97
House
Fly (Musca
domestica)1
Parasites
(Hymenoptera:
Pteromalidae)
Associated
with Poultry
Manure
in North
Carolina2
DONALD A. RUTZ AND RICHARD C. AXTELL
Dept. of Entomology, North Carolina State Univ., Raleigh 27650 ABSTRACT
Environ. Entomol. 9 : 175-180 (1980)
A comprehensive 12-mo. survey of indigenous house fly parasites was conducted in the 3 geographic regions of North Carolina. Eight parasite species, Muscidifurax raptor Girault and Sanders, Spalangia cameroni Perkins, S. endius Walker, S. nigra Latreille, S.
nigroae-nea Curtis, S. n. sp. nigroae-near drosophilae, Pachycrepoideus vindemiae (Rondani), and Nasonia vitripennis Walker were found. M. raptor was the most abundant parasite collected and the
only species active throughout the year. S. cameroni, S. endius and S. nigroaenea, active from June through Nov., were the prevalent Spalangia species. A discussion of collection techniques is included.
A major pest problem of the poultry industry is flies,
primarily the house fly Musca domestica L., and this is
the most acute in caged-layer operations. Problems
as-sociated with a unilateral approach to fly control in
caged-layer poultry operations have generated
consider-able interest in the development of integrated fly
man-agement programs (Axtell 1968, 1970a,b, Legner and
Dietrick 1974) with emphasis on biological control,
par-ticularly parasitic wasp releases (Morgan et al. 1975,
Olton and Legner 1975, Pickens et al. 1975).
Knowledge of indigenous parasites and their effect on
fly populations within a geographic region is essential
for the development and assessment of the biological
component of an integrated fly management program
suited to that region. This information provides baseline
data for determining the effect of enhancement of
indig-enous parasite populations through cultural practices or
future mass releases of indigenous or possibly exotic fly parasites.
Therefore, a comprehensive survey of the occurrence,
relative abundance and seasonal abundance of
indige-nous house fly parasites was conducted in the 3
geo-graphic regions of North Carolina.
Methods and Materials
This survey included the Coastal Plain (Craven and Lenior Co.), Piedmont (Chatham, Orange and Alam-ance Co.) and Mountain (Wilkes and Davie Co.) regions of North Carolina.
The Coastal Plain is a nearly level area extending in-land from the Atlantic Ocean an average of 200 km. This region has an average annual temperature of 17°C; av-erage annual precipitation of 112-142 cm and a freeze-free season ranging from 200-280 days. The Piedmont is essentially a plateau of rolling hills, ranging in eleva-tion from 46-305 m. In the Piedmont, annual tempera-tures average 15°C, with 112-122 cm annual precipita-tion and a freeze-free season of 200-220 days. The Mountain region with elevations ranging from 305-1828 m is marked by numerous peaks, valleys and cross chains of mountains. The mountains have a 150-200 day freeze-free season with average annual temperatures of
, Diptera: Muscidae.
2 Paper No. 5937 of the Journal Series of the North Carolina Agric. Res. Serv., Raleigh. Received for publication Mar. 19, 1979.
'1)1980 Entomological Society of America
10°-15°C and an average of 102-203 cm annual precip-itation.
Five farms in each of the 3 regions were visited
monthly from May 1977 to Apr. 1978. Three types of
caged-layer poultry houses were included in the survey:
narrow California type, wide span and high rise (Pied-mont region only). Narrow California type houses were open-sided structures (30-90 m long X 3 m wide; 1500-5000 bird capacity) with one row of 2-tiered wire
stair-step cages, 2 or 3 birds/cage, suspended 1-1.5 m above
a dirt floor and running the length of the house along each side of a single concrete aisle. Wide span houses
were either open-sided or closed-sided (controlled
envi-ronment, fan ventilated) structures, 60-90 m long X
6-9 m wide with a bird capacity of 8000--12000. These
houses had one row of 2-tiered wire stairstep cages, 2 or
3 birds/cage, suspended above a dirt or concrete floor
and running the length of the house along each side of
3-4 concrete aisles. High rise houses, sometimes
re-ferred to as deep pit houses, were 2 story structures,
either open-sided or closed-sided (controlled
environ-ment), 122-152 m long X 9-12 m wide with a
20,000-25,000 bird capacity. Birds were held on the 2nd story
in rows of 3 or 4-tiered wire stairstep cages (2 or 3 birds/ cage) which ran the length of the house along each of 3-4 wooden aisles. The 1st floor was used for manure ac-cumulation.
Pupal bags and pupal samples were used to monitor
parasite populations. Each pupal bag (14 mesh screen)
contained 25 laboratory-reared house fly pupae« 1 day
old). On each farm 10 bags were left for 7 days/mo on the periphery of the manure at a depth of 5-10 cm where fly pupation was likely to take place. Manure in most situations was quite wet resulting in a concentration of shallow pupation sites (5-10 cm deep) in the drier areas at the periphery of the manure. Samples of naturally oc-curring house fly pupae (ca. 100-500 pupae/sample; 10 samples/farm) were also collected monthly from the manure. Pupae from the pupal bags and naturally occur-ring pupae were held in the laboratory for ca. 45-60 days at 27°C and 60 ::!:10% rh to allow time for parasite development and emergence.
Parasites were identified with keys (Boucek 1963, Kogan and Legner 1970, Legner et al. 1976) and by comparison with specimens identified by E.F. Legner
175
176 ENVIRONMENT AL ENTOMOLOGY Vol. 9, no. 2
(Div. of Biological Control, Dniv. of Calif., Riverside). Representative identified material of Spalangia spp. was confirmed by Z. Boucek (British Museum of Natural History).
Results and Discussion
Eight species of house fly pupal parasites were found. These included: Muscidifurax raptor Girault and Sand-ers, Spalangia cameroni Perkins, S. n. sp. near
droso-philae, S. endius Walker, S. nigra Latreille, S. nigroae-nea Curtis, Pachycrepoideus vindemiae (Rondani) and Nasonia vitripennis Walker. M. raptor, P. vindemiae,
and N. vitripennis are considered cosmopolitan. Of the remaining species, S. cameroni and S. nigroaenea have not previously been reported from North Carolina. (E.E. Grissell, NMNH, pers. comm.).
Relative abundance and seasonal abundance of house fly pupal parasites recovered by the pupal bag collection technique in the 3 geographic regions of North Carolina are presented in Table 1. M. raptor was the most abun-dant parasite recovered statewide. S. cameroni and S.
endius were the most abundant Spalangia species found
in the Coastal Plain and Mountain region. In the Pied-mont, S. cameroni was the predominant Spalangia spe-cies collected. P. vindemiae was abundant throughout the state in the pupal bag "Collections,ranking 2nd in overall relative abundance in the Coastal Plain and 3rd in the Piedmont and Mountain regions. Two specimens of Spalangia n. sp. near drosophilae were collected in the Piedmont region during June.
With regards to seasonal abundance (Table 1), M.
raptor was the only parasite species recovered
through-out the year. M. raptor showed little variation in sea-sonal abundance in the 3 geographic regions other than being more prevalent during the warmer months.
Spa-langia species were generally collected from June through
Nov. In the high rise houses, sampled only in the Pied-mont, Spalangia were collected over a longer period. This lengthened period of Spalangia activity was prob-ably due to the comparatively warmer temperatures within this house type, generated by the large amounts of decomposing manure and also by the large number of chickens present. S. cameroni was more prevalent dur-ing late summer and fall while S. endius and S.
nigroae-nea were more abundant during the summer. P. vinde-miae showed considerable regional variation in seasonal
abundance. In the Coastal Plain, P. vindemiae was col-lected from May through Nov. and Mar. P. vindemiae was recovered during June through Aug., Oct., Mar., and Apr, in the Piedmont; however, in the mountains, this parasite was collected only in June and Aug.
Parasite activity, as indicated by parasitism rates, was greatest from June through Nov. in all geographic re-gions (Table 1). Parasitism during these months aver-ages 25.6, 26.5, and 17.1%/mo in the Coastal Plain, Piedmont, and Mountain regions, respectively.
M. raptor was also the most abundant parasite
re-covered from naturally occurring house fly pupae col-lected in the 3 geographic regions of North Carolina (Table 2). M. raptor accounted for 47.4, 62.2, and 59.2% of all parasites emerging from pupae collected in the Coastal Plain, Piedmont, and Mountain regions,
re-spectively. S. cameroni, S. endius, and S. nigroaenea
were the most abundant Spalangia species collected
throughout the year. Statewide, the mean relative
abun-dance of S. cameroni ranged from 9.3-22.3%; S. endius
ranged from 1.9-15.9%; and S. nigroaenea ranged from
13.5-25.3%. Infrequent small numbers of S. nigra and
P. vindemiae were also collected.
The overall relative abundance of Spalangia was higher from field collected pupae than from laboratory-reared pupae placed in the field (pupal bags). Legner (1967) claimed that M. raptor parasitized more pupae near the
surface of the manure, while Spalangia, were active
deeper in the manure. Although deep manure (coning)
was not common at the sample sites, it is possible that
loosening of the manure during pupal bag positioning
facilitated attack by M. raptor and P. vindemiae and
re-sulted in an increase in their relative abundance and a
corresponding decrease in Spalangia relative abundance
in the pupal bag collections. Another possible
explana-tion is that Spalangia species, particularly S. endius,
may have avoided lower house fly pupal densities
(pu-pal bags) in preference for higher densities (Ables and
Shepard 1974a, Legner 1967) of naturally occurring
house fly pupae.
Sex ratios of the 4 prevalent house fly pupal parasites
favored females (Table 3). Furthermore, collections made
during the cold months tended to contain a greater
per-centage of females than collections made during warm
months.
Morgan and Patterson (1975) reported that M. raptor
was the most prevalent house fly parasite collected in
Florida with S. nigroaenea and P. vindemiae also being
quite common. In South Carolina, Ables' and Shepard
(1974b) reported that S. nigroaenea was the most
abun-dant and M. raptor o~e of the least abunabun-dant house fly
parasites collected. After an additional year of
monitor-ing, however, Ables !md Shepard (1976) concluded that
M. raptor was one of the 3 predominant house fly
para-sites in South Carolina along with S. nigroaenea and S.
endius. Furthennore, the biweekly pupal sample collec-tion data presented by Ables and Shepard (1976) showed that M. raptor was the most abundant house fly parasite
recovered from mid-July through Nov. with the
excep-tion of one collecexcep-tion date. Their initial conclusions
were based primarily on emergence trap collections
sup-plemented by biweekly pupal samples. Our. experience
with emergence traps indicated that the traps favored the
collection of Spalangia which appeared more
photopo-sitive thanM. raptor and could explain the low numbers
of M. raptor initially reported in South Carolina. The
smaller numbers of M. raptor collected by Ables and
Shepard (1976) with emergence traps than from their
pu-pal sample collections in the same poultry houses
sup-ports our observation. In addition to emergence traps
fa-voring collection of Spalnagia, we encountered several
other problems which made the traps impractical for
sur-vey purposes. Trap positioning was very important for
if the traps were not placed over concentrations of fly
pupae in the manure, few parasites were recovered. The
traps were also very susceptible to wind and large
accu-mulations of manure which necessitated trap cleaning
;I> ~
-'l)
00
0
Table I.-Relative abundance and seasonal abundance of parasitic Hymenoptera that emerged from laboratory-reared house fly pupae exposed in pupal bags in poultry manure in the three geographic regions of North Carolina (May 1977-Apr. 1978).
% relative abundance (seasonal abundance)a.b
Species May June July Aug. Sept. Oct. Nov.
<::
Coastal Plain -IN
Muscidifurax raptor 80.0 ( 9.0) 75.0 (13.2) 75.6 (23.6) 75.8 (20.9) 75.1 (16.7) 84.9 (12.4) 76.2 (10.3) i<'
Spalangia cameroni 3.6 (10.1) 0.7 ( 3.4) 10.6 (46.1) 8.9 (30.3) 2.0 ( 4.5) 3.3 (5.6) ;I>
S. endius 14.9 (38.1) 10.0 (45.4) 3.9 (15.5) 0.3 ( 1.0) ><-I
S. nigroaenea 5.6 (53.8) 1.8 (30.8) 0.2 (3.9) 1.0(11.5) tT1t""
Pachycrepoideus vindemiae 20.0 ( 1.4) 0.8 ( 0.9) 11.8 (23.8) 9.5 (17.0) 14.7 (21.1) 13.1 (12.4) 20.5 (22.9) t""
% parasitismd 1.5 20.9 35.1 31.7 26.6 19.1 19.9 ::I:
0
Piedmont <::
M. raptor 98.7 (11.6) 98.1 (18.5) 92.6 (25.2) 80.0 (17.4) 53.1 ( 8.7) 90.9 ( 9.7) 80.0 ( 3.9) C/JtT1
S. cameroni 0.3 ( 0.4) 1.9 ( 3.9) :0.8 (17.9) 45.3 (56.4) 1.9 ( 1.6) 20.0 ( 7.4) t""""'
S. endius 0.3 ( 3.1) 4.3 (71.9) 1.6 (15.6) -<
S. nigroaenea 1.3 (33.3) 0.2 (11.1) 1.2 (55.6) "t:I
P. vindemiae 1.4 ( 6.2) 0.9 ( 6.2) 8.0 (41.9) 7.2 (18.5) >::0
% parasitism 18.3 30.7 42.4 34.6 26.7 17.3 7.6 >C/J
Mountains :jtT1
M. raptor 100.0 ( 7.5) 28.3 ( 3.5) 90.7 ( 8.5) 88.6 ( 22.6) 86.4 (16.8) 99.3 (26.0) 74.1 (10.8) C/J
S. cameroni 6.5 (11.1) 6.4 (11.1) 7.8 ( 27.2) 5.6 ( 8.6) 21.0 (42.0)
S. endius 16.7 (43.4) 2.9 ( 7.5) 2.1 ( 11.3) 8.0 (18.9) 0.7 ( 3.8) 4.9 (15.1)
S. nigroaenea 1.1 (100. )
P. vindemiae 48.5 (98.5) 0.4 ( 1.5)
% parasitism 8.0 14.0 12.7 25.6 10.4 26.4 13.5
Table l.-(Continued)
--.J 00
% relative abundance (seasonal abundance)a,b
Species Dec. Jan. Feb. Mar. Apr.
Coastal Plain Muscidifurax raptor Spalangia cameroni S. endius
S. nigroaenea
Pachycrepoideus vindemiae % parasitismd
100.0 (0.1) 66.7 ( 0.1) 100.0 ( 0.8)
100.0 (1.1)
0.0 0.1
1.0
Piedmont
M. raptor
S. cameroni S. endius S. nigroaenea
P. vindemiae
% parasitism
66.0 (2.6) 30.0 (8.9) 4.0 (9.4)
100.0 (0.4) 100.0 (0.5)
6.7 0.7 0.9
Mountains
M. raptor
S. cameroni S. endius S. nigroaenea
P. vindemiae
% parasitism
100.0 (0.6) 100.0 (0.7)
1.0 0.0 1.3 0.0 7.3
,Relative abundance values are that species percentage of the total number of parasites (all species) collected each month from 1250 exposed pupae in each of 3 regions (25 pupae/bag, 10 bags/farm, 5 farms/region! month).
h Seasonal abundance values are the percentage of the total 12-mo collection of that species recovered during that month.
CRelative abundance means are based on the total number of parasites collected over the 12-mo survey period; parasitism means are based on parasitism data from June through Nov.
d Percentage of exposed house fly pupae from which adult parasites emerged.
;;
33.3 ( 0.5)
0.3 1.1
33.3 ( 0.3) 53.7 ( 1.1)
22.0 ( 3.5)
66.7 (14.8) 24.3 (12.4)
1.8 4.4
100.0 ( 3.0)
Total
Meanc No. collected
76.6 1407
4.8 89
5.3 97 t!1
1.4 26 Z
11.9 218 -<
25.6 0
Z
83.7 1947
.
t!1Z11.0 257
""
:»1.4 32
t-0.4 9 t!1
3.5 81 Z""
26.5 0
0
t-84.0 1108 0p
6.6 87 -<
4.0 53
0.2 3
5.2 68
Table 3.-Sex ratios of the 4 prevalent house fly pupal parasites associated with poultry manure in North Carolina (May 1977-Apr. 1978).
Species
Muscidifurax raptor Spalangia cameroni S. endius
S. nigroaenea
, Based on the total number of parasites collected by both pupal bag (25 labo-ratory-reared pupae/bag, 10 bags/farm, 5 farms/region/month) and pupal sample (ca. 100-500 naturally occurring pupae/sample, 10 samples/farm, 5 farms/region/month) collection techniques in all 3 geographic regions of North Carolina.
nigroaenea, the more prevalent species found in North
Carolina, have previously been reported as the prevalent
house fly parasites in the Eastern Hemisphere (Legner
and Olton 1968) and Western Hemisphere (Legner et a!.
1967) .
Previous house fly parasite surveys used only one or
possibly 2 survey methods which may have tended to
collect certain parasite species over others and possibly even missed certain parasites in an area. In our survey,
for example, S. n. sp. near drosophilae was only
col-lected by pupal bags and S. nigra in the Piedmont and
Mountains was collected only by pupal samples.
Gen-erally, we found that M. raptor was readily collected by
both pupal bag and pupal sample survey techniques;
however, the pupal sample technique produced
rela-tively more Spalangia while the pupal bags collected
more P. vindemiae. Therefore, a combination of both
pupal bag and pupal sample survey techniques are rec-ommended for monitoring house fly parasites.
Based on our data, M. raptor was the only parasite active throughout the year and the most abundant species collected in all geographic regions of North Carolina. Together,S. cameroni, S. endius andS. nigroaenea, the most prevalent species of Spalangia, were less abundant than M. raptor. Generally species of Spalangia have been favored candidates for use as biological agents for house fly control (Legner 1967, 1977). However, as pointed out by Legner (1977), generalizations about par-asite effectiveness for fly control is risky due to great variations in the adaptations of various strains to differ-ent environmdiffer-ental conditions. Since M. raptor is well adapted to habitat and climatic conditions in North Car-olina, this parasite appears to be a promising biological fly control candidate and should be considered for mass rearing and release in integrated fly management pro-grams.
Acknowledgment
We thank T.D. Edwards of this laboratory for his as-sistance in conducting the field work and Dr. E.F. Leg-ner, Div. of Biological Contro, Univ. of Calif., River-side and Dr. Z. Boucek of the British Natural Museum, London for their help in identification of specimens.
REFERENCES CITED
Ables, J. R., and M. Shepard. 1974a.Responsesand com-petition of the parasitoids Spalangia endius and
Muscidi-April 1980 RUTZ & AXTELL: HOUSE FLY PARASITES 179
Table 2.-Relative abundance of parasitic Hymenoptera that emerged from naturally occurring house fly pupae collected
from poultry manure in the 3 geographic regions of North Carolina (May 1977-Apr. 1978).
% relative abundance"
May June July Aug. Sept. Oct. Nov. Dec.-Apr. Meanb
Coastal Plain
Muscidifurax raptor 78.9 47.3 52.9 84.7 32.1 51.0 25.4 15.4 47.4
Spalangia cameroni 12.9 6.8 2.9 4.6 25.0 42.4 69.2 16.7
S. endius 15.1 15.8 3.1 12.0 1.0 6.7 10.2
S. nigra 0.1 0.1
S. nigroaenea 21.1 24.7 24.0 8.2 51.3 23.0 25.3 15.4 25.3
Pachycrepoideus vindemiae
.
0.5 1.0 0.3Total parasites collected 38 93 1235 413 368 200 834 13
Piedmont
M. raptor 66.0 96.8 49.4 57.1 63.4 0.9 34.7 32.4 62.2
S. cameroni 6.5 1.1 20.4 28.6 32.4 66.1 54.8 16.2 22.3
S. endius 7.0 0.6 3.8 4.2 4.1 1.9
S. nigra 0.2 0.1
S. nigroaenea 20.5 1.3 30.2 10.5 33.0 10.5 47.3 13.5
Total parasites collected 415 833 172 133 71 230 409 74
Mountains
M. raptor 64.0 10.3 64.1 66.9 48.1 35.5 62.8 97.2 59.2
S. cameroni 12.0 31.0 3.8 11.8 3.5 5.5 19.2 2.8 9.3
S. endius 24.2 24.3 13.9 21.9 6.4 9.0 15.9
S. nigra 3.5 0.4 0.1
S. nigroaenea 16.0 31.0 7.4 7.4 23.9 52.6 9.0 15.0
P. vindemiae 8.0 2.6 0.5
Total parasites collected 25 29 733 1224 694 327 586 36
.
Relative abundance values are that species percentage of the total number of parasites (all species) recovered each month from ca. 5000-25,000 pupae ineach region(ca. 100-500 pupae/sample. 10 samples/farm, 5 farms/region).
b Based on the total number of parasites collected over the 12-mo survey period.
% females a
May-Oct. Nov.-Apr. Mean
58.2 63.4 58.9
60.9 64.5 62.5
59.4 63.4 59.8
180 ENVIRONMENTAL ENTOMOLOGY Vol. 9, no. 2
furax raptor (Hymenoptera: Pteromalidae) at different densities of house fly pupae. Can Entomol. 106: 825-30. Ables, J. R., and M. Shepard. 1974b. Hymenopterous
par-asitoids associated with poultry manure. Environ. Ento-mol. 3: 884-6.
1976. Seasonal abundance and activity of indigenous hymen-opterous parasitoids attacking the house fly (Diptera: Mus-cidae). Can. Entomol. 108: 841-4.
Axtell, R. C. 1%8. Integrated house fly control: populations of fly larvae and predaceous mites, Macrochles muscado-mesticae, in poultry manure after larvicide treatment. J. Econ. Entomol. 61: 245-9.
19703. Integrated fly controt program for caged-poultry houses. Ibid. 63: 400-5.
1970b. Fly control in caged-poultry houses: Comparison of larviciding and integrated control programs. J. Econ. En-tomol. 63: 1734-7.
Boucek, Z. 1%3. A taxonomic study in Spalangia Latr. (Hy-menoptera, Chalcidoidea). Acta Entomologica Musei Nat. Pragae 35: 429-511.
Kogan, M., and E. F. Legner. 1970. A biosystematic revision of the genus Muscidifurax (Hymenoptera: Pteromalidae) with descriptions of four new species. Can. Entomol. 102: 1268-90.
Legner, E. F. 1%7. Behavior changes the reproduction of
Spalangia cameroni, S. endius, Muscidifurax raptor and Nasonia vitripennis (Hymenoptera: Pteromalidae) at in-creasing fly host densities. Ann. Entomol. Soc. Am. 60: 819-26.
1977. Temperature, humidity and depth of habitat influenc-ing host destruction and fecundity of muscoid fly para-sites. Entomophaga 22: 199--206.
Legner, E. F., and E. I. Dietrick. 1974. Effectiveness of su-pervised control practices in lowering population densities of synanthropic flies on poultry ranches. Entomophaga 19: 467-78.
Legner, E. F., and G. S. Olton. 1%8. Activity of parasites from Diptera: Musca domestica, Stomoxys calcitrans and species of Fannia, Muscina and Ophyra n. At sites in the Eastern Hemisphere and Pacific Area. Ann. Entomol. Soc. Am. 61: 1306-14.
Legner, E. F., E. C. Bay, and E. B. White. 1%7. Activity
of parasites from Diptera: Musca domestica, Stomoxys calcitrans, Fannia canicularis and F. femoralis at sites in the Western Hemisphere. Ibid. 60: 462-8.
Legner, E. ;"., I. Moore, and G. S. Olton. 1976. Tabular
keys and biological notes to common parasitoids of syn-anthropic Diptera breeding in accumulated animal wastes. Entomol. News 87: 113-44.
Morgan, P. B., and R. S. Patterson. 1975. Field parasitiza-tion of house flies by natural populaparasitiza-tions of Pachycrepo-ideus vindemiae (Rondani), Muscidifurax raptor Girault and Sanders and Spalangia nigroaenea Curtis. Florida En-tomol. 58: 202.
Morgan, P. B., R. S. Patterson, G. C. La Brecque, D. E. Wiedhaas, A. Benton, and T. Whitfield. 1975. Rearing and release of the house fly pupal parasite Spalangia
en-dius Walker. Environ. Entomol. 4: 609-11.
Olton, G. S., and E. F. Legner. 1975. Winter inoculative releases of parasitoids to reduce house flies in poultry manure. J. Econ. Entomol. 68: 35-8.
Pickens, L. G., R. W. Miller, and M. M. Centala. 1975.
Biology, population dynamics, and host finding efficiency of Pachycrepoideus vindemiae in a box stall and a poultry house. Environ. Entomol. 4: 975-9.
Reprinted from the