Veterinary Parasitology: Regional Studies and Reports 20 (2020) 100411

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Veterinary Parasitology: Regional Studies and Reports

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Original Article

Development and number of generations of Haematobia irritans (Diptera: T

Muscidae) in bovine fecal masses in the semiarid region of Brazil
Lídio Ricardo Bezerra Meloa, Márcia Alves Medeirosa, Lucas Alencar Fernandes Beserraa,
Antônio Thadeu Medeiros Barrosb, Franklin Riet-Correaa,c, Sérgio Santos Azevedoa,
⁎
Vinícius Longo Ribeiro Vilelaa,d,
a
Programa de Pós-Graduação em Ciência e Saúde Animal, Universidade Federal de Campina Grande (UFCG), Avenida Universitária s/n. Patos, Paraíba, Brazil
b
Embrapa Gado de Corte, Av. Rádio Maia 830. Campo Grande, Mato Grosso do Sul, Brazil
c
Instituto Nacional de Investigación Agropecuaria (INIA), Plataforma de Salud Animal, Estación Experimental INIA Tacuarembó, Ruta 5 km 386, Tacuarembó, Uruguay
d
Departamento de Medicina Veterinária, Instituto Federal da Paraíba (IFPB), Avenida Presidente Tancredo Neves s/n. Sousa, Paraíba, Brazil

A R T I C LE I N FO A B S T R A C T

Keywords: The horn fly (Haematobia irritans) is particularly unique among the parasites that primarily affect Brazilian cattle
Horn fly farming. Appropriate control strategies fundamentally depend on epidemiological knowledge, which is parti-
Ectoparasite cularly scarce in Northeastern Brazil. This study aimed to elucidate the ecology of the immature horn fly in the
Non-parasitic phase semiarid region of Brazil. Bovine fecal masses were collected and covered with emergence traps to collect the
horn fly for sexing and counting. Weather records of the region were concurrently acquired. A total of 11,390H.
irritans were collected from 601 fecal masses, with a sex ratio of 0.9:1 (male: female). Horn fly emergence was
observed in 78% (15%–100%) of the fecal masses, varying from 1 to 185 (mean = 23.3) flies/fecal mass,
predominantly at the beginning of the rainy season. The minimum period for egg-to-adult development of H.
irritans varied from 7 to 11 days, indicating the occurrence of 30 generations per year in the region. Rapid
development of the immature horn fly in the semiarid region, throughout the year may results in a high number
of generations and infestations in cattle herds.

1. Introduction
The horn fly (Haematobia irritans) is a small hematophagous dip-
teran that preferentially affects cattle and eventually horses, sheep, and
canines (Bruce, 1964). This species was first recovered in Brazil in the
1980s in Roraima (Valério and Guimarães, 1983); however, the fly
subsequently dispersed to other states and within a decade, it had
spread throughout the country.
A horn fly bite causes intense discomfort to the host, interfering
with rest and productivity (Guglielmone et al., 1997). The importance
of fly is recognized in several countries, considering the fact that this fly
is one of the major ectoparasites affecting cattle. It estimated to cause
annual losses of US$ 2.56 billion in Brazil (Grisi et al., 2014).
Horn flies remain on cattle and females lay eggs in the feces after
mating. The eggs hatch in less than 16 h and the larvae develop in the
fecal mass for approximately 4 days, subsequently developing into
pupae. The adults emerge from pupae in the fecal mass after approxi-
mately 5 days (Bruce, 1964).
Recent studies on the population dynamics of H. irritans in the
Paraíba semiarid region have demonstrated relatively high rates of in-
festations in herds throughout the year. Fly population predominantly
peaks after the onset of rainfall (March) and in the dry season (October/
November), with average infestations of up to 226.4 flies/animal
(Medeiros et al., 2018). For further epidemiological evaluation of the
horn fly in the semiarid region, this study investigated specific aspects
of the biological cycle of the non-parasitic phase of this fly in the region.
These studies complement the knowledge regarding the parasitic phase
of the organism in the Brazilian semiarid region and contribute to the
control programs for this parasite in that region.
It is noteworthy that, despite its economic importance, a relatively
small number of studies have examined the bioecology of this parasite
in Brazil; furthermore, there are fewer studies regarding its immature
phase.
2. Material and methods
The study was conducted for one year, from July 26, 2016 to July
28, 2017, at the Núcleo de Pesquisas para o Trópico Semiárido

⁎
Corresponding author at: Avenida Presidente Tancredo Neves, s/n, Jardim Sorrilândia, ZC 58800-970 Sousa, PB, Brazil.
E-mail address: vinicius.vilela@ifpb.edu.br (V.L.R. Vilela).

https://doi.org/10.1016/j.vprsr.2020.100411
Received 24 January 2020; Received in revised form 8 April 2020
Available online 13 April 2020
2405-9390/ © 2020 Elsevier B.V. All rights reserved.
L.R.B. Melo, et al.
(Nupeárido Farm), Universidade Federal de Campina Grande - UFCG
(07°0′25”S, 37°16′41”W), municipality of Patos, Paraiba State,
Northeastern Brazil. This farm was located at an altitude of 242 m, on
the banks of the Jatobá dam. The region had a warm semiarid climate
and is classified as type BSh according to the Köppen-Geiger climate
classification, with annual rainfall ranging from 600 to 700 mm;
monsoon season from January to May (> 90% of rainfall), and dry
season extending from June to December.
During the study, the farm had a herd of 65 Sindhi cattle (33 cows,
30 calves, a breeding bull, and a steer) naturally infested with the horn
fly. The animals were kept in a semi-extensive system in a native field
area with predominantly white mallow (Sida sp.) and panasco grass
(Aristida sp.); the cattle were not treated with any form of antiparasitic
agents during the study. The experimental herd was gathered for
milking in a picket near the corral on each day, in the late afternoon.
The diet of the animals was supplemented with chopped elephant grass
(Pennisetum sp.) and corn bran during the months (September to
January) of forage shortage.
Twenty freshly deposited and intact fecal masses were randomly
selected and collected between 6 am and 8 am, for approximately 1.5 h,
on each collection day. The masses were collected using a shovel, by
scraping the soil under the fecal mass to avoid its disruption; if dis-
rupted, another sample of a fecal mass was selected. The fecal masses
were subsequently deposited in wooden crates (35 × 50 × 5 cm) and
transferred to a paddock, to protect them from being trampled by an-
imals. Then emergence traps were immediately installed over the
masses.
The emergence traps (Corrêa et al., 2013) (Fig. 1) included a pyr-
amidal metal frame, with a 50-cm base, covered with a polyester or-
ganza. At the top of the trap, a metal ring was attached to fit a plastic
funnel, made from the neck of a 2-l clear PET (polyethylene ter-
ephthalate) bottle. This was connected to a collector that was made
from an identical type of bottle to capture the adult flies. The connec-
tion between the funnel and the collector was made by gluing a PET
bottle cap with the lid removed to a hole in the lower-central part of the
bottle (collector), as shown in Fig. 1. The ends of the metal base had 16-
cm long pins (iron rebar) to better fix the trap to the ground.
The traps were monitored daily and the entomological materials
were collected, dry packaged in labeled plastic containers, and
Fig. 1. A. Emergence trap used in a study on the non-parasitic phase of Haematobia irritans in the semiarid region of Paraiba state, Brazil. B. Structure detail: collector
(a), funnel (b), support ring (c), pyramidal frame (d) and base with ground anchor pins (e) (Extracted from Corrêa et al., 2013).
2
Veterinary Parasitology: Regional Studies and Reports 20 (2020) 100411
transferred to the Laboratory of Parasitic Diseases of Domestic Animals
(LPDDA/UFCG) for horn fly identification, counting and sexing ac-
cording to the methods described by Cicchino et al. (1994). Trap col-
lections were stopped after horn fly emergence was completed for each
generation; completion was considered to have occurred when no horn
fly was observed for 3 consecutive days in all collectors, although their
emergence had been previously observed in at least one of the fecal
masses. Daily processing of the collected entomological material fa-
cilitated the real-time determination of the emergence peaks of each
generation, which were used to define the next collection of fecal
masses. Collection of fecal masses followed the development (egg to
adult) of each generation, which was rigorously performed for 4 days
after the emergence peak of the previous generation. Therefore, the
interval between fecal mass collections depended on the duration of the
horn-fly biological cycle throughout the year, and each collection cor-
responded to the initiation of a new generation.
Throughout the study, climate records for temperature, relative
humidity, and rainfall were obtained from a local weather station
(INMET Station 82,791, Patos, PB), 8 km from the study site. Monthly
averages of temperature and relative humidity corresponded to the
arithmetic mean of the daily maximum and minimum values that were
measured throughout the study.
Influence of climatic variables associated with biological parameters
was analyzed using the Pearson's correlation coefficient (r), and the
emergence frequency of males and females was compared by the Mann-
Whitney's test, with the statistical software Bioestat 5.0 (Ayres et al.,
2007).
This study was approved by the Ethics Committee of UFCG, Patos-
PB and authorization for execution was obtained (Registration 068/
2016).
3. Results
Climatic conditions observed during the study were typical for the
region, with monthly average temperatures ranging from 24.7 to
33.0 °C (mean = 28.4 °C) and relative humidity between 23.3% and
60.1% (mean = 41.3%). Despite the fact that the average annual
rainfall in the region ranged from 600 mm to 700 mm, rainfall during
the study year was only 476 mm. Maximum and minimum precipitation
L.R.B. Melo, et al. Veterinary Parasitology: Regional Studies and Reports 20 (2020) 100411

Fig. 2. Average number of Haematobia irritans recovered from bovine fecal masses from July 28, 2016 to July 17, 2017 (30 generations) and climatic parameters
recorded throughout the experiment, in the municipality of Patos, Paraiba, Brazil.

was recorded in February (136.2 mm) and July 2017 (10.6 mm), re- irritans in the fecal masses ranged from 7 to 11 days (average 9.1).
spectively (INMET, 2017). The months from January to April were the However, emergence was initiated within 7 to 8 days in 29 (96.7%)
wettest, while those from July to December (except November) were generations. Considering a pre-laying period (emergence of horn fly
the driest, with no records of precipitation (Fig. 2). immediately after laying the eggs) of 4 days, counting from the emer-
Throughout the experiment, 620 fecal masses were collected, gence peak of each generation, emergence was found to occur in 30
among which, the results of 19 were discarded due to problems with generations of horn fly under semiarid conditions in the Paraiba state.
trapping and/or captured insects (typically caused by ants). In total, After the first month, there was a stable pattern in the number of
11,390H. irritans were collected from the emergence traps generations occurring throughout the study, which alternated between
(mean = 24.3; range = 1–185 flies/fecal mass). The frequency of horn 2 and 3 generations each month (Fig. 2).
fly emergence in fecal masses ranged from 15% to 100% throughout the The average number of horn fly/fecal mass ranged from 1.7 (26th
collections, with an average of 78% for the 601 fecal masses that were generation) to 84.1 (14th generation). Typically, the emergence of H.
analyzed. irritans adults ranged from 2 (24th, 26th, and 27th generations) to
The number of horn flies per generation ranged from 5 (26th gen- 5 days (2nd, 4th, 13th, and 14th generations). Average duration of the
eration - May) to 1514 (14th generation - January). Furthermore, the emergence of H. irritans ranged from one (26th generation - May) to
monthly measurement of the total captured horn fly ranged from 61 3.5 days (13th generation - December), with an average of 1.7 days.
(June) to 3129 (January). Furthermore, with regard to the duration from the oviposition of H.
The results of sexing of 11,349 horn flies revealed 5277 (46.5%) irritans females in the fecal masses until the emergence peak, there was
males and 6072 (53.5%) females, with a sex ratio of 0.9: 1 (male: fe- a variation of 7 to 10 days (mean = 8.3 days). A higher frequency of
male). Female emergence was higher than male emergence in 93.3% emergence was observed on the eighth (20 generations) and ninth (7
and 86.6% of fecal masses on the first and peak emergence day, re- generations) days after the H. irritans females laid eggs in the fecal
spectively. Therefore, females were considerably more frequent than masses.
males on the first day of emergence (63.0% and 37.0%, respectively) A greater number of horn flies per generation was observed from
and on the peak emergence day (56.2% and 43.8%, respectively). July to January (1st to 16th generation) in conditions of high tem-
However, the males (65.8%) were significantly more abundant than the perature (average 29.5 °C) and low humidity (average 33.2%). There
females (34.2%) on the last day of emergence in 76.7% of the ob- was a sudden increase in the number of emerged flies (n = 881) in
servations (Table 1). Emergence of females was higher than that of November (10th generation), which coincided with the onset of the first
males in 83.3% of the generations. rain after a long drought of several months; additionally, the rain in
The minimum time required for the development (egg - adult) of H. January (14th generation) resulted in an emergence peak of 1514 flies.
The increased rainfall (357.2 mm) and relative humidity (RH) (average
50.6%) from the 17th generation (February) until the end of the study
Table 1
Mean absolute frequency of Haematobia irritans males and females in bovine resulted in a reduction in the number of flies. During this period, the
fecal masses, in relation to the emergency day, from August 2016 to July 2017, average temperature (27.3 °C) decreased by slightly more than 2 °C in
in the semiarid region of Paraíba state, Brazil. comparison with the period of greatest fly abundance.
Linear correlation analysis between biological parameters and cli-
First day of emergence
mate variables (mean temperature and mean RH) was statistically sig-
Sex Average Median Standard error P value nificant (p < .05), as presented in Table 2. There was no significant
Male 46.6 15.5 13.1 P = 0,139 correlation between all the biological parameters and the rainfall in-
Female 79.4 28.5 18.8 dexes analyzed.
Emergence peak
Sex Average Median Standard error P value
Male 98.4 53.5 18.7 P = 0,371 4. Discussion
Female 126.2 77.0 22.7

Emergence end The methodology used in the present study differed from that used
Sex Average Median Standard error P value
previously in the country, in which the number of generations was
Male 4.4 2.0 0.9
Female 2.3 1.0 0.7 P = 0,018 estimated from the temperature of the fecal masses (Rodrigues and
Marchini, 2001) or fecal masses were collected monthly and kept under
HF= horn fly; FM= fecal mass laboratory conditions (Barros, 2002). In this study, the samples of fecal

3
L.R.B. Melo, et al.
Table 2
Significant results of the linear correlation analysis between Haematobia irritans biological parameters and climate variables in the municipality of Patos, Paraíba,
from August 2016 to July 2017.
Parameter
Oviposition period until start (1st day) of emergency (days)
Oviposition period to emergency peak (days)
Average emergency period (days)
Average number of HF/FM (total)
Average number of emergency HF/FM
Emergency frequency (%)
masses did not present chronological periodicity but obeyed the bio-
logical rhythm of the species in the region. Since the fecal masses re-
mained in the environment throughout the study period, there was a
continuous and observable correspondence that occurred between the
fecal masses and the collections of the early generation.
Oviposition does not occur immediately after emergence; there is a
need for previous feeding, copulation, and oogenesis. Copulation begins
on the second day after emergence, and on the third day, 93% of fe-
males develop fertile eggs (Beadles et al., 1977). Initial ovipositions are
observed on the third day after emergence (Kuramochi and Nishijima,
1984; Krafsur et al., 1992) and few females at least 4 days old do not
oviposit (Krafsur et al., 1992). Therefore, using a pre-oviposition period
of 4 days after the emergence peak permitted all emerged individuals to
reach sexual maturity, following which a significant majority of females
began the oviposition on the day of fecal mass selection/collection,
which led to the next generation.
On an average, 24.3 flies/fecal mass were obtained from 78% of the
masses in the present study. This value was significantly higher than
that recorded by the Pantanal of Mato Grosso do Sul State (7.1 flies/
fecal mass) (Barros, 2002) and 1.5 pupae/fecal masses in 64.3% of the
Fecal masses (Sereno and Sereno, 1999). The high frequency of horn
fly/fecal mass in the semiarid region could be attributed to higher rates
of infestations observed in the Sindhi herd of the region (Medeiros
et al., 2018) when compared with those in Nelore animals in the Pan-
tanal (Barros, 2001), which has ultimately been associated with a
higher number of ovipositions and adults per fecal mass.
Emergence of males (46.5%) and females (53.5%) was correlated
with the relation (48:52) observed by Kuramochi (2000) from the cattle
collections. Additionally, Macedo et al. (2001) reported a lower fre-
quency of H. irritans males in the field- and laboratory-maintained
cattle feces. The higher frequency of females at the beginning of the
emergence period highlighted their faster rate of development com-
pared with males.
The relatively short period of time (7 days) required for the devel-
opment of H. irritans from an egg to an adult represented one of the
shortest recorded developmental periods for the species in the wild.
This value was formerly observed in the municipality of Boa Vista,
capital of Roraima-RR, few years after the entry of this fly into the
country (Collares, 1990). Under controlled conditions, Palmer et al.
(1981) reported a similar developmental period (7.7 days) from eggs
incubated at 30 °C. This result indicated that rapid development of the
horn fly in the Paraiba semiarid region, with high average temperatures
(28.4 °C) and low thermal amplitude ( ± 3 °C), was recorded during the
study. Despite relatively high temperatures in the Pantanal, the devel-
opment period for H. irritans was shorter than that in the semiarid re-
gion (9 days, temperature range = 27.3 to 30.2 °C) (Barros, 2002). In
addition to the high average air temperature, the strong daily insolation
in the northeastern semiarid (Araújo et al., 2005) was associated with a
further increase the fecal mass temperature, which led to an increase in
the rate of larval development.
The maximum amount of time to start the emergence that occurred
in July (end of rainy season) was consistent with the findings reported
Veterinary Parasitology: Regional Studies and Reports 20 (2020) 100411
Average temperature Average RH
r p r p
−0.6778 < 0.0001 0.4447 0.0138
−0.5978 0.0005 – –
0.6751 < 0,0001 −0.7696 < 0,0001
0.6583 < 0,0001 −0.6973 < 0,0001
0.6299 < 0,0002 −0.6899 < 0,0001
0.6614 < 0,0001 −0.7154 < 0,0001
by Barros (2002) in the Pantanal region; however, the duration in the
semiarid region did not exceed 9 days, at an average temperature of
25.6 °C (24.7–27.8 °C). In the Pantanal (2002), it reached 17 days,
considering the lower average temperatures (19.4 °C). Influence of the
temperature as a factor to determine the duration of immature devel-
opmental was demonstrated for H. irritans by Palmer et al. (1981).
As a consequence of this rapid biological cycle, the horn fly pro-
duced 30 annual generations in the semiarid region, which were sig-
nificantly higher than those previously observed in other regions of the
country. Rodrigues and Marchini (2001) in Piracicaba, State São Paulo,
reported the occurrence of 19.1 annual generations, with complete
development in 2 to 3 weeks under favorable conditions. In the Pan-
tanal, Barros (2002) suggested the occurrence of 22 annual generations,
without the interruption of the biological cycle in winter, during which
the development period nearly doubled in relation to the most favor-
able stations. However, it is imperative to note that the maintenance of
fecal masses in buckets in the laboratory resulted in an increase in the
temperature associated with the external environment and eliminated
the influence of environmental factors including insolation and daily
thermal oscillation.
Considering the high levels of temperature, low thermal oscillation
and high insolation, during the 3-and-a-half years preceding the present
study, a considerable number of generations (average 2.5/month)
promoted infestations for the horn fly in most animals (≥96%) of a
herd of the same property (Medeiros et al., 2018).
H. irritans abundance peaks in the traps (generations 10 and 14)
coincided with the onset of rainfall in the region; however, the in-
creased frequency and intensity of rainfall over the monsoon season
considerably reduced the number of horn flies in the fecal masses.
Barros (2001) and Almeida et al. (2010) reported that the influence of
the high precipitation on the low levels of fly infestations in the animals
was possibly due to the fact that the high amounts of rain destroyed the
fecal mass and created an unfavorable environment for the develop-
ment of the flies. Macedo et al. (2001) reported a reduction in or even
the absence of H. irritans emergence in fecal masses maintained in the
field owing to the heavy rainfall following the placement of emergence
traps, resulting a in sudden reduction in the number of immature and
adult individuals due to partial destruction of fresh fecal masses. Si-
milarly, Bianchin and Alves (2002) reported that the destruction of
fecal masses in pastures due to excessive rainfall (≥100 mm) in the
short space of a few days was ultimately associated with disruption of
the biological cycle of the flies, which was subsequently related to a
reduction in the number of infestations.
In the semiarid environment, higher frequencies of horn flies in the
traps were observed at low humidity (range = 23.3% to 37.0%).
Regarding other biomes, population peaks have been associated with
humidity levels above 70% (usually between 70% and 80%), as ob-
served in the Cerrado (Almeida et al., 2010), Pantanal (Barros, 2001),
and Planalto Catarinense (Souza et al., 2005). In a study on horn fly
population dynamics at an identical site (Nupeárido Farm), infestation
peaks were consistently observed during dry seasons, favored by the
presence of large dams (Medeiros et al., 2018). Large reservoirs
4
L.R.B. Melo, et al.
appeared to influence the climate around them; furthermore, the pre-
sence of such a microclimatic effect, particularly translated by in-
creased humidity and reduced temperature, was proportional to the
proximity of the reservoir (Santos Júnior and Caracristi, 2012).
Therefore, it is possible that the humidity at the study site, situated on
the banks of one reservoir (Jatobá Reservoir) and 3 km from another
(Farinha Reservoir), was higher than that recorded at the climatological
station located 8 km from the site of study. The influence of the local
microclimate could explain the abundance of horn fly in the traps,
despite the low levels of humidity outside the area of influence of the
reservoirs.
An extremely significant negative correlation was noted between
temperature and developmental periods, which indicated that a higher
level of average temperature was associated with a shorter develop-
mental period of the horn fly. This corroborated the results of previous
studies on the influence of this parameter on immature fly development
(Palmer et al., 1981). However, the correlation between RH and de-
velopment of immature fly forms primarily reflected the inversed in-
fluence of temperature. This was in turn negatively correlated with RH,
considering the fact that the rapid rate of forming a superficial crust in
the fecal mass, after the process of egg laying, maintained the high
levels of humidity inside the fecal mass during the short developmental
period of the immatures, which ensured that the immatures were not
remarkably susceptible to the influence of relative humidity.
Similarly, the negative correlation between RH and frequency of
emergent fecal masses, along with the number of flies/fecal mass, could
be considered as demonstrations of the fact that correlation between
variables does not imply causality (Holland, 1986). Both correlations
appeared to be an indirect consequence of increased infestations in
warmer seasons, as observed in the region (Medeiros et al., 2018); ul-
timately, a greater degree of infestations was associated with increased
ovipositions in the fecal masses and, consequently, increased flies/fecal
masses, with an increase in abundance and frequency of emergent fecal
masses.
5. Conclusions
Development of the immature horn fly in fecal masses of cattle
primarily occurs throughout the year in the semiarid region of Paraiba
state, influenced by particular large reservoirs. The high (relatively
stable) temperatures during the year were associated with a short
biological cycle (7 to 11 days), which determined the occurrence of 30
annual generations of this parasite in the region.
The fast, non-parasitic phase and the several generations of horn fly
in the semiarid region predispose to the higher rates of occurrence of
herd infestations and consequent economic loss, while accelerating the
potential selection of populations resistant to insecticide treatments.
Therefore, adoption of proper control measures is recommended only if
necessary.
Ethical statement
The work was approved by the Ethics Committee on the Use of
Animals by the Federal Institute of Education, Science and Technology
of Paraíba, Sousa Campus, Brazil (Approval number, 01250.012779/
2016-83).
Declaration of Competing Interest
The authors declare that there are no conflicts of interest related to
Veterinary Parasitology: Regional Studies and Reports 20 (2020) 100411
the present study.
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