10.5061/DRYAD.GMSBCC2JS
Biagolini-Jr., Carlos
0000-0002-3699-3337
University of Brasília
Macedo, Regina H.
University of Brasília
Philornis parasitism: impact on nestlings and risk factors involved
Dryad
dataset
2020
Coordenação de Aperfeicoamento de Pessoal de Nível Superior
https://ror.org/00x0ma614
471945/2013-7
National Council for Scientific and Technological Development
https://ror.org/03swz6y49
1789/2015
Animal Behavior Society
https://ror.org/031nh9x49
2021-01-26T00:00:00Z
2021-01-26T00:00:00Z
en
https://doi.org/10.1111/jav.02592
69999 bytes
3
CC0 1.0 Universal (CC0 1.0) Public Domain Dedication
Parasitic botfly larvae (Philornis ssp., Diptera: Muscidae) are found in
nests of several bird taxa, although prevalence and nestling tolerance
vary considerably among species. Here we describe patterns of botfly
infestation in blue-black grassquit (Volatinia jacarina) nestlings. We
identified the most typically affected nestling body parts and assessed
parasite prevalence, impact on nestling survival, changes in nestling body
shape and mass index. Additionally, we tested whether climatic conditions,
nest morphology and habitat characteristics are associated with larvae
abundance. Blue-black grassquits had low breeding success (15%), but most
failures resulted from predation by vertebrate predators. We estimated
that only 1% of nestlings died due to botfly infestation, and the number
of larvae in nestling body did not affect nest success. Infected chicks
exhibited a higher body mass to tarsus length ratio, and higher tarsus
asymmetry. Previous studies indicate that adult grassquits with a higher
body mass index have lower dominance status and mating success. Thus, we
argue that although botflies had a small impact on offspring survival,
they may reduce fitness in adulthood. There was no evidence that
environmental conditions and nest morphology are linked to the number of
larvae on nestlings. Territories with higher food supply had lower
infestation rates. Possibly, food-rich habitats allow parents to invest
more time in offspring care (brooding nestlings), thus protecting them
from fly attacks. The present study brings to light new perspectives
concerning bird-botfly interaction
Study site and species This study was carried out within the University of
Brasília campus, in central Brazil (15°45'S; 47°52'W), in an
area of 20 ha. The vegetation is classified as Cerrado sensu stricto
(tropical savanna) with high plant diversity (Assunção and Felfili 2004,
Aguilar et al. 2008). We monitored breeding activities of blue-black
grassquits between November to April, across two breeding seasons
(2017-2018; 2018-2019). Throughout the breeding season, males blue-black
grassquits defend territories and attract mates by performing multimodal
displays (Manica et al. 2016, Manica et al. 2017). Both sexes build the
nest and provide parental care. The small cup-shaped nests are placed in
the forks of shrubs (more frequently) or in dense grass undergrowth
(Carvalho et al. 2007, Aguilar et al. 2008). Predation is considered the
main factor leading to lack of breeding success (Almeida and Macedo 2001,
Carvalho et al. 2007, Aguilar et al. 2008, Dias et al. 2010). Cheating
behaviors, such as extra pair paternity and intraspecific brood
parasitism, occur in blue-black grassquits (Carvalho et al. 2006, Manica
et al. 2016). Little is known about botfly infection in this species, but
literature reports indicate that they are infected by the subcutaneous P.
glaucinis and P. trinitensis (Teixeira 1999). Data collection We searched
for nests by slowly walking across the field site at least twice each
week, inspecting the vegetation and watching for birds carrying nesting
materials. New and active nests were checked at intervals of up to three
days, until chicks fledged or the nest was lost to predation. Incubation
and nestling periods lasted up to 10 days each (Carvalho et al. 2007). If
eggs were present in a nest on a given day and eggs hatched on the
following day, we assumed that hatching had occurred on the second day.
For chicks hatching after a checking interval of two-three days, or nests
found in the nestling period (20 of 180), we estimated hatching day by
comparisons with chicks of known age. The disappearance of eggs before
hatching or of nestlings before seven days of age, associated with a
damaged nest, was attributed to nest predation. Nestling death due to
botfly larvae infestation was assumed when nestlings were found dead in
the nest and larvae were found in the nest or nestling. Nest desertion was
assumed when parents no longer cared for the eggs, which remained in the
nest > 10 days. Whenever eggs were deserted, we collected and
opened them to check for development. After this inspection, eggs were
classified as “infertile” if no embryo was found, or “death in
development” if we found a dead embryo. Nest success was assumed when
nestlings disappeared from the nest at or later than 7 days post-hatch and
no signs of predation were detected (i.e. the nest remained intact in the
vegetation). Nestling body condition was recorded up to three times for
each nestling, and included mass (taken with a 10g, 0.1g resolution Pesola
spring scale), both left and right tarsus length (digital caliper Mitutoyo
500-196-30B, 0.01 mm resolution), and number of larvae and their location
on the nestling´s body (we did not identify larvae to the species level).
A body mass index was calculated by dividing nestling weight by average
tarsus length. In adult grassquits, it has been found that body mass index
correlates negatively with intestinal parasite load (Costa and Macedo
2005, Aguilar et al. 2008) and social dominance (Santos et al. 2009). Nest
body asymmetry was calculated based on the absolute difference between
left and right tarsus lengths. The location of larvae was mapped onto the
nestling´s body areas: head-neck, wings, legs, and main body (see figure
1); large larvae could occupy more than one area. We did not band
nestlings at the nest since this could influence natural predation rate by
increasing the contrast between nestlings and nest background material.
Climatic data were obtained from the open database provided by the
Brazilian meteorological institute (Instituto Nacional de Meteorologia -
INMET), which provided a regional sampling location less than 10 km from
the study site. For each nest, we averaged the daily rainfall and
temperature for a period encompassing 14 days, from seven days before and
after hatching. When nests were no longer active, they were collected for
measurements associated with their architecture, after which they were
deposited in the museum collection Coleção Ornitológica Marcelo Bagno, at
Universidade de Brasília. We used two variables to characterize nest
architecture: nest wall density and nest wall openness. Nest wall density
was calculated as the ratio of nest weight to wall volume (mg/mm3). Nest
weight was obtained with a high precision balance (Shimadzu BL320H, 1mg
resolution) after the nest was air dried at 75ºC for 24h. Nest wall volume
was estimated as the difference between external and internal nest wall
volumes. Volume was estimated using the semi-ellipsoid volume formula V =
2/3 × π × a × b × c, where a and b are perpendicular measurements of nest
outer/inner diameter and c is nest height/depth. Nest wall openness was
estimated as the average of four measurements of nest wall openness taken
on different sides of the nest. A detailed description of the method is
provided in Biagolini-Jr and Macedo (2019). In brief, photos of the nest
were taken with a white styrofoam ball (50mm in diameter) placed inside
the nest chamber. Then, with an image editor software (GIMP version 2.10)
we cropped the styrofoam ball image section and converted it to a black
and white scale. Using the R package bwimage (Biagolini-Jr 2019), we
estimated nest wall openness as the proportion of white pixels relative to
total number of image pixels. We assessed food availability and vegetation
density in five spots at distances of 3 m from the nest within two weeks
after nestlings fledged. We did not demarcate parental territories, but
assume that the sampled spots had a high probability of falling within
territories (Aguilar et al. 2008). We estimated the abundance of seed
resources by averaging the number of seed inflorescences counted in 50 x
50 cm grids placed at each of the five spots (Manica et al. 2014).
Vegetation density was estimated in five plots of 30x100 cm, by adapting
the Zehm et al. (2003) method. In summary, a photograph was taken of the
vegetation against a panel of 100 x100 cm white cloth placed
perpendicularly to the ground on the largest side of the plot. The
photograph was converted to a pure black and white image (GIMP version
2.10). Vegetation density was estimated as the proportion of black pixels
relative to total number of pixels (Biagolini-Jr and Macedo 2019). Host
nest density was estimated as the number of grassquit nests, within a
radius of 50 meters of the focal nest being considered, with clutches that
hatched in the period of 10 days before and after nest hatching date at
the focal nest. We chose this range because it encompasses both the
nestling period and the botfly pupation period from a possible previously
infected nest (Saravia-Pietropaolo et al. 2018). We used the R package
geosphere Version 1.5 (Hijmans et al. 2019) to calculate distances between
nests.