Asphondylia
websteri Felt 1917 (Diptera:
Cecidomyiidae), the alfalfa gall midge, is a polyphagous galling
midge that attacks immature fruiting bodies of native (Gagné
& Woods 1988)
and exotic crop plants in the
southwestern USA (Barnes 1946, Gagné & Wuensche
1986). This
midge emerged as a pest of cultivated legumes in the southwestern USA
in the early 1900's where larvae caused damaged
to pods by feeding in the ovary and immature fruiting bodies. Galling
of very young fruit can affect seed set and honey production. Damage to
alfalfa at this time appeared to range from inconsequential to 20-30%
damage being observed in some areas (Barnes 1946).
The exact home range of A. websteri is uncertain, but
the southwestern USA
and Mexico
are thought to be areas constituting the natural range in North America as this midge was first recorded
from this area in 1909 (Barnes 1946, Gagné & Orphanides
1992, Gagné & Woods 1988, Rogers
1972).
Prior to 1917, economic entomologists in the USA considered this midge
to be A. miki
Wachtl, a pest of legumes in central Europe, France,Italy, Hungary,
Russia, and possibly England (Barnes 1946). Felt (1917) considered this
highly isolated population of an invasive "European" pest in the
southwestern USA "remarkable" but the identity of the midge could not
be reassessed until a sufficient series of material was available for
examination and comparison to European material. Reared material was
made available in 1917 and sufficient morphological differences
between the A. miki from
Europe and the southwestern USA Asphondylia
were determined to exist (e.g., smaller size, darker color, and less
setae for the US species) that the US Asphondylia
was named A. websteri after
Professor Webster who supplied the type series of reared material for
examination (Felt 1917).
There are over
250 described species of Asphondylia,
with many additional known species that remain undescribed
(Gagné & Waring
1990). Asphondylia spp. are
cosmopolitan in distribution and the majority appear to be mono- or
stenophagous (Barnes 1939). Some Asphondylia
spp. exhibit sufficiently high host fidelity they have been considered
as
classical biological control agents for invasive weed species
(Cruttwell-McFadyen & Bennett 1995). Other species of Asphondylia,
like A. websteri
and A. gennadii, are polyphagous, and
in some instances, can be important pests on non-native crops
(Gagné &
Orphanides 1992, Gagné & Wuensche 1986, Rogers 1972).
Surveys for fruit feeding pests of Hass and non-Hass avocados over
November-December 2007 in Guatemala detected large numbers of deformed
avocado fruit < 2cm in length in a commerical Hass avocado orchard
in Sumpango, Sacatepéquez. Visual examination of fruit indicated
that
up to 85% of "off bloom"
fruit set from flowering that occurred over the period August-September
was attacked despite
prophylactic applications of broad spectrum insecticides. Deformed
fruit did not set on trees and was observed to drop to the
ground. Dissection of deformed fruit in the field revealed the
existance of internally feeding larvae. Subsequent rearing of field
collected material revealed that A.
websteri was the agent responsible for fruit damage that was
promoting premature abscission. The rearing and identification of A. websteri from Hass avocados in
Guatemala is the first official record for this midge from Central
America and the first time this insect has been recorded attacking
immature fruit of avocados.
Adult Asphondylia websteri: Adult males and
females of this midge are small and typically around 2.25 mm in length.
Antenna are long often greater than 3/4 of the body length. Eyes are large and black, the
thorax is a dark
reddish brown with occassionally yellowish brown markings. Legs are
brown in color, halteres are pale yellow, and the wings are hylaine
almost without setae and characterized by a light brown costal vein.
Larvae and Pupae: In Hass
avocados, immature A. websteri
feed in the ovaries of developing fruit. Female flies appear to lay one
egg per fruit. Larvae complete development within fruit and create an
escape tunnel in the side of the fruit from which the adult fly can
emerge. The emergence tunnel is created by a "spatula", a structure on
the head region of third instar larvae that is used to scrape away
plant material until a thin exocarp wall is formed at the distal end of
the tunnel. Pupation occurs within the central cavity of the deformed
fruit. When the fully developed adult midge is within the pupal case
the pupa advances to the end of the escape tunnel using abdominal
spicules to gain traction within the tunnel. The pupa opens the
necrotic entrance in the exocarp wall to the outside world by applying
it pupal horns to the closed end of the tunnel and rotating its body
about the longitudinal axis thereby cutting open the exit hole (Gagné et al. 2004). Once the
circular tunnel entrance is open, the pupa advances partway out of the
tunnel exit and the adult midge then emerges from the protruding
pupal case. Typically, the deformed fruit dehisces shortly after the
emergence of the adult fly, and drops from the tree. Subseqeuntly,
abscissed fruit with protruding midge pupal cases can be collected from
the ground.
Asphondylia
websteri escape tunnel entrance shown in a deformed fruit
(bottom fruit in left photo). Protruding pupal case from which the
adult midge has emerged (center). A.
websteri pupae that emerged fully from fruit prior to the
emergence of adult midges (right).
Feeding
Damage: As larvae develop and feed internally, infested young
Hass avocado fruit become mis-shapen acquiring a thin and elongated
appearance. This
shape is extremely characteristic for young avocados infested by A. websteri. Internally, the young
avocado fruit is hollowed out by larval feeding. Gagné et al. 2004 mention that in
avocado fruit attacked by Bruggmanniella
perseae, a cecidomyiid from Colombia and Costa Rica, the central
chamber in the fruit becomes colonized by the hyphae of what is
presumed to be a symbiotic fungus. It was not noticed whether Hass
avocado fruit in Guatemala attacked by A. websteri also promoted fungal
growth in the central feeding chamber.
Hass fruit undergoing normal
development are shown on the right in the photo above. Elongate fruit
on the right have Asphondylia
websteri larvae developing inside.
Natural Enemies of Asphondylia websteri: Larvae
of A. websteri were heavily
parasitized by five species of hymenopterous parasitoid: (1) Torymus sp. A, (2) Torymus sp. B (both
Hymenoptera: Torymidae); (3) Rileya
sp. (Hymenoptera: Eurytomidae); (4) Paragaleopsomyia
sp. (Hymenoptera: Eulophidae), and (5) Lyrcus sp. (Hymenoptera:
Pteromelidae). The dominant parasitoid species reared from A. websteri in Guatemala was Torymus sp. B.
Torymus
spp. (Hymenoptera: Torymidae) (photo above) were the most common
parasitoids reared from Asphondylia
websteri larvae infesting Hass avocados in Guatemala.
In addition to parasitoids, larvae of A.
websteri were attacked by Epipona
guerini (Hymenoptera: Vespidae: Polistinae). Adult wasps were
observed foraging in the study orchard, cutting open infested fruit
with their mandibles, and extracting A.
websteri larvae and eating them. The sides of fruit from which A.websteri were removed by E. guerini were characterized by
large circular holes.
Epipona
guerini opening an immature Hass avocado fruit infested with a
larva of Asphondylia websteri (left
photo). Epipona guerini
extracted Asphondylia websteri larvae
from fruit and ate them (middle photo). Fruit from which Asphondylia websteri have been
removed by Epipona guerini
were characterized by large circular holes in the side of the fruit
(right photo).
BARNES,
H. F. 1946. Gall midges of economic importance. Vol. II. Gall
midges of fodder crops. Crosby Lockwood and Son LtD. U.K.
CRUTTWELL-MCFADYEN,
R. E., AND F. D. BENNETT. 1995. Potential biocontrol
agents of Portulaca oleraceae L. from
the Neotropics. Biol. Cont. 5: 189-195.
FELT, E. P. 1917. Asphondylia
websteri n. sp. J. Econ. Entomol. 10: 562.
GAGNÉ, R. J., AND G. M. ORPHANIDES. 1992. The pupa and larva
of Asphondylia gennadii (Diptera:
Cecidomyiidae) and taxonomic implications. Bull. Entomol. Res. 82:
313-316.
GAGNÉ,
R. J., F. POSADAM, AND Z. N. GIL. 2004. A new species of Bruggmanniella
(Diptera: Cecidomyiidae)
aborting young fruit of avocado Persea americana
in Colombia
and Costa Rica.
Proc. Entomol. Soc.Wash. 106: 547-553.
GAGNÉ,
R. J., AND W. M. WOODS. 1988. Native American plant hosts of Asphondylia websteri (Diptera:
Cecidomyiidae). Ann. Entomol. Soc. Am. 81: 447-448.
GAGNÉ,
R. J., AND A. L. WUENSCHE. 1986. Identity of Asphondylia
(Diptera: Cecidomyiidae) on Guar, Cyamopsis tetragonoloba
(Fabaceae) in the Southwestern United States.
Ann. Entomol. Soc. Am. 79: 246-250.