Negative effect of mite (Knemidokoptes) infection on reproductive output in an
African raptor
Author(s): Julia L. van Velden, Ann Koeslag, Odette Curtis, Tertius Gous, and Arjun Amar
Source: The Auk, 134(3):498-508.
Published By: American Ornithological Society
DOI: http://dx.doi.org/10.1642/AUK-16-134.1
URL: http://www.bioone.org/doi/full/10.1642/AUK-16-134.1
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Volume 134, 2017, pp. 498–508
DOI: 10.1642/AUK-16-134.1
RESEARCH ARTICLE
Negative effect of mite (Knemidokoptes) infection on reproductive output
in an African raptor
Julia L. van Velden,1* Ann Koeslag,1 Odette Curtis,2 Tertius Gous,3 and Arjun Amar1
1
FitzPatrick Institute of African Ornithology, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch, South Africa
Overberg Lowlands Conservation Trust, Napier, South Africa
3
Helderberg, South Africa
* Corresponding author: juliavanvelden@gmail.com
2
Submitted July 8, 2016; Accepted February 6, 2017; Published April 12, 2017
ABSTRACT
Knemidokoptes is a genus of subcutaneous mites found in the skin of multiple avian hosts, although few cases have
been reported in wild raptors. Population monitoring of Black Sparrowhawks (Accipiter melanoleucus) on the Cape
Peninsula, South Africa, between 2001 and 2012 revealed multiple birds with infection symptoms in some years.
Examination of 3 dead birds displaying symptoms such as baldness and skin lesions confirmed infection by
Knemidokoptes spp., whereas we found no cases of subclinical infection in birds without symptoms (n ¼ 16). Up to 5%
of birds in the population were infected in some years, which represents the first record of multiple birds displaying an
infection by Knemidokoptes in a wild population of raptors. A male bias in infection prevalence was detected.
Prevalence of infection symptoms was generally low in other populations elsewhere in South Africa, although possibly
higher in urban areas. Breeding performance (both productivity and nesting success) was significantly lower for
individuals following infection and also in comparison with noninfected birds throughout the study period. This is the
first study to demonstrate the negative effect that these mites may have on breeding performance in a wild bird
species, and our results suggest that this parasite could potentially influence population dynamics over time.
Keywords: Black Sparrowhawk, breeding performance, Knemidokoptes, nesting success, parasites, productivity
Effet négatif d’une acariase causée par Knemidokoptes sur l’efficacité de la reproduction d’un rapace
africain
RÉSUMÉ
Les acariens du genre Knemidokoptes sont des acariens sous-cutanés que l’on trouve dans la peau de nombreux hôtes
aviaires, bien que peu de cas aient été rapportés chez les rapaces sauvages. Le suivi des populations d’Accipiter
melanoleucus dans la péninsule du Cap, en Afrique du Sud, entre 2001 et 2012, a révélé que de nombreux oiseaux
présentaient des symptômes d’infection au cours de certaines années. L’examen de trois oiseaux morts présentant des
symptômes tels que la calvitie et des lésions cutanées a révélé une acariase causée par Knemidokoptes, alors que nous
n’avons trouvé aucun cas d’infection subclinique chez les oiseaux sans symptômes (n¼16). Près de 5 % des oiseaux de
la population étaient infectés lors de certaines années, ce qui représente la première mention de plusieurs oiseaux
souffrant d’une acariase causée par Knemidokoptes dans une population sauvage de rapaces. Un biais en faveur des
mâles dans la prévalence de l’infection a été détecté. La prévalence des symptômes d’infection était généralement
faible dans les autres populations ailleurs en Afrique du Sud, bien que possiblement plus élevée dans les zones
urbaines. La performance reproductive (productivité et succès de nidification) était significativement plus faible chez
les individus après l’infection et comparativement aux oiseaux non infectés tout au long de la période étudiée. Il s’agit
de la première étude démontrant l’effet négatif que ces acariens peuvent avoir sur la performance reproductive d’une
espèce d’oiseau sauvage; elle suggère que ce parasite peut potentiellement influencer la dynamique des populations
dans le temps.
Mots-clés: Accipiter melanoleucus, performance reproductive, Knemidokoptes, succès de nidification, parasites,
productivité
INTRODUCTION
How parasites and their hosts interact has fascinated
biologists for centuries (Darwin 1859). Bird–parasite
interactions have proved particularly useful in demon-
strating how parasites can mediate the ecology and
evolution of their hosts (Proctor and Owens 2000).
Research suggests that parasites can be as important as
predators or resource limitation in limiting the growth of
host populations (Anderson and May 1979). This contrasts
Q 2017 American Ornithological Society. ISSN 0004-8038, electronic ISSN 1938-4254
Direct all requests to reproduce journal content to the AOS Publications Office at pubs@americanornithology.org
J. L. van Velden, A. Koeslag, O. Curtis, et al.
with the alternative paradigm of ‘‘successful’’ parasites
evolving to do little or no harm to their hosts, with
commensalism as the end result of the interaction between
host and parasite (Toft 1991). There is, however, considerable evidence against this theory, with many cases
showing that parasites may negatively affect reproduction
(Møller 1993, Richner et al. 1993, Fitze et al. 2004) and
survival (Richner and Tripet 1999), which, in turn, can
influence the host species’ population dynamics and
evolution (Toft 1991).
Parasite loads are rarely distributed evenly within
populations (Clayton and Moore 1997), and parasite
prevalence or intensity may vary across ages, sexes, or
color morphs (Christe et al. 2007, Lei et al. 2013). In many
cases, males may show greater prevalence and intensity of
parasites than females as a result of fundamental biological
and behavioral differences (Christe et al. 2007), and such
male biases are seen in both birds and mammals (Poulin
1996). These differences may be due to steroid hormones
such as testosterone, which, while enhancing the male
host’s secondary sexual characteristics, can also suppress
its immune system (Folstad and Karter 1992). Behavioral
differences such as aggression between males or decreased
male grooming during the mating season may also account
for this bias (Christe et al. 2007). Furthermore, age can also
be significant in determining parasite levels. Older
individuals can have significantly higher parasite burdens,
possibly due to differences in hormonal exposure (Weatherhead and Bennet 1991, Norris et al. 1994, Deviche et al.
2001) or simply due to their length of exposure to potential
parasites or vectors. Alternatively, younger individuals may
have higher parasite burdens because they have yet to
acquire immunity or resistance (Lei et al. 2013).
Parasitic mites are a taxonomically diverse group,
including 2,500 species that are dependent on birds
(Proctor and Owens 2000). Mites and their avian hosts
have highly diverse relationships, ranging from detrimental
to beneficial for their hosts. The genus Knemidokoptes
(Acari: Knemidokoptidae) is a relatively understudied
group of subcutaneous mites found in the skin of the
face, legs, or body of avian hosts. They feed on the host’s
tissue or eat the feather quill’s pith (Proctor and Owens
2000, Dabert et al. 2013), and infection can result in the
condition known as ‘‘scaly leg,’’ ‘‘scaly face’’ (Kirmse 1966),
or ‘‘depluming itch.’’ Symptoms of infection include feather
loss, lesions on the face and beak, and lesions and
encrustations on legs or body (Pence 2008). Proliferation
of growths can cause beak deformities and loss of digits
(Pence 2008, Goulding et al. 2012). About 20 wild
passerines from a variety of families are known hosts
(Latta and O’Connor 2001). The propensity of these mites
to cause epizootic events has been documented in poultry,
in caged birds, and, increasingly, in wild birds (Pence et al.
1999).
Mite infection and reproduction in Black Sparrowhawks
499
In one of the very few studies that have explored the
fitness consequences in wild birds of infection by
Knemidokoptes, Latta (2003) examined infections in
Prairie Warblers (Setophaga discolor) and Palm Warblers
(S. palmarum) in the Dominican Republic. He found that
mite infection caused significantly reduced muscle-mass
scores, reduced site persistence, and reduced annual
return rates after migration—factors that are indicative of
lower survival rates. The compromised physiological
condition of the parasitized individual may increase
susceptibility to mortality during migration, even when
the mite infection may not be fatal in itself (Latta 2003).
This study and a previous one (Latta and O’Connor 2001)
both found that habitat was an important variable, that
Knemidokoptes infections were more common in dry
desert scrub than at higher elevations and in moist
habitats, and that there was a positive relationship
between dry habitat type and the prevalence of infections.
A dry environment like that of the desert thorn scrub
could exert greater physiological stress than moist
habitats, which could promote transmission to a weakened bird. Suboptimal habitats may necessitate increased
expenses of time and energy in foraging, a cost that may
suppress the bird’s immune function. Alternatively, dry
desert habitats may be conducive to a favorable mite
microclimate, aiding the latter’s survival and reproduction (Latta 2003).
Knemidokoptes infestations appear to be uncommon in
birds of prey (Miller et al. 2004). The 3 recorded cases were
all in captive individuals: a Swainson’s Hawk (Buteo
swainsoni; Miller et al. 2004), a captive Great Horned
Owl (Bubo virginianus; Schulz et al. 1989), and a captive
hybrid falcon (Falco spp.; Heidenreich 1997). In the only
study conducted on Knemidokoptes in Africa, focused on
the Cape Wagtail (Motacilla capensis) population of
Dassen Island, Goulding et al. (2012) found that infection
by Knemidokoptes jamaicensis was more than twice as
prevalent on this island as on the mainland, perhaps due to
lower predation rates on the island. Goulding et al. (2012)
also found that larger individuals were more likely to
exhibit signs of infection.
Black Sparrowhawks (Accipiter melanoleucus) have
recently colonized the Cape Peninsula, South Africa, the
first successful breeding attempt having been recorded in
1993 (Oettlé 1994). Since then, the population has
increased substantially to an estimated 50 breeding pairs
(Martin et al. 2014a). Despite this apparent success, a
number of birds with balding heads and/or leg lesions have
been seen in this population in recent years. These
symptoms were considered to indicate infection by
Knemidokoptes, and a postmortem on a dead bird found
with these symptoms appeared to confirm this, the death
being attributed to a severe mite infestation (MacGregor
2012). No abnormalities were detected in the organs of this
The Auk: Ornithological Advances 134:498–508, Q 2017 American Ornithological Society
500 Mite infection and reproduction in Black Sparrowhawks
bird, apart from severe mite infection, pectoral muscle
atrophy, and reduced fat reserves.
In the present study, we investigated infection of Black
Sparrowhawks by this parasite in more detail and
examined the influence that infection might have on an
individual’s reproduction. First, we tested whether the
symptoms described above were indeed closely associated
with Knemidokoptes infection by examining the latter’s
presence in 19 dead birds, 3 of which showed visual
symptoms; the other 16 were asymptomatic and thus could
be used to explore subclinical prevalence. If symptomatic
birds were positive for mites and asymptomatic birds were
not, this would indicate that visual observation can be used
to accurately monitor the prevalence of this parasite in a
population. Second, we determined the frequency of
occurrence of these symptoms on the Cape Peninsula
over a 12 yr period (2001–2012) and examined whether
the occurrence of these symptoms differed between sexes
or between morphs of this polymorphic species (Amar et
al. 2013). Third, using historical data, we examined the
extent of the occurrence of these symptoms elsewhere
across South Africa. Finally, to examine whether mite
infection influenced the reproductive output of infected
birds within the Cape Peninsula, we (1) explored nesting
success (either successful, with chicks fledged; or unsuccessful, where the nest failed at any stage between
courtship and fledging) and productivity (the number of
chicks produced) before and after infection for individually
identifiable birds; and (2) compared breeding attempts
across the population for pairs containing either infected
or noninfected birds.
METHODS
Monitoring of the Cape Peninsula Population
We used data from the monitored Black Sparrowhawk
population on the Cape Peninsula from 2001 to 2012. The
study area featured a matrix of habitats, including urban
gardens, alien pine (Pinus spp.) and eucalyptus (Eucalyptus
spp.) plantations, and small pockets of indigenous
Afromontane forest and Fynbos (Curtis et al. 2007). Our
study area covered a surface of approximately 35 3 17 km2.
For a map of the study area and locations of nests, see
Martin et al. (2014a). Altitudes where the birds breed
range from sea level to ~300 m, and the climate is
temperate, with locally variable winter rainfall (Martin et
al. 2014a).
Monitoring was conducted during the breeding season
(March–November) in each year (Martin et al. 2014a,
2014b). Territories were visited regularly (approximately
monthly) throughout the season until breeding was
detected, and then breeding attempts were monitored
weekly until conclusion. Where possible, we identified the
sex-specific morphs (dark or light) of both parents
J. L. van Velden, A. Koeslag, O. Curtis, et al.
attending a nest, which was possible in ~90% of breeding
attempts. The species is easy to sex visually, males
weighing ~60% less than females (Ferguson-Lees and
Christie 2001). We fitted unique color-ring combinations
to as many breeding adult birds and nestlings (2–3 wk old)
as possible. Adults were trapped on territories using a balchatri trap baited with live white Domestic Pigeons
(Columba livia domestica; Berger and Mueller 1959).
During breeding monitoring, we recorded the color-ring
combination of any ringed birds. During observation with
binoculars or a digital camera, we recorded the occurrence
of any individual Black Sparrowhawk showing visual
symptoms of Knemidokoptes infection. Sightings of
nonbreeding birds with visual symptoms were also
recorded and occurred primarily at monitored breeding
territories, but sporadic observations outside of breeding
territories, such as photographs taken by the public, were
also used. The use of visual observations may cause a bias
toward heavily infected birds with obvious symptoms.
These results are therefore likely to be an underestimate of
the true prevalence of infection.
Sampling Dead Birds for Mite Infection
The presence of Knemidokoptes infections was investigated
on 19 deceased Black Sparrowhawks, which had been
found dead from various causes such as road accidents or
collisions with windows. We aimed to confirm whether
symptomatic birds were indeed infected by Knemidokoptes, as suspected, and also whether any nonsymptomatic
birds showed subclinical effects. Corpses were frozen and
skin scrapings taken from a random leg and from the head
of the bird using anatomical markers—namely, from the
halfway point of the tarsometatarsus, at both the front and
the back of the leg; from the top or side of each toe; and
from the crown of the bird’s head. A total of 7 skin samples
were taken from each bird. The scrapings were taken from
just under the leg scales or feathers of the bird, using a
scalpel, and placed on individual slides. A small amount of
potassium hydroxide (10% KOH) was added to each
scraping, in order to macerate the waxy layer of the scales
and skin (Schulz et al. 1989, Pence et al. 1999). A coverslip
was applied and the slides were examined at 403
magnification with a compound microscope. The presence
of mites was noted for each slide. All slides received the
same search effort of ~5 min per slide, in order to
standardize effort and ensure efficient and thorough
examination. Additionally, a heavily symptomatic male
bird (specimen A) was sent for postmortem examination
by the Western Cape state veterinarian (MacGregor 2012).
Establishing Infections Elsewhere in South Africa
We contacted researchers elsewhere in South Africa who
had monitored Black Sparrowhawks to establish whether
they had seen birds with symptoms of Knemidokoptes
The Auk: Ornithological Advances 134:498–508, Q 2017 American Ornithological Society
J. L. van Velden, A. Koeslag, O. Curtis, et al.
Mite infection and reproduction in Black Sparrowhawks
501
TABLE 1. Information on symptoms of mite infection in Black Sparrowhawks across South Africa, including the source, time period,
location, and number of breeding events (n) for each study.
Source
Tarboton and Allan 1984
E. Wreford personal communication
Malan and Robinson 2001
H. Chittenden personal communication
http://fireflyafrica.blogspot.com/2012/07/black-sparrowhawk.html
Present study
Tate et al. 2016
Total
infection (i.e. baldness and leg lesions). Sources of this
information are summarized in Table 1. For sites or studies
with multiple monitored pairs, we also obtained information on the number of breeding events monitored and the
number of infected birds seen. The percentage of the
breeding population that was infected was calculated and
compared with that of the Cape Peninsula population.
Statistical Analysis
We used a chi-square test to examine whether either sex or
morph (dark or light) was infected at a higher rate than
expected. This analysis used the data on prevalence of
infection symptoms in wild, live, infected individuals (n ¼
20). Expected proportions of infected individuals of the 2
morphs, based on the average percentages of dark and
light birds in the population (i.e. 76% dark and 24% light;
Amar et al. 2013), were applied to all infected individuals
of known morph (n ¼ 20). We estimated the expected
numbers of infected males and females from all observed
infected individuals of known sex (n ¼ 14), assuming a
balanced 1:1 sex ratio (Brown and Brown 1979).
To explore the influence of infection on nesting success
and productivity, 2 separate analyses were performed using
generalized linear mixed models (GLMM) in R (R
Development Core Team 2013). Our first analysis assessed
the difference in breeding performance before and after
infection, at the level of the individual, using birds that
were individually recognizable between years. We also
analyzed the relationship of infection to nesting success
and to productivity. Nesting success was treated as
binomial (1 ¼ successful breeding, 0 ¼ unsuccessful
breeding), where unsuccessful breeding occurred if the
nest failed at any stage between courtship and the chicks
leaving the nest. Productivity, defined as the number of
chicks surviving to leave the nest for any breeding event,
ranged from 0 to 3 chicks and approximated a Poisson
distribution.
Each bird in the first analysis was given a unique
identifier, which was specified as a random term to control
for the nonindependence of samples for the same bird
prior to and after infection. Even when an infected bird
was unringed, it could be reliably identified by its morph,
Period
Location
n
1976–1980
2011–2012
2001
2010–2011
2012
2001–2012
2014
Nylsvley
Kwa-Zulu Natal
Across South Africa
Kwa-Zulu Natal
Port Elizabeth
Cape Peninsula
Across South Africa
118
29
58
2
1
442
109
759
its sex, and the presence of infection, and therefore
breeding outcome could still be determined and attributed
to specific birds. Individuals could be identified relatively
accurately because this was a small population in which
pairs and individuals were relatively faithful to nesting
territories (Martin et al. 2014a). If a bird was not color
ringed, the combination of its lack of color rings (.75% of
adults were color ringed), its infection status, and its
morph could be used to reliably identify the individual.
Our second analysis explored the breeding performance
of a pair within a year, in relation to whether the pair
contained an infected bird or not. This analysis therefore
took advantage of our more extensive dataset. We included
only years in which at least one individual of a pair was
infected (2007–2012). The effects of infection on both
nesting success and productivity were analyzed. We
included ‘‘year’’ and ‘‘territory’’ as random variables within
this GLMM. Although the variable ‘‘territory’’ was used in
this analysis, in the majority of cases this equates to a
unique identifier of a ‘‘pair.’’ The analysis therefore
examined the reproductive output of a pair breeding at a
territory in relation to the infection status of the pair, and
also compared pairs within the same year. Preliminary
analyses using a general linear model (with age fitted as the
response variable and sex fitted as an explanatory variable)
confirmed that there was no difference in mean age
between infected and uninfected birds (females: infected
mean age ¼ 6.38 yr, uninfected mean age ¼ 5.77, F ¼ 0.586,
df ¼ 191, P ¼ 0.444; males: infected mean age ¼ 6.90,
uninfected ¼ 5.81, F ¼ 1.499, df ¼ 170, P ¼ 0.22).
RESULTS
Confirmation of Knemidokoptes Infection
Among the 19 dead individuals sampled using skin
scrapings, 3 adult males were found to be infected with
Knemidokoptes. Two individuals had severe symptoms
(specimen A: bald with severe leg lesions; specimen B: bald
with ‘‘scaly’’ legs but with no obvious leg lesions), and
microscopic examination of skin scrapings confirmed that
both were infected on the head and legs with Knemidokoptes. Specimen A was confirmed as infected through a
The Auk: Ornithological Advances 134:498–508, Q 2017 American Ornithological Society
502 Mite infection and reproduction in Black Sparrowhawks
J. L. van Velden, A. Koeslag, O. Curtis, et al.
infer subclinical prevalence conclusively with only 16
samples.
Temporal Prevalence of Infection within the Cape
Peninsula Population
Between 2001 and the end of 2012, within the Cape
Peninsula study area, we observed 20 cases of live birds
with infection symptoms among a maximum of 98 ringed
birds (20.4%). In total, 442 breeding events have been
monitored in this population. Of the 20 infected birds, 10
were part of a breeding pair, whereas the other 10 birds
were observed outside of territories and could not be
ascribed to a pair. Multiple infections appeared to occur in
the same years (Figure 2) and only started appearing once
the population had exceeded 25 territorial pairs.
Among these 20 wild, live, infected birds, 13 were dark
and 7 were light morphs. The ratio of infected birds of the
2 morphs did not differ significantly from expected given
the proportion of dark and light birds in this population, in
which dark morphs are more prevalent (76% dark morph;
v2 ¼ 1.33, P ¼ 0.25). Among the 14 infected birds of known
sex were 11 males and 3 females; assuming a 1:1 sex ratio,
the proportion of males infected was significantly higher
than expected (v2 ¼ 4.57, P ¼ 0.03).
FIGURE 1. Female Black Sparrowhawk with symptoms of mite
infection; note the bald head and severe leg lesions. Photo
credit: G. Tate
postmortem carried out by the state veterinary laboratory,
and specimen B was confirmed as infected using the same
microscopic examination of skin scrapings by one of the
authors (J.V.V.). One other individual (specimen C), which
had only a very small lesion on the leg, was also found to
be infected by Knemidokoptes; in this case, however, the
symptoms would probably not have been detected from
general visual observation of the free-living bird. The mites
were identified as Knemidokoptes spp. by one of the
authors (T.G.) and further confirmed by Heloise Heyne of
Onderstepoort Veterinary Institute, although the species
was not identified. Mites were seen in burrows they had
excavated in the skin at a subcutaneous level.
None of the 16 Black Sparrowhawk carcasses without
visual symptoms were found to be infected with mites
(including 6 adult males, 4 adult females, 3 juvenile males,
and 3 juvenile females). It therefore appears that the
symptoms of bald head and leg lesions (Figure 1) were
exclusively linked with infection by Knemidokoptes in this
species of bird, and it also appears that there is little
subclinical infection by this parasite. However, we cannot
Nesting Success and Productivity in Relation to
Infection Status
To investigate the effect of infection on breeding
performance, we carried out 2 separate analyses. Our first
analysis examined breeding performance before or after
infection for recognizable individuals. There were data on
nesting success and productivity for 10 individuals, which
spanned 34 breeding attempts, including 15 before
infection and 19 during or after infection. We found that
both nesting success (whether young fledged or not) and
productivity (total number of chicks fledged) were
significantly lower once a member of the pair was infected,
compared to these values prior to infection (nesting
success: v2 ¼ 4.06, P ¼ 0.044; productivity: v2 ¼ 5.560, P
¼ 0.018). The estimates of the coefficient were 0.32 (95%
confidence interval [CI]: 0.64 to 0.01) for nesting
success and 1.38 (95% CI: 2.52 to 0.23) for productivity. For those individuals that became infected (i.e. showed
symptoms), average nesting success (6 SE) was 0.53 6
0.13 prior to infection but fell to 0.21 6 0.09 following
infection, and average productivity was 1.24 6 0.31 prior
to infection but fell to 0.29 6 0.17 following infection
(Figure 3).
Our second analysis included all breeding attempts by
all birds in years in which at least one bird from a pair was
infected (2007–2012) and compared breeding performance of pairs with at least one infected bird to that of
uninfected pairs. Between 2007 and 2012, we recorded the
outcomes of 247 breeding attempts, 18 of which had at
The Auk: Ornithological Advances 134:498–508, Q 2017 American Ornithological Society
J. L. van Velden, A. Koeslag, O. Curtis, et al.
Mite infection and reproduction in Black Sparrowhawks
503
FIGURE 2. Number of infected Black Sparrowhawks (bars) that were part of a breeding pair in the Cape Peninsula population for
each year of the study, compared to the total number of birds in the breeding population (points).
least one infected bird present. Five of the infected birds
had multiple breeding attempts included in this analysis,
while 6 birds had only a single breeding attempt included.
The results were similar to those of our first analysis, with
significantly lower productivity (v2 ¼ 10.70, P ¼ 0.001)
and nesting success (v2 ¼ 12.12, P , 0.001) for breeding
attempts including infected birds. The estimates of the
coefficient were 1.51 (95% CI: 2.40 to 0.60) for
productivity and 2.54 (95% CI: 3.96 to 1.11) for
nesting success. The values were similar to those in the
previous analysis, with an average (6 SE) nesting success
of 0.66 6 0.03 for noninfected pairs but only 0.16 6 0.09
for pairs with at least one infected partner, and average
productivity of 1.19 6 0.08 for noninfected pairs but only
0.26 6 0.15 for infected pairs. In 9 of 18 infection cases
(50%), breeding failure could not be attributed to a
specific cause other than mite infection itself; and in 5 of
these 9 cases, breeding failed at the nest-building stage.
Among the other 9 infection cases in which a cause of
failure was known, there were 4 cases of failure due to
geese harassment, 3 cases in which the female was
suspected to be infertile, and 2 cases in which the nest
tree was disturbed by humans.
Infections by Knemidokoptes Elsewhere in South
Africa
Including the Cape Peninsula, only 5 areas of South Africa
had reports of Black Sparrowhawks with symptoms of mite
infection such as balding and leg lesions. Besides the Cape
Peninsula, we obtained records of birds with infection
symptoms in Port Elizabeth, Dullstroom, Nkaleni Valley,
and around the Durban area (Figure 4). No infections were
reported in the rest of the country. Port Elizabeth was
found to have the highest number of infections in relation
to the number of breeding events studied (3/18), followed
by Durban (3/50) and the Cape Peninsula (20/447).
Infections around the Durban area were recorded only in
recent years (2011 and 2012): E. Wreford recorded 3
infections from 29 breeding events (Table 1). Within the
former Transvaal area (Nylsvley), Tarboton and Allan
(1984) monitored 118 breeding events and recorded no
cases of infection. Across South Africa, Malan and
Robinson (2001) monitored 58 breeding events and
recorded no incidence of infection. Finally, a wide survey
across South Africa in 2014 by Tate et al. (2016) reported 3
birds with infections (2 in Port Elizabeth and 1 in
Dullstroom). Thus, it appears that infection has only been
FIGURE 3. Average (6 SE) nesting success (hatched bars) and
productivity (black bars) of individual Black Sparrowhawks that
were part of a breeding pair—recorded as infected (n ¼ 10),
before infection, and after infection—during breeding on the
Cape Peninsula between 2001 and 2013. Differences before and
after infection were significant (P , 0.05) for both variables.
The Auk: Ornithological Advances 134:498–508, Q 2017 American Ornithological Society
504 Mite infection and reproduction in Black Sparrowhawks
J. L. van Velden, A. Koeslag, O. Curtis, et al.
FIGURE 4. Map of South Africa showing the distribution of monitored Black Sparrowhawks. The size of each circle is proportional to
the log number of breeding events monitored in the respective area. Gray portions of each pie chart represent the proportion of
uninfected breeding events studied, and black the proportion of birds with symptoms of infection by mites in the genus
Knemidokoptes.
witnessed over the past decade and is largely confined to
urban areas.
DISCUSSION
We found evidence consistent with the assumption that
the symptoms (bald heads and leg lesions) suspected of
being the result of infection by Knemidokoptes were indeed
associated exclusively with infection by this subcutaneous
parasitic mite. Our study is the first to report a large
number of clinical Knemidokoptes infections in a wild
population of a bird of prey. Among the 16 Black
Sparrowhawks that showed no such symptoms, none were
found to be infected. These results suggest that observations of symptomatic birds can be used to monitor the
prevalence of this parasite in a population and that
subclinical levels of infection are low. The prevalence of
subclinical infection by Knemidokoptes in other captive
and wild birds is undocumented (Pence et al. 1999). We
were unable to confirm the exact species of mite because
genetic identification to the species level is currently
limited by a lack of reference sequences.
Importantly, this is the first time that reduced breeding
performance has been found in birds with Knemidokoptes
infections, which was evident both when comparing
breeding performance before and after severe infection
and also from the larger analysis comparing breeding
performance of noninfected and infected pairs. Following
infection, nesting success and productivity were at less
than half the level found prior to infection. This is,
however, a correlative study, and it cannot be said that mite
infection definitely caused the reduction in breeding
performance. A bird in an already weakened state could
be more susceptible to infection, given that metabolic
stress causes immunosuppression and, thus, increased
susceptibility to parasitic diseases (Folstad and Karter
1992, Deerenberg et al. 1997), and this weakened state
would negatively affect breeding separately. Interestingly,
the productivity of infected birds before infection was
similar to overall productivity levels for the uninfected
population as a whole (i.e. 1.24 6 0.31 for 35 breeding
attempts vs. 1.19 6 0.04 for 352 breeding attempts), and
so infected birds were not necessarily those already in
poorer condition or inhabiting lower-quality territories. If
that had been the case, we might have expected to see
lower productivity before infection compared to the
productivity of other birds. This depressed nesting success
and productivity of infected birds indicates that, in theory,
this parasite has the potential to influence population
growth rate in this species.
Within the Cape Peninsula population, we found a sex
bias in infection prevalence, with more males infected than
would be expected assuming a 1:1 sex ratio. This male bias
may actually be an underestimate, since ringing studies
The Auk: Ornithological Advances 134:498–508, Q 2017 American Ornithological Society
J. L. van Velden, A. Koeslag, O. Curtis, et al.
indicate that detectability is higher for female than for
male Black Sparrowhawks (Tate et al. 2017). Similar male
biases in infection rates have been found in some species.
For example, breeding adult male Red Crossbills (Loxia
curvirostra) had a higher rate of infection by K. jamaicensis
than females (Benkman et al. 2005). In contrast, however,
no difference in the prevalence of infection by K.
jamaicensis was found between the sexes of Prairie
Warblers, although Benkman et al. (2005) conducted their
study during the nonbreeding period, which may have had
an influence (Latta 2003). Male-biased parasite prevalence
has frequently been found (Roberts et al. 2004) and has
been linked to the presence of hormones such as
testosterone, which can suppress immune function (Folstad and Karter 1992). Behavioral traits specific to males,
such as territorial disputes or reduced preening during the
breeding season, may also play a role. Male Black
Sparrowhawks perform most of the hunting (Tate et al.
2016) and possibly most of the territorial defense (Newton
1986) throughout the breeding season, and this greater
energetic cost may put them under greater physiological
stress than females, which has been linked to reduced
immune function (Deerenberg et al. 1997). Indeed, in this
same population, male Black Sparrowhawks infected with
the blood parasite Haemoproteus nisi had a higher parasite
load than females (Lei et al. 2013).
We found no significant difference in the incidence of
infection between dark and light morphs. There may,
however, have been a lack of statistical power in this test,
as a result of the small sample sizes for each group. Genes
coding for melanin-based plumage color have previously
been shown to have pleiotropic effects (Catania and Lipton
1993, Hoekstra 2006), including providing improved
parasite resistance. Indeed, in our study population, dark
morphs had a higher resistance to infection by the blood
parasite H. nisi than light morphs (Lei et al. 2013). It was
suggested that the improved ability to resist chronic bloodparasite infection may explain the bias toward dark
morphs in the Cape Peninsula population (Amar et al.
2013, Leit et al. 2013). In the only other study exploring
ectoparasite burden in polymorphic raptors, it was found
that the prevalence of the blood-sucking fly Carnus
haemapterus in Common Buzzards (Buteo buteo) increased with the darkness of nestling plumage (Chakarov
et al. 2008).
Close contact is likely necessary for transmission of
Knemidokoptes between hosts (Wichmann and Vincent
1958), although some experiments have found that direct
contact does not necessarily ensure transmission (Kirmse
1966). One possibility is that Black Sparrowhawks in our
study population are becoming infected through infected
prey. This species feeds almost exclusively on birds (Malan
and Robinson 1999, Suri et al. 2016) and regularly preys on
domestic fowl (Suri et al. 2016), which are known to be
Mite infection and reproduction in Black Sparrowhawks
505
infected by multiple Knemidokoptes species (e.g., K.
mutans; Morishita 1996), including within the Cape
Peninsula (J. L. van Velden personal observation). If this
infection pathway is responsible, it may explain the male
bias in infection, given that males will spend more time
processing prey during the breeding season—for example,
plucking the prey before providing the processed item to
the female or juveniles (Brown and Brown 1979, Katzenberger et al. 2015). Males may therefore have a higher
exposure risk than females.
Another possible transmission pathway may occur when
infected birds transmit mites to either partners (horizontal
transmission) or chicks (vertical transmission). Although
there did appear to be an age bias in Knemidokoptes
infection, given that all infected birds were adults, it is
possible that chicks die or recover without the infection
ever being recorded, or that symptoms develop too slowly
to be recorded when they are nestlings. However,
subsequent to our analysis, 2 nestlings with clinical
symptoms were produced by an infected parent (A.
Koeslag personal observation), which suggests that vertical
transmission may occur. Parasite virulence, in terms of the
host’s reproductive success, tends to be greater in
horizontal transmissions than in vertical transmissions,
because vertically transmitted parasites are dependent on
the host’s reproductive success in order to be passed on to
a new host, whereas horizontal parasites are relatively
independent of the host’s reproduction (Clayton and
Tompkins 1994). Consistent with our results, a higher
prevalence of Knemidokoptes was found in adult Eurasian
Tree Sparrows (Passer montanus; Mainka et al. 1994), and
infection by K. jamaicensis was found only in adult Red
Crossbills (Benkman et al. 2005).
The cities of Cape Town, Port Elizabeth, and Durban
were found to be the areas with the most infection events.
The other infection occurrences were single reports within
a very small sample size and therefore cannot give much
information. Given the diversity of sites around South
Africa that have been subjected to scientific study, as well
as the very few records from members of the public
following an appeal for records (van Velden and Amar
2013), we believe that our data probably do reflect the real
situation with respect to the prevalence of Knemidokoptes
infection within South Africa. Although 5% of the Cape
Peninsula population being infected does not necessarily
constitute an epizootic event, this finding is still considerable when compared to other studied populations of
wild birds of prey. One explanation for the higher
frequency of infection observed in the Cape Peninsula
population could be the greater monitoring effort to which
this population has been subjected; however, in other
regions with long-term intensive monitoring, such as
Nysvley, no cases were reported. It is possible that the
Cape Peninsula is suboptimal habitat for Black Sparrow-
The Auk: Ornithological Advances 134:498–508, Q 2017 American Ornithological Society
506 Mite infection and reproduction in Black Sparrowhawks
hawks, which may make this population susceptible to
mite infection via physiological stress (e.g., Latta and
O’Connor 2001). However, this explanation seems unlikely
given the rapid colonization and population expansion
seen over the past 2 decades (Martin et al. 2014a).
The reduced nesting success and productivity we
oberved after infection by Knemidokoptes may arise
because the adult birds become too agitated to incubate
effectively; physical irritation has previously been identified
as a cause of nest failure and desertions in other bird–
parasite systems (Duffy 1983, Clayton and Tompkins
1995). However, this may be less important, given that
there was a male bias in infection and that males do not
play a significant role in incubation. In our observations of
female Black Sparrowhawks on the Cape Peninsula that
exhibited signs of clinical infection, the birds appeared to
be agitated, restless, and nervous of disturbance, often
flying off the nest when approached. These behavioral
changes will likely disturb incubation, leading to clutch
failure. If the male is infected, hunting efficiency may be
reduced, which may, in turn, negatively affect breeding
performance. Additionally, the productivity of this species
is significantly affected by nest usurpation by Egyptian
Geese (Alopochen aegyptiaca; Curtis et al. 2007, Sumasgutner et al. 2016), and the weakened state of infected
Black Sparrowhawks may potentially compromise the
ability of these individuals to defend against geese or build
replacement nests.
Conclusion
This is the first study of mites in the genus Knemidokoptes
within a wild population of birds of prey. All other cases of
infection by these mites occurred in lone, usually captive,
birds of prey. The prevalence of this infection in the Cape
Peninsula and Durban populations seems unusually high.
Breeding performance was lower following mite infection
than prior to it, and was lower for infected pairs than for
noninfected pairs, which has the potential to affect the
stability of this population over time. Males appear to be
especially affected by this infection, potentially because of
the greater energetic costs they bear at breeding, leading to
a weakened immune system, or else from greater exposure
to vectors such as infected prey. Infections in this
population emerged only after the number of pairs
surpassed 25, and therefore it may be a density-dependent
parasite. Although the population of Black Sparrowhawks
has been steadily increasing since their colonization of the
Cape Peninsula, Knemidokoptes infections could, in theory,
reduce this growth rate through the negative effect on
breeding performance. Although the Black Sparrowhawk
is not a species of conservation concern, an understanding
of this parasite’s occurrence and its effects on a wild raptor
J. L. van Velden, A. Koeslag, O. Curtis, et al.
species may prove useful should epizootic events occur in
another threatened raptor population.
ACKNOWLEDGMENTS
We thank G. Tate for help in providing samples; R. Martin, E.
Wreford, G. Malan, H. Chittenden, W. Tarboton, and P.
Sumasgutner for use of their data; and H. Heyne for help with
mite identification.
Funding statement: The National Research Foundation of
South Africa provided funding for this research. None of the
funders had any influence on the content of the submitted
manuscript. None of the funders require approval of the final
manuscript to be published.
Ethics statement: All research was performed in accordance
with approved guidelines. All procedures adhered to the legal
requirements of South Africa and were carried out under a
Cape Nature Hunting Permit (no. 0035-AAA004-00428), a
South African National Parks permit, and a SAFRING ringing
permit (no. 1439). All protocols were approved by the
University of Cape Town Science Faculty Animal Ethics
Committee (no. 2012/V37/AA).
Author contributions: A.A. conceived the study and
designed the methods. J.V.V. and A.K. conducted the research.
J.V.V. and A.A. analyzed the data and wrote the paper. A.K.,
T.G., and O.C. contributed substantial materials, resources, or
funding.
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