (Fig. 3). The results of a reduced major axis regression reveal no difference
in size between parasitized and unparasitized nestlings in
mass, tarsus, beak gape, beak length, or beak width (Table
3). In all cases, except beak depth, the 95% confidence intervals of the slopes include one. Beak depth is the only variable for which the 95% confidence intervals do not
encompass a slope of one. Young birds have similar beak
depths; however, as nestlings get older the beak depth of
unparasitized birds tends to be larger than that of unparasitized birds (Fig. 3).
Mean growth rates of nestlings in parasitized and unparasitized nests were not significantly different for any of the six
variables measured (Fig. 4; mass: v2 = 0.86, P = 0.77; tarsus:
v2 = 0.54, P = 0.46; gape: v2 = 0.78, P = 0.38; beak length:
v2 = 0.09, P = 0.77; beak depth: v2 = 0.78, P = 0.38; and bead
width: v2 = 0.10, P = 0.38).
3.3.
Ecological conditions and nestling mortality
In 2004, 100% of observed nestlings died, and this was one of
the driest breeding seasons on record (total rain January–
May = 51.1 mm). The early part of the breeding season in
2005 was also extremely dry. In February 0.2 mm of rain fell,
and only six pairs bred. Of those, four out of six nests produced nestlings. Heavy rains fell from March 9 to 15
(109.2 mm), with little to no rain falling after March 15. Very
little rain fell in April (0.8 mm). After the rains, breeding
was synchronous with two periods in which nestlings were
present in nests: March 27–April 16 and April 28–May 10.
In 2005, mortality in nests with parasites was highest in
February (86%: six out of seven nestlings), followed by the second cohort after the rain, April 28–May 10 (46%: 19 out of 41
nestlings). The first cohort of nestlings to hatch after the rain,
12
12
10
10
8
8
6
6
4
4
2
2
0
0
0
20 40 60 80 100 120 140 160 180 200
Parasite load
0
10
20
30
40
50
Parasite load per nestling
60
Fig. 2 – Frequency distribution of parasite loads in 2005. (A) Parasite load was determined for individuals nests. (B) Parasite
load was then standardized to the number of nestlings per nest.
B I O L O G I C A L C O N S E RVAT I O N
605
1 4 1 ( 2 0 0 8 ) 6 0 1 –6 0 9
Table 2 – Results of a Pearson correlation of parasite load and parasite load per nestling with breeding variables, nestling
mortality, and fledging success (N = number of nests)
Parasite load
N
Clutch initiation date
Clutch size
Number of nestlings
Number of dead nestlings in nests with parasites
Proportion of dead nestlings in nests with parasites
Number of nestlings fledged
Proportion of nestlings fledged
R
32
32
32
19
19
5
5
Parasite load per nestling
p
0.12
0.55
0.88
0.10
0.13
0.61
0.61
0.28
0.11
0.03
0.39
0.36
0.31
0.31
R
p
0.37
0.34
0.33
0.06
0.56
0.58
0.58
0.04
0.06
0.06
0.81
0.01
0.30
0.30
20
16
14
12
10
8
6
4
2
0
18
Tarsus (mm)
Mass (g)
Values in bold are statistically significant.
16
14
12
10
8
6
6
0 2 4 6 8 10 12 14 16
Mass (g)
Beak length (mm)
9
8
7
6
6
5
4
3
2
6
7
8
9
10
Gape (mm)
11
2
3
4
5
6
Beak length (mm)
7
8
Beak width (mm)
7
Beak depth (mm)
10 12 14 16 18 20
Tarsus (mm)
7
10
Gape (mm)
PARASITIZED NESTS
11
8
6
5
4
3
7
6
5
4
3
3
4
5
6
Beak depth (mm)
7
3
4
5
6
7
Beak width (mm)
UNPARASITIZED NESTS
8
Fig. 3 – Size of parasitized and unparasitized nestlings at days 1–8 and day 11. The dashed line has an intercept through the
origin and a slope of one. Points falling on this line indicate that the size of parasitized and unparasitized nestlings is equal.
from March 27 to April 16, had the lowest nestling mortality
(29%: 23 out of 81 nestlings). Fledglings were recorded only
from this cohort (12%: 10 out of 81 nestlings fledged). How-
ever, when observations came to an end in May, 12 nestlings
were still alive. The fate of these nestling is unknown,
although all had visual signs of parasites.
606
B I O L O G I C A L C O N S E RVAT I O N
Table 3 – Results of a reduced major axis regression of
size variables for parasitized and unparasitized nestlings
Intercept
Mass
Tarsus
Gape
Beak length
Beak depth
Beak width
1.12
0.76
0.52
0.16
0.92
0.38
(3.45,
(3.52,
(2.98,
(1.05,
(1.82,
(2.17,
1.20)
1.99)
1.93)
0.73)
0.01)
1.41)
1.32
1.12
1.05
1.07
1.26
1.12
Slope
R2
(1.00,
(0.91,
(0.79,
(0.88,
(1.06,
(0.79,
0.93
0.95
0.92
0.96
0.97
0.89
1.64)
1.33)
1.31)
1.27)
1.46)
1.44)
The 95% confidence intervals are reported in parentheses.
1.8
No parasites (n = 2 nests)
Parasites (n = 7 nests)
Growth Rate (change per day)
1.6
1.4
1.2
1.0
0.8
0.6
0.4
0.2
0.0
Mass (g) Tarsus Gape
(mm) (mm)
Beak
length
(mm)
Beak
depth
(mm)
Beak
width
(mm)
Fig. 4 – Mean nestling growth rate (calculated as the mean
change in a variable per day) between parasitized and
unparasitized G. fortis nests. Differences are not statistically
significant.
3.4.
Beak morphology and nestling mortality
Beak morphology was determined for males and females of
38 pairs in 2005 and 15 pairs in 2006. The distribution of beak
morphology of breeding adults was representative of the population as a whole (2005: v2 = 5.08, p = 0.08; 2006: v2 = 3.00,
p = 0.22). Beak morphology of males and females was not correlated with any breeding factors in 2005 and 2006 (Table 4), or
with nestling mortality and parasite load in 2005 (Table 4). In
2006, only three nests contained dead nestlings, precluding a
rigorous statistical test of the relationship between beak morphology and nestling mortality. Parasite prevalence, but not
load, was determined for nests in 2006. A logistic regression
found that beak morphology was not a significant predictor
of parasite prevalence (male beak PC1: N = 13 nests;
W = 1.42, p = 0.23 and female beak PC1: N = 13 nests;
W = 0.34, p = 0.56).
4.
Discussion
Nestling mortality in nests with P. downsi larvae was extremely high in G. fortis at El Garrapatero (Table 1). Parasite re-
1 4 1 ( 2 0 0 8 ) 6 0 1 –6 0 9
lated mortality, coupled with mortality due to predation,
resulted in only 12 fledglings out of 159 nestlings over a three
year period. While combined mortality was high in all years,
predation of nestlings was much higher in 2006 than in
2005, and nestling mortality in parasitized nests was lower
in 2006 than in 2005 (Table 1). However, many of the nestlings
that were predated in 2006 were also parasitized by P. downsi.
Had predation been lower, many of those nestlings would
likely have died due to parasite related causes.
Parasite load was variable across nests with many nests
having relatively few parasites and a few nests having many
parasites (Fig. 2). This distribution is a common feature of
many host-parasite systems (Anderson and Gordon, 1982).
Parasite load was not correlated with any aspects of host
breeding behavior or nestling mortality in this system (Table
2). However, when parasite load was calculated as a function
of the number of nestlings in the nest, it was correlated with
clutch initiation date (Table 2). This result suggests that birds
which breed first might be more vulnerable to parasitism than
later nesting birds, and stands in contrast to previous studies
of hematophagous parasites in other species of birds which
found no relationship between parasite load and date of
clutch initiation (Hurtrez-Bousses et al., 1999). Parasite load
per nestling was also correlated with the proportion of nestlings that died in a nest. These results together suggest that
selection should favor birds with larger clutch sizes, which
would effectively reduce the number of parasites per nestling
within the nest.
Nestling size and growth were not found to differ between
parasitized and unparasitized nests, a finding that stands in
contrast to previous studies of P. downsi parasitism of Darwin 0 s finches (Fessl et al., 2006b). The failure of this study to
detect differences between parasitized and unparasitized
nestlings may be due to small samples sizes, as few nests
were parasite free. However, variation in ecological conditions
might also explain these results. During the Fessl et al. (2006b)
study in 2004, very little rain fell, and Santa Cruz experienced
one of the most severe droughts in a 40 year period (Grant and
Grant, 2006). Starvation and malnourishment potentially contributed to decreased nestling growth rates in parasitized
nests. By contrast, late 2005 and 2006 were very wet years,
and food resources were abundant. The increased availability
and quality of food during these years might have off-set the
detrimental effects of parasitism to nestling growth. The 2005
breeding season provides some evidence that rainfall might
influence nestling condition. During the wettest part of 2005
(late-March to early-April) nestling mortality due to parasites
was the lowest (29%), and this was the only period of time in
which nestlings fledged.
The potential evolution of host defenses, such as increased adult provisioning, also may help to explain why
growth rates in this study differed from those of Fessl et al.
(2006b). Several studies documenting the impacts of hematophagous ectoparasites on nestling growth in other avianparasite systems have found no difference in size or growth
rates between parasitized and unparasitized nestlings (Johnson and Albrecht, 1993; Merino and Potti, 1995; Hurtrez-Boussès et al., 1997; Miller and Fair, 1997). One hypothesis for this
result is that adults adjust feeding rates when nestlings are
parasitized (Mason, 1944; Johnson and Albrecht, 1993). In
B I O L O G I C A L C O N S E RVAT I O N
607
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Table 4 – Pearson correlation coefficients for beak morphology and breeding variables, nestling mortality, and fledging
success for 2005 and 2006 (N = number of nests)
2005
N
Clutch initiation date
Clutch size
Number of nestlings
Number of dead nestlings in nests with parasites
Proportion of dead nestlings in nests with parasites
Number of nestlings fledged
Proportion of nestlings fledged
Parasite load
Parasite load per nestling
28
28
26
19
19
5
5
26
26
2006
Male beak PC1 Female beak PC1
0.01
0.15
0.30
0.29
0.36
0.68
0.68
0.002
0.21
0.06
0.05
0.22
0.13
0.03
0.59
0.59
0.17
0.34
N
23
21
15
–
–
–
–
–
–
Male beak PC1 Female beak PC1
0.18
0.06
0.02
–
–
–
–
–
–
0.21
0.09
0.18
–
–
–
–
–
–
No correlations were statistically significant (p > 0.05).
support of this hypothesis, adult provisioning has been found
to increase in nests of blue tits with hematophagous fly larvae
(Christe et al., 1996; Triplet and Richner, 1997; Hurtrez-Boussès et al., 1998; Banbura et al., 2004). There are currently no
data on feeding rates of adult Darwin 0 s finches with respect
to parasite load or ecological conditions.
Previous studies of beak morphology in this population
suggest that large and small morphs may have a fitness
advantage in comparison to birds with intermediate sized
beaks (Hendry et al. 2006; Huber et al. 2007; A.P. Hendry
et al., unpublished data). However, beak morphology was
unrelated to parasite load. Thus, it appears as though bill
morphology does not confer a fitness advantage with respect
to parasitism. Interestingly, parasitized nestlings had smaller
beak depths than unparasitized nestlings (Table 3, Fig. 3).
Selection acts on beak size and shape in response to food
availability and inter- and intra-specific competition (Boag
and Grant, 1981; Schluter et al., 1985; Grant and Grant,
2006), and beak morphology, in turn, correlates with bite force
(Herrel et al., 2005a,b) and acoustic features of songs (Podos,
2001; Huber and Podos, 2006). Thus, parasitized offspring
might have reduced fitness after reaching adulthood. In addition, parasitized birds have been found to have deformed
beaks as a result of larval feeding in the nasal cavity (Fessl
et al., 2006a). These results have interesting implications for
how heritability is measured in populations. Heritability estimates are calculated by comparing traits of adults to their offspring. Charmantier et al. (2004) found that nests containing
hematophagous fly larvae had decreased heritability estimates of morphological traits in comparison to nests without
larvae. Thus, knowledge about parasite prevalence is vital to
determining how trait variation is measured across generations in natural populations. The degree to which parasitized
nestlings differ from their parents with respect to beak morphology has implications for the stability of the bimodality
at El Garrapatero.
In conclusion, the relationship between Darwin 0 s finches,
P. downsi, and finch predators is dynamic. While overall mortality due to parasitism is high, ecological conditions and
possible host defenses might have the potential to counter
some of the detrimental affects of P. downsi on nestling size
and growth. The earliest record of P. downsi on the Galápagos
Islands is 1964, and collections made by Peck et al. on Santa
Cruz in 1989 contained specimens of P. downsi (Causton et al.,
2006). Assuming that P. downsi was present at El Garrapatero
during this period, Darwin 0 s finches may have begun to
evolve defenses against parasites in the 40 years ensuing
the introduction of P. downsi. Possible host defenses that
have not been tested in any population of Darwin 0 s finches
to date include increases in adult provisioning, nestling
behavior, and the evolution of a Philornis-specific immune
response.
No long term data exist that document interactions between Darwin 0 s finches and P. downsi in a single population,
and in general little is known about the natural history of P.
downsi (Dudaniec and Kleindorfer, 2006). Parasitism of P.
downsi larvae on nestling G. fortis has the potential to lead
to dramatic population declines of Darwin 0 s finches, not just
in this population, but through out the archipelago as a whole
(Wiedenfeld et al. 2007; Wikelski et al., 2004). Detailed, longterm research into the dynamics of host-parasite adaptation
and coevolution in Darwin 0 s finches is urgently needed.
Acknowledgements
I thank the Galápagos National Park and the Charles Darwin
Research Station for providing support for this research. Jeffrey Podos, Andrew Hendry, Anthony Herrel, Luis Fernando
de Leon, Bieke Vanhooydonk, Ana Gabela, Eric Hilton, Haldre
Rogers, Dan Buresh, and Steve Johnson provided assistance in
the field. Funding was provided by National Science Foundation Grant IBN 0347291 to Jeffrey Podos, National Science
Foundation Grant DDIG 0508730 to Jeffrey Podos and S.K.H.,
an American Ornithologists 0 Union Student Research Grant,
an Explorer 0 s Club grant, a Sigma Xi Grant-in-Aid of Research,
an Animal Behaviour Society Student Research grant, and a
University of Massachusetts Woods Hole Fellowship. Jeffrey
Podos, Andrew Hendry, Ethan Clotfelter, Elizabeth Jakob, Benjamin Normark, Dale Clayton and three anonymous reviewers provided comments on earlier drafts of this manuscript.
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