Occurrence and overlapping of pharyngeal hot
flies Pharyngomyia picta and Cephenemyia
auribarbis (Oestridae) in red deer of southern
Spain
I. Ruíz-Martínez & F. Palomares.
Di’par1,nen1 ofParasuology, (Jnivi’rsiij’ oJ(iranada, Unii’ersiiv (‘u,npus ‘La (‘arluja.
Granada 18011, Spain
bEstación Biologica Doñana (QSIQ, .4vda Maria Luisas/n. Sevilla 41013, Spain
(Accepted 17 September 1992)
ABSTRACT
Ruiz Martinez, I. and Palomares, F., 1993. Occurrence and overlapping of pharyngeal bot flies
Pharvngonivia picta and (‘cphenemyia auribarhis (Oestridae) in red deer of southern Spain. I ‘ci.
!‘arasiiol., 47: 119—127.
From I 985 to 1990, 372 red deer ( (ervus elaphus) from southern Spain were examined for larvae
of pharyngeal bot flies Pharyngorn via picla and (‘ephenemyia auriharbis. The infestation was related
to age, sex and intensity of infection. Fawns and adult deer (more than 5 years old) had a significantly
(I’< 0.05) higher prevalence and intensity of infection than younger deer. Conversely, no significant
difference has been noted between sexes. Ninety percent of deer were found to be infested. A simultaneous occurrence of both species was found in 23% of cases, with noticeable differences between
prevalence and intensity of infection (measured in number of bots per head for each species). Quantitative overlapping between P. picla and ( auriharhis seems relative and their biological cycles did
not overlap completely.
INTRODUCTION
The larvae of Oestrids Pharyngomyia and Cephenemyia are widely distributed in the Holarctic region and are commonly found in Cervus, Capreolus,
Alces, Dama, Rangifer, Odocoileus and Ovis (Bennett and Sabrosky, 1962;
Zumpt, 1965). These parasites were cited by Aristotle (Thompson, 1910),
when he wrote, almost certainly describing larvae of Pharyngomyia, “...with­
out any exception stags are found to have maggots living in roots of the tongue
and in the neighbourhood of vertebra to which the head is attached”. Corn(‘orrespondence to: 1. Ruiz Martinez, Department of Parasitology, University of Granada. Universit Campus’La Cartuja’, Granada 18011, Spain.
(
monly called ‘bot fly larvae’ (Cameron, 1932), other authors consider it more
correct to use the term ‘pharyngeal hot flies’ (Bennett, 1962). Under this denomination three species of the genus Cephenemyia and two of Pharyngomyia occur in the Palaearctic region (Zumpt, 1965). However, in southwest
Europe, few data are available on the occurrence of these species and there
are no data on multiple infestation with two or more pharyngeal bot fly species in the same host (Gil Collado et al., 1985; Gutierrez et al., 1991 ). In
addition, these authors carried out necropsies I or 2 days after the death of
hosts, and therefore data may be altered by larval translation.
There are well known cases of Cephenemyia spp. larvae causing extreme
discomfort and/or death in red deer of Minnesota (Fitch, 1928) and California (McLean, 1940). Larvae may occasionally penetrate the skull and enter
the brain, causing pain and death. Normally, Cephenem via or Pharyngom via
infections do not cause death (McMahon and Bunch, 1989), but frequently
cause destruction and dislodge host tissues (Capelle and Senger, 1959; Cogley,
1987).
The present study describes the relationships between prevalence and the
age and sex of the host, parasite localization and the overlapping of instars of
the two species inhabiting the same hosts in southern Spain.
MATERIALS AND METIIOI)S
From 1985 to 1990 during the months of November—March, 372 red deer
(Cervus elaphus hispanicus) (181 females and 191 males) were examined.
Animals were killed on social hunts in the northeastern Sierra Morena mountains (39°30’N, 4°30’E). This area (120000 ha) is composed of private
zones, ‘Sierra de Andujar’ and ‘Despeflaperros’ Natural Parks, in which 3500
red deer are hunted every year.
Heads and necks of deer were cut off, placed in plastic bags and stored in a
freezer until examination (between 1 and 6 h after death). For the parasite
predilection site study, we only used animals dead for no more than 16 h as
larvae (mainly first and second instars) may migrate (Dudzinski, 1970; Sugar,
1976).
Lungs, trachea and broncheal tubes were examined. A mid-sagittal cut was
also made through the skull with a band-saw so as to expose the nasal turbinates, ethmoid olfactory area, retropharyngeal pouches, the mouth and associated muscles. Recovered larvae were registered according to their site of
attachment: (a) esophagic and tracheal area; (b) mouth and palatine area;
(c) nasal and olfactory area (see Fig. I).
Recovered larvae were conserved in vials containing complex fixative medium (RuIz Martinez et al., 1989). They were then examined in the laboratory, and species and instar were identified (Zumpt, 1965; Gil Collado et al.,
1985). Red deer were grouped by sex and age classes of less than 1 year
Fig. 1. Schematic localization of parasites on host’s cavities in zones: (A) esophagic—tracheal
area; (B) mouth and palatar area; (C) nasal and olfactory area. •, P. picta; 0, C. aurebarbis.
(n=80), 1—4 years (n= 128) and more than 5 years (n= 164) for analysis
(Taber and Larson, 1980).
RESULTS AND DISCUSSION
It is commonly accepted that Pharyngomyia picta and Cephenemyia auribarbis may have a joint occurrence in palaearctic red deer (Sugar, 1974; Gil
Collado et a!., 1985), but the nature of this association has not been described, i.e. overlapping between species, localization and seasonality. As
shown in Table 1, prevalence of both species varied with age class, sex and
intensity of infestation. Fawns and adult deer (more than 5 years of age) had
TABLE I
Prevalence of Pharyngomyia picta and Cephenemyia auribarbis in red deer of different sex and age classes
Age
class
(years)
Total no.
of deer
observed
Total no.
infested
<1
1—4
80(21.5)
128 (34.5)
>5
Total
Overall
mean
Total
no. of
larvae
Mean
per
head
Males
78(97.5) 2418
107(83.6) 2037
31.00
19.04
32(16.7)
100(52.3)
30(93.7)
92(92.0)
48 (26.5)
28(15.5)
48(100)
15(53.6)
164(44.1)
150 (91.5) 4575
30.50
59(30.9)
56(94.4)
105 (58.0)
94 (89.5)
372
335(90.0) 9030
Figures in parentheses are percentages.
No.
observed
191
26.85
Females
No.
infested
No.
observed
178(93.2) 181
No. infested
157(86.7)
MONTHLY PREVALENCE
MEAN
BOTS PER HEAD
35-,
30-I
-
X 2695
--
25-1
20
15
A
10
5
A
a
A
—4
NOV
DEC
JAN
‘
FEB
Fig. 2. Monthly prevalence and number of hots per head of red deer in southern Spain. •.
auriharl,is.
I’. picta; A
(‘V
-
significantly (ANOVA, P-<O.05) higher prevalence and intensity of infection
than deer less than I to 4 years of age (differences were smaller between male
age classes). However, there was no significant difference in prevalence and
intensity of infection between sexes (P<O.05).
Although the prevalence rates of these parasites oscillate noticeably with
geographical area and host species, in general with higher levels associated
with host type (see Table 3), the mean number of bots per head obtained in
our study (27) were very similar to those obtained for Cephenemyia spp. in
Odocoileus hemionus (35—36) by Capelle and Senger (1959) and McMahon
and Bunch (1989). It was important to examine recently dead deer (not more
than 18 h) because first instar larvae may be displaced from bronchi and
associated neck muscles (see Sugar, 1974 for P. picta). The intensity of infection obtained by some other authors was lower than in this study (e.g. a mean
of 18.5 bots per head for P. picta was found by Gutierrez et al., 1991). The
high number of bots per head observed in this study (Table 1) is perfectly
correlated with adverse effects associated with the infestation: weight loss
(Dudzinski, 1970) and increased mortality rate (Fitch, 1928; Cowan, 1946).
A joint occurrence of P. picta and C. auribarhis larvae occurred on average
in 23.1% of cases. However, these values varied with the period studied (Fig.
2). Analysis of the monthly variation of mean bots per head of both species,
revealed that the rate of overlapping was very low (Fig. 2). For example, in
November, 50% of red deer heads were parasitized by larvae of C. auriharhis
123
30
20
10
20
A
•
L liii
A
•
L III
70-E
60
a
50
2010-
A
L III MATURE
90
80706050
A
40
U
302010
P
PUPA
50
A
302010
NÔAI
DEC
isN
FEB
Fig. 3. Proportion of instars and inter-instars during the study period.
C. aurtharbis.
P. picta; A.
and 98% by P. picta, but their intensity of infection varied from 25.4 bots per
head for P. picta and 4.6 bots per head for C. auribarbis.
There was little coincidence between developmental instars of both species
(Fig. 3). While in November—January most of the C auribarbis found were
mature third instar larvae, only half of the total number of P. picta observed
was at the same stage. From January to March, C. auribarbis pupated and P.
picta maintained development of its third instar. An apparently Continuous
infection was maintained by the extended maturation period of P. picta
(Sugar, 1976) while the maturation period of C. auribarbis was much shorter
(Cameron, 1932; Gil Colladoet al., 1985). Consequently, C. auriharbis, with
46% having pupated by December (Fig. 3), may undergo pupal diapause and
I 24
FABLE 2
Frequency
(%) of parasite developmental Instars in hosts’ cavities
P picla
No. of larvae
I ocalizalion
Area (a)
Area (h)
Area (c)
( . aurz/arhg.s
No. of larae
L
I2
1 + I.
L
785
448
45
422()
145
3360 (72.4)
29 (0 6)
746 (16.6)
29) 1254)
23 (20)
)3I (72.6)
74()
514(65.91 236(527) 370(74.7)
129(16.4)
8 (4.0)
35 (7.1)
42 ( Ill I
94 (43.3)
(I 2)
L 1—mature
Pupae
3)
Iotal
3() fl
7() ( 61) 7)
301
Locahiation
Area (a)
Area (l)
\rca (ç)
I) (
40 (33.0)
6 (5.0)
75 (62.0)
44(338)
((L(
85 (65.4)
SI (648)
(9 6)
622(840)
(0.3
32 (25.6)
I 6 (I 5.5
219 (72.S
(71
‘Differences between total larvae recos ered and total tars ae in this table, larvae unlocated or located in other
areas not considered.
‘Set’ Fig. I for delinition of areas (a). (hI and Ccl.
P. picta with a long maturation period may pupate from mid-April to May.
Via oral infestation (Cogley and Anderson, 1981 ), they establish themselves
in their hosts from May to October. In our study, only first instar larvae of P.
picta were recovered with varying levels of’ intensity from November to March.
No first instars of C. auriharbis were found in this period. Our observations
agreed with those of Gil Collado et al. (1985). Gutierrez et al. (1991), Sugar
(1976) and Cameron (1932) who claimed that the newly established larvae
first appear from late May to mid-July.
Both species were found in the hosts’ cavities (Table 2); however, no significant variation was observed between differing geographical zones. Similarly, there were no differences in the predilection sites (parasite localization) of larvae of these two species (Table 3). Thus, we agree with Bennett’s
(1962) use of the name pharyngeal bot fly: in our study 64% of larvae were
observed in the esophagic and tracheal area, while 27% were found in nasal
and olfactory areas (Fig. 1). McMahon and Bunch (1989) observed that 77%
of C’ephenemyia spp. were found in the tracheal fold immediately posterior
to the epiglottis and corniculate cartilages. The numerous larvae feeding on
the esophago—tracheal area may produce damage to host tissues by their oral
hooks and cuticular spines (Cogley, 1987), with the resultant effect of weight
loss (Dudzinsky, 1970) and finally death (Fitch, 1928; Cowan, 1946; Cheatum, 1951). We think that these effects (death) may be rare, because the
effect of parasite infections is not always a reduction in host abundance
(Washburn et al., 1991).
McMahon and Bunch (1989) stated: “...abnormal pupation was also observed within several mule deer, which could be in response to adverse envi
TABLE 3
Geographic variation of prevalence in Pharin,mniiu and (ephenemria infi.station
Parasite
Host(s)
Presaleiice
(%)
Locality
Ref.
(aurtharhis
(ervus c/up/m3
Cephenernv,a
Odocoileus hc,nionus
C. jell i’soni
Pharvngoiu via c!a
C’. phoinfera
C sumulutor
(.sizmuIaror
(‘ephenemi’ia
Pharingom via picra
C’. auriharhis
Phari’ngornv,apicia
C aurt,arh,s
Odocoilezo hctiiionu
(ervuc i’Iapliu.
100
25
75
IOU
62
49
86
74
5—13
80—90
97
97
100
58
IOU
89
91)
Scotland, UK
New York. USA
Montana. USA
Ols7tyn, Poland
Cameron, 1932
(‘heatum. 1951
(‘apelle and Senger. 1959
Phari’ngo,n ito
C’. auriharbe
(‘ephenenn’ia
ff110
I’hari’ngotnvia picla
I’hari’ngonn’iu pub
C’. auriharhis
0. rirginianu.s
(‘apreolus caj,rcolus
(‘apreolus caj,reolus
0. i’irginianus
(‘ervu, Dama. Capreotus
Ccrrus, Dama, (‘apreolu’,
(i’ri’u.’, elaphio
(‘eri’io e/ctp/uc
(ervu.’, elaphus, Datna dania
(ervus elai,hus. I)a,na dania
Odocoileus heititonu.’,
(‘cr1113 c’Iaplius
(‘er,’us elaphus
(‘errus claphus
24
Ontario. Canada
Diverse. Czcchosl.
I)ivcrse. Poland
Texas. USA
Budakeszi, Hungary
Budakesii, I 1ungar
Diverse. Hungary
Diverse, Hungary
Toledo, Spain
Toledo. Spain
Utah. USA
Córdoba, Spain
Jaén. Spain
Jaën. Spain
Drozdi. 1961
Bennett. 1962
Dyk. 19651
Dud7inski, 1970
Samuel ci al.. 19712
Sugar. 1974
Sugar, 1974
Sugar. 1976
Sugar. 1976
Gil Collado et al.. 1985
Gil Collado Ct al., 1985
McMahon and Bunch. 1989
c;uticrrcz ci al.. 1991
This study
This study
‘In 1)udiinski (1970).
2ln McMahon and Bunch (1989).
cM
ronmental conditions whereby third instars increase their chance of survival”. In contrast, Drozdz (1961) and Cameron (1932) concluded that
pupae of C. auribarbis and P. picta can exit the host in fecal pellets. Gil Collado et al. (1985) concluded that this is true for C. auriharhis and invalid for
P. picla. Our observations (Table 2) confirmed the latter assumption. There
is evidence that 73% of pupae of C’. auriharhis were situated in the esophago—
tracheal area, while 69% of P. picla were located in the nasal—olfactory area.
These observations do not oppose McMahon and Bunch’s opinion, and we
think that pupae located in the esophago—tracheal area with puparium formed
have increased chances of survival.
\CKNOWI.ED(iMENTS
The authors wish to thank Isidro Prados, Grabriel Laguna and Alejandro
Reina for advice and collaboration in capturing and sampling deer, especially
José A. Vacas. We extend our gratitude to Dr. Francisco Fuertes for the dissections and necropsies. The work was supported by postdoctoral grants of
CSIC (F.P.) and Granada University (I.R.M.).
REFERENCES
Bennett, (;.F.. 1962. On the biology of (‘ephcncmvia photo/era (l)iptera: Oestridae). the pharyngeal hot of the white-tailed deer Odocoileus virginianuc. Can. J. Zool.. 40: 1195—1210.
Bennett. (i,F. and Sabrosky. C.W.. 1962. ‘l’he nearctic species of the genus (‘ephcncnn’iu (Diptera: Ocstridae). Can. J. Zool.. 40: 43 1—448.
Cameron, AL., 1932. The nasal bot fly. (‘ephenemi’ia aurtharhis Meigen (Diptera. lachinidae)
of the red deer. (‘ervus elajthus L. Parasitology. 24: 1 85—195.
(‘apelle. K.J. and Senger, CM.. 1959. Occurrence of(‘ephenemi’ia )e//I’sonl in a sample of Montana Mule deer. J. Parasitol., 45: 32.
(‘heatum. EL.. 1951. Disease in relation to winter mortality of deer in New York. J. Wildi.
Manage.. 15: 216—220.
(‘ogley. T.P.. 1987. Effects of (‘ephenemi’ia spp. (Diptera: (.)estridae) on the nasopharynx of
black—tailed deer ( Odoco,/eu.c he,nionu.s i’olunibianits). J. Wildl. Dis., 23: 596—605.
(‘ogley. TY and Anderson. JR.. 1981. Invasion of black-tailed deerhv nose hot fly larvae (I)iptera’. Oestridae). tnt. J. Parasitol.. 11(4): 28 1—286.
Cowan, 1.McT.. 1946. Parasites, diseases, injuries and anomalies of the columbian black-tailed
deer. Odo(m/i.’us hemionus co/unthianus Richardson, in British (‘olunibia. (‘an. J. Re.. 24:
7 1-103.
l)rozd,. J.. 1961. New data from biology of Phart’ngomi’ia ptcw Meig.. larvae (Diptera’. Oestridae) C’eri’us elaplius parasite. Wiad. Parazytol.. 7(2)’.373—379.
Dud,inski, ‘N.. 1970. Studies on (‘ephenem via stimulator (Clark) (Diptera: Oestridae). the
parasite of the European roe-deer (‘apreolus capreolus. II. Invasiolog..•\cta Parasitol. Pot..
18: 573—592.
Fitch. (‘P.. 1928. A preliminary note on the occurrence of a head and throat hot in the wild
deer ((‘erl’u.s i’trç’inianu.c) of Minnesota. Cornell Vet.. 18: 235—357.
Gil Collado, J.. Valls, J.L. and Fierro dc Riva, Y., 1985. Estudio de las larvas de Oestridae
parasitas de Cervidae en España. Bol. Soc. Port. Entomol. (Suppi. I), 1985: 467—475.
Gutierrez, P.N., Ruiz, P., Tavira, C., Martinez Cruz, S. and Becerra, C.. 1991. Morfologia, preyalencia e incidencia de Pharvngornyia picra en el ciervo (Genus elaphu.c) de Sierra Morena.
In: S. Mas Coma, J.G. Esteban, M.D. Bargues, M.A. Valero and M.T. Galán-Puchades, (Editors). ICASEP-1, Parasitology in the Southwest Europe. Valencia, 325 pp.
McLean, D.D., 1940. The deer of California. Calif. Fish Game, 26: 159—160.
McMahon, D.C. and Bunch,T.D., 1989. Bot fly larvae (Qephene’nria spp., Oestridae) in Mule
deer (Odocoileusheinionus) from Utah. J. Wildl. Dis., 25(4): 636—638.
Ruiz-Martinez, I., Soler-Cruz, M.D., Pérez-Jimënez, J.M. and Diz-LOpez. M., 1989. Preparation ofdipteran larvae for scanning electron microscopy, with special reference to myiasigen
dipteran species. Scanning Microsc. Int.. 3(l): 387—390.
Sugar. L.. 1974. The occurrence of nasal throat bot flies (Oestridae) in wild ruminants in Hungary. Parasitol. Hung., 7: 18—189.
Sugar. L., 1976. Seasonal incidence of larvae of Pharvngornyia picra (Meigen) 1824 and Cephenein via aurtharhis (Meigen) I 824 (Oestridae) in red deer (Cervus elaphus hippelaphus) in
Hungary. Parasitol. Hung., 9: 73—84.
Taber, R.D. and Larson, J.S., 1980. Criteria of sex and age. In: S.D. Schcmnitz (Editor), Wildlife Management Techniques Manual. Wildlife Society, Washington. DC, pp. 143—202.
Thompson, D.A., 1910. The works of Aristotle. Vol. lii. The Clarendon Press, Oxford. pp. 50—
63.
Washburn, J.O., Mercer, D.R. and Anderson, J.R., 1991. Regulatory role of parasites: impact
on host populations shifts with resource availability. Science, 253: 185—188.
Zumpi, F., 1965. Myiasis in Man and Animals in the Old World. Buiterworths, London. 267
pp.