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SYSTEMATICS, MORPHOLOGY AND PHYSIOLOGY
Morphology of Immature Stages in the Neotropical Nonfrugivorous
Tephritinae Fruit Fly Species Rachiptera limbata Bigot (Diptera:
Tephritidae) on Baccharis linearis (R. et Pav.) (Asteraceae)
DANIEL FRÍAS
Instituto de Entomología, Univ. Metropolitana de Ciencias de la Educación, Casilla 147, Santiago, Chile
lfriasdaniel@gmail.com
Neotropical Entomology 37(5):536-545 (2008)
Morfologia dos Estados Imaturos da Espécie de Mosca das Frutas Neotropical não Frugívora Rachiptera
limbata Bigot (Diptera: Tephritidae) em Baccharis linearis (R. et. Pav) (Asteraceae)
RESUMO - Rachiptera limbata Bigot desenvolve-se em Baccharis linearis (R. et Pav) na região de
Santiago, Chile. As larvas alimentam-se dos caules e secretam um líquido, que em contato com o ar,
forma uma câmara larval, onde ocorre a passagem para o estádio de pupa. Os estádios larvais das
espécies neotropicais de Tephritinae são pouco conhecidos. O presente estudo descreve a morfologia dos
estádios larvais de R. limbata, comparando-os com outras espécies de Tephritinae, em uma abordagem
filogenética. Foram analisados, em microsopia de luz e de varredura, o complexo antenomaxilar, as
dobras da cutícula, as margens da abertura oral, o esqueleto cefalofaríngeo, os espiráculos anterior e
posterior e os lóbulos anais das larvas de primeiro, segundo, terceiro estádios e da pupa. O esqueleto
cefalofaríngeo é altamente esclerotizado e apresenta um orifício ou abertura na cornua ventral,
característica essa que parece ser plesiomórfica em R. limbata e outras espécies neotropicais. Os
espiráculos anteriores estão ausentes nas larvas de primeiro estádio. Nas larvas de segundo e terceiro
estádios são desenvolvida formando cinco túbulos curtos dispostos em fileira única. Nas larvas de
primeiro e segundo estádios, as aberturas dos espiráculos têm cerdas únicas; nas larvas de terceiro
estádio não há cerdas. Essa última característica parece decorrer de uma atraso no desenvolvimento
(neotenia) da larva de R. limbata, quando comparada a outras espécies neotropicais e neárticas.
PALAVRAS-CHAVE: Adaptação, neotenia, caráter plesiomórfico, apomórfico
ABSTRACT - Rachiptera limbata Bigot develops on Baccharis linearis (R. et Pav.) in the areas around
Santiago, Chile. The larvae feed on stem tissues and secrete a liquid that hardens to form a protective
feeding and pupation chamber. The immature stages of Neotropical species of Tephritinae are poorly
known. In this paper, the morphology of the immature stages of R. limbata are described and compared,
in a phylogenetic context, with other Tephritinae species. Antennomaxillary complex, pads, oral ridge,
cephalopharyngeal skeleton, anterior and posterior spiracles and anal lobes of first-, second-, third-instar
larvae and pupae were studied with optical and scanning electron microscopy. The cephalopharyngeal
skeleton is darkly sclerotized and shows an opening or window in the ventral cornua. This trait seems
to be plesiomorphic in R. limbata and in other Neotropical species. First-instar larvae anterior spiracles
are absent; whereas in second and third instars spiracles are developed as a row of five short tubules.
In first- and second-instar larvae, the posterior spiracular slit has only a single hair per bundle; whereas
third-instar larvae lack hairs. This last trait seems to be consequence of a larval development delay and
an apomorphic trait in R. limbata, compared to other Neotropical and Neartical species.
KEY WORDS: Adaptation, neoteny, plesiomorphic, apomorphic traits
The genus Rachiptera Bigot belongs to the subfamily
Tephritinae. The species of Tephritinae are the most
specialized of Tephritidae. The larvae of these non
frugivorous species predominantly infest flower heads as
well as stem buds, leaves or roots of Asteraceae the largest,
most advanced, and widespread family of Angiosperms.
Nevertheless, several species infest a few other families
such as: Acanthaceae, Goodeniaceae, Lamiaceae, and
Vervenaceae (Headrick & Goeden 1998, Norrbom et al.
1998, Han & McPheron 2000). The Tephitinae is a large
and diverse subfamily with more than one hundred genera.
However, it is believed to be a monophyletic group, which
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Neotropical Entomology 37(5)
shares derived characters (synapomorphies) that are evidence
of exclusive common ancestry (Han & McPheron 2000,
Korneyev 2000).
The genus Rachiptera belongs to the tribe Eutretini Munro
and includes four exclusive Neotropical species: R. biarcuata
Hendel and R. percnoptera Hendel, distributed only in Chile;
R. virginales Hering, an endemic species from Brazil; and R.
limbata Bigot distributed in Argentina and Chile. The larvae
of Rachiptera and Strobelia Rondani are the only species of
Tephritidae that form a globular protective structure outside
their gall (Aljaro et al.1984, Norrbom et al. 1998). R. limbata
is a monophagous and bivoltine species that attacks the
endemic Baccharis linearis (R. et Pav.) from Chile.
Females lay their eggs into branch apical meristems of
B. linearis. The larvae feed from the stem inner tissues and
secrete a liquid that is expelled throughout the damaged areas
of the stem. This secretion is clear, but in contact with air
forms a spongy material with high water absorption capacity.
Pupation takes place within the larval chamber, approximately
twenty days after oviposition. The chamber is non-dehiscent
and adults must use an escape route made by the larva. Adult
populations emerge during spring and summer (Porter 1929,
Aljaro et al. 1984). Neotropical Tephritinae morphology of
immature stages, with only a few exceptions, are poorly
known (Frías 1985, Gandolfo & Hernández 1999, Steck
& Wharton 1986). This paper describes the morphology of
three instar larvae and pupae of R. limbata, compared other
Tephritinae and Trypetidae morphology, discussed in an
evolutionary biology framework.
Material and Methods
The research was conducted during spring and summer
of 2003-2005, near Pirque, 33º lat.S, 71º long.W, 28 km
southeast from Santiago City 650 m elevation. Immature
stages of R. limbata were reared from field collected feeding
chambers of B. linearis. The eggs were collected from apical
meristems of B. linearis and first-instar larvae from small
chambers (ca. 0.2 cm diam) located in the apical meristems
of host plants. Second-instar larvae were collected from
chambers ca. 0.5-1.0 cm of diam and third-instar larvae from
chambers of ca. 1.5-2.5 cm of diam.
Twenty five larvae of each instar and twenty pupae were
killed and fixed in boiling water for one minute and preserved
in 70% ethanol. For optical studies larvae were treated
overnight in 10% KOH following the methods of Steck &
Wharton (1986); a process that allowed for unobstructed
viewing of the cephalopharyngeal skeleton, antenomaxillary
complex, anterior and posterior spiracular complexes. The
treated larvae were dissected and the anterior and caudal
segment were slide mounted in Canada Balsan.
Another ten larvae of each instar were prepared for
scanning electron microscopy (SEM). The alcohol-stored
specimens were cleaned in hot distilled water with a few
drops of detergent, fixed in 3% glutaraldehyde in cacodylate
buffer,then fixed in 1% osmium tetroxide, and dehydrated in
a 50%, 70%, 95% and 100% acetone series. Specimens were
prepared for SEM observations by using critical-point drying
(Sovall Critical-Point Drying System) and coating with gold.
The specimens were examined at an accelerating voltage
of 30 KV on a JEOL.JSM-25-SII SEM. Terminology used
follows that of Headrick & Goeden (1990), White & ElsonHarris (1992), White et al. (2000) and Frías et al.( 2006).
Results
Egg. White, elongate, 0.79 to 0.98 mm long, and 0.37- 0.45
mm wide, with a broad short pedicel, 0.08- 0.15 mm long
and 0.10- 0.14 cm wide. Ten eggs were measured in situ in
apical meristem tissues (Fig. 1).
First-instar larva
Body. White, elongate-ellipsoidal, conical anteriorly,
truncated posteriorly; length 0.7 - 0.9 mm; width 0.15-0.30
mm (n = 25) (Fig. 2)
Cephalic segment. Conical and sharp, with a longitudinal
dorsal suture within the antennomaxillary sense organ,
dorsally and laterally with six extended irregular, long
smooth cuticular folds, oral ridges absent (Figs. 3-5);
antennomaxillary sense organ is not sclerotized, antenna one
segmented. Sensilla of maxillary palp, surrounded by a wide
cuticular fold (Fig. 6). Cephalopharyngeal skeleton is darkly
sclerotized, mandible black, mouthook tridentate (Figs. 4, 9),
apical and preapical teeth brown, curved, and similar in length
(Fig. 5), with a small third tooth (Fig. 9). Ventral apodeme
of mandible well developed and broad, with a small sharp
projection located posteriorly; dorsal apodeme curved, sharp,
and well developed (Fig. 9). Hypopharyngeal sclerite, and
bridge of hypopharymgeal sclerite, black, the latter located
approximately in the middle of hypopharyngeal sclerite.
Labial sclerite black, adjacent to hypopharyngeal sclerite.
Parastomal bar brown, adjacent to hypopharyngeal sclerite;
pharyngeal sclerite black, dorsal bridge of pharyngeal
sclerite dark brown and sclerotized. Dorsal cornu black and
bifurcated, with some brown areas; ventral cornu black, with
some brown bifurcated areas and two concentric sclerotized
pedicel
egg
Fig. 1. Egg of R. limbata inserted in apical meristeme of
B. linearis.
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Frías - Morphology of Immature Stages in the Neotropical Nonfrugivorous Tephritinae Fruit Fly Species...
psp
mand
Fig. 2. First-instar larva of R. limbata feeding from stem
inner tissues; posterior spiracles: psp, mandible: mand.
bars united posteriorly in a circular shape with a window
located centrally; ventral bridge of pharyngeal sclerite black
(Fig. 9).
Prothorax. Anterior area with a long cuticular fold;
circunscribed by four rows of posteriorly directed, minute
acanthae; dorsally with two round papilla sensilla (Figs. 3,
5); anterior spiracles absent.
Caudal segment. Circumscribed by minute acanthae (Fig.
7). Posterior spiracles slightly sclerotized, peritreme yellow,
with three spiracular slits nearly three times as long as wide;
dorsal, ventral and lateral spiracular bundles with only one
nonbranched hair (Fig. 8).
Second-instar larva
Body. Pale yellow, elongate-ellipsoidal, conical anteriorly,
truncated posteriorly; 1.0 - 2.9 mm long and 0.8-1.5 mm
wide.
Cephalic segment. Extended and distinctly pointed, with a
longitudinal dorsal suture. Dorsum covered with irregular
cuticular pads (Fig. 12), antennomaxillary sense organ with
medial integumental petals and with lateral integumental
petals (Fig. 13). Frontolateral view shows some irregular,
extended pads, without oral ridges (Fig. 14). Antennomaxillary
sense organ sclerotized, with a one-segmented antenna (Figs.
13, 15). Maxillary palps surrounded by a wide cuticular
fold, with three papillate sensilla and two knob sensilla, one
additional dorsolateral sensillum, equidistant from antenna
and maxillary palp (Figs. 13-15). Cephalopharyngeal
skeleton is darkly sclerotized, mandible black, mouthook
tridentate (Figs. 10, 12); apical and preapical teeth brown,
curved, and similar in length, third tooth is brown and
small. Ventral apodeme of mandible well developed and
broad, posteriorly with a small sharp projection, dorsal
apodeme curved, sharp, and well developed. Hypopharyngeal
sclerite and bridge of hypopharyngeal sclerite, black, this
latter located approximately in middle of hypopharyngeal
sclerite. Labial sclerite black, curved and separated from
hypopharyngeal sclerite. Parastomal bar is brown, adjacent
to hypopharyngeal sclerite; pharyngeal sclerite black,
dorsal bridge of pharyngeal sclerite dark brown and heavily
sclerotized. Dorsal cornu black and bifurcated, with some
brown areas; ventral cornu is black with some brown areas,
bifurcated, with two concentric bars darkly sclerotized, united
posteriorly in a circular shape with an opening or window
located centrally. Ventral bridge of pharyngeal sclerite is
black (Fig. 10).
Prothorax. Smooth anterior area lacking rugose pads,
circumscribed by four rows of posteriorly directed minute
acanthae, posteriorly the dorsolateral area , covered by rugose
pads (Fig. 12). Anterior spiracles slightly sclerotized with
five short tubules (Figs. 12, 16).
Caudal segment. Posterior spiracles, moderately sclerotized,
peritreme yellow, with three spiracular slits nearly two and a
half times as long as wide; with only one dorsal, ventral, and
lateral nonbranched hair in spiracular bundles (Fig. 17).
Third-instar larva
Body. Pale yellow; length 3.50-4.88 mm, width 1.80-3.10
mm; elongate-ellipsoidal, conical anteriorly, truncated
posteriorly, distinctly segmented, located inside of B. linearis
larval chamber apical meristemes (Figs. 18, 19, 20).
Cephalic segment. Anteriorly extended to sharp apex, with
a longitudinal dorsal suture. Dorsum covered with round
cuticular pads (Figs. 21, 22). Lateral view shows extended
pads, without oral ridges (Fig. 23). Medial integumental
petals within the antennomaxillary sense organ and two long
lateral integumental petals (Fig. 24). Antennomaxillary sense
organ heavily sclerotized, with a one-segmented antenna.
Maxillary palps surrounded by a wide cuticular fold, with
three papillate sensilla and two knob sensilla, one additional
dorsolateral sensillum, equidistant from antenna and
maxillary palp (Fig. 24). Cephalopharyngeal skeleton darkly
sclerotized, mandibles black, mouthook tridentate (Fig. 22),
apical and preapical tooth curved and subequal in length
(Fig. 21), third tooth shorter than apical and preapical tooth
(Fig. 11). Ventral apodeme of mandible well developed and
broad, posteriorly with a sharp projection; dorsal apodeme
is rounded and well developed. Hypopharyngeal sclerite
is black, hypopharyngeal bridge located approximately in
middle of hypopharyngeal sclerite. Labial sclerite broad,
black, curved, and separated from hypopharyngeal sclerite.
Parastomal bar is brown, adjacent to hypopharyngeal sclerite;
pharyngeal sclerite, black, dorsal bridge of pharyngeal
sclerite, brown, and slightly sclerotized. Dorsal cornua black
and bifurcated, with some brown areas; ventral cornu is black
and bifurcated, with two heavily sclerotized concentric bars,
united posteriorly in a circular shape with a window located
centrally. A brown triangularly shaped ventral projection is
located at the intersection of the two concentric bars. Ventral
bridge of pharyngeal sclerite is black (Fig. 11).
Prothorax. Anteriorly smooth lacking rugose pads,
posteriorly, the dorsolateral area covered by rugose pads
(Fig. 21). Anterior spiracles slightly sclerotized with five
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psen
3
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Neotropical Entomology 37(5)
4
proth
ĺ
cfd
cephseg
ĺ
cfd
anmso
ĺ
ĺ
ĺ
acanth
anmso
mand
6
5
ant
ĺ
acanth
ĺ
mxp
ĺ
ĺ
cfd
at
pat
cfd
8
7
sslt
hr
psp
Figs. 3-8. First-instar larva of R. limbata. Cephalic segment and prothorax, anterior view (3); acanthae: acanth, antennomaxillary
sense organ: anmso, cephalic segment: cephseg, cuticle fold: cfd, prothoxax: proth, papilla sensillum: psen. Cephalic segment,
anterior view (4); antennomaxillary sense organ: anmso, mandible: mand, the arrows show the three teeth of mandible. Cephalic
segment and prothorax, lateral view (5); acanthae: acanth, apical tooth: at, cuticle fold: cfd, preapical tooth: pat. Antennomaxillary
sense organ, anterior view (6); antenna: ant, maxillary palp: mxp. Caudal segment, posterior view (7); posterior spiracles: psp.
Posterior spiracles (8); spiracular slit: sslt, hair: hr.
short tubules in a single row (Figs. 21, 23).
Caudal segment. Intermediate area is smooth, lacking
minute acanthae, dorsal ventral and lateral area with minute
acanthae, anal lobe is unilobed and flat (Fig. 25). Posterior
spiracles with heavily sclerotized peritreme and a moderately
sclerotized, surrounded by a wide cuticular fold. Three
spiracular slits, four times as long as broad, each with a wide
and moderately sclerotized rima, and without dorsal, ventral,
and lateral spiracular hairs (Fig. 26).
Pupa. Puparium black and barrel-shaped, ranging from
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Frías - Morphology of Immature Stages in the Neotropical Nonfrugivorous Tephritinae Fruit Fly Species...
Discussion
de
db
dap
mand
pb
phes
at
pat
hpes
hphb
vap
wd
vb
vc
Fig. 9. Cephalopharyngeal skeleton of first-instar larva
of R. limbata. Apical tooth: at; dorsal apodeme: dap; dorsal
bridge: db; dorsal cornu: dc; hyphopharyngeal bridge: hphb;
hyphopharyngeal sclerite: hphes; mandible: mand; preapical
tooth: pat; pharyngeal sclerite: phes; ventral apodeme: vap;
ventral bridge: vb; ventral cornu: vc; window: wd. Scale bar
10 Pm.
Isc
Fig. 10. Cephalopharyngeal skeleton of second-instar larva
of R. limbata. Labial sclerite: lsc. Scale bar 10 Pm.
tsvp
Fig. 11. Cephalopharyngeal skeleton of third-instar larva
of R. limbata. Triangular shape ventral projection: tsvp. Scale
bar 10 Pm.
4.9-5.3 mm long to 2.3-3.2 mm wide. Pupation takes place
in the larval feeding chamber, that measures ca.1.5-2.5 cm
diam externally (Fig. 27). Anterior end of puparium oriented
towards the apex of chamber. Third-instar larvae excavate the
chamber wall to form a window at the apex of the chamber for
the emerging adult to gain egress from the pupal chamber.
Different larval development stages of R. limbata can
be distinguished by size, morphology, and sclerotization of
cephalopharyngeal skeleton, cephalic segment morphology,
anterior and posterior spiracles, prothorax morphology, and
features on the caudal segment. The labial sclerite of firstinstar larvae is adjacent to the hypopharyngeal sclerite, and
in second- and third-instar larvae the labial sclerites are
curved and separated from the hypopharyngeal sclerite. In
three instar larvae the ventral cornua is black, bifurcated, and
with two sclerotized concentric bars united posteriorly in a
circular shape with an opening or window located centrally.
In the three instars larvae, at the intersection of the two bars
is a brown and moderately sclerotized triangularly shaped
ventral projection. This ventral cornua window has also been
described in the Palearctic species Xiphosia miliaria Schrank,
Terellia ceratocera Hendel, Tephritis hyoscyami L. (Persson
1963), in the Oriental species Rhabdochaeta naevia Ito and
R. asteria Hendel (Sueyoshi 1999), in the Nearctic species
Eutreta diana (Osten Sacken) and Eutreta angusta Banks
(Steck & Wharton 1986) and in the Neotropical species
Trupanea foliosi Frías, T. footei Frías, T. chrysanthemifolii
Frías and T. simpatrica Frías (Frías 1985, Frías 2005),
and Pseudoeaspis biseta Hendel (Gandolfo & Hernández
1999).
According to the phylogeny put forward by Korneyev
(2000) on Tephritinae tribes and subtribe relationships, the
species of the genera Xiphosia Robineau-Desvoidy and
Terellia Robineau-Desvoidy belong to the “lower” and
more primitive tribes of Tephritinae. The species of the
genera Rachiptera, Eutreta Loew, Rhabdocheta Meijere,
Tephritis Latreille, Trupanea Schrank, and Pseudoeaspis
Hendel belong to the “higher” tribes: Eutretini (Eutreta
and Rachiptera), Schisopterini Bezzi (Rhabdocheta),and
Tephritini Newman (Tephritis, Trupanea and Pseudoeaspis).
The wide distribution of these traits along different biotic
regions and their presence in lower and higher tribes, appear
as a plesiomorphic character in R. limbata and the other
Neotropical species.
No anterior spiracles in first-instar larvae were detected
in R. limbata. In second and third larval instars, the anterior
spiracles appear as five short tubules in a single row, slightly
sclerotized, located laterad of the posterior margin of the
prothorax. First-instar larvae of Rhagoletis pomonella
(Walsh) (Snodgrass 1924) and Anastrepha ludens Loew
(Carroll & Wharton 1989) (Trypetinae) were described
as having the anterior spiracles absent or with spiracles
appearing as a minute pore only discernible with a scanning
electron microscope as in Bactrocera tryoni Froggatt (White
& Elson -Harris,1992). Second- and third-instar larvae have
a variable number of tubules, between nine and 44 depending
on the genera (White & Elson-Harris 1992, Frías et al. 2006).
Similarly, first-instar larvae in the Tephritinae have anterior
spiracles absent or that appear as flattened pores. Second- and
third-instar larvae have a variable number, between one and
six short tubules (Goeden 2001a, b; 2002). Nevertheless, in
the first-instar larvae of Procecidochares blanci Goeden &
Norrbom, P. kristineae Goeden, P. lisae Goeden, Aciurina
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Neotropical Entomology 37(5)
13
12
cpd
asp
adsen
mip
lip
15
14
P3
K1
P1
P2
K2
cpd
16
17
Figs. 12-17. Second-instar larva of R. limbata. Cephalic segment and prothorax, anterior view (12), anterior spiracles: asp, cuticle
pad: cpd. Antennomaxillary complex, anterior view (13), additional dorsolateral sensillum: adsen, medial integumental petals: mip,
lateral integumental petals: lip. Cephalic segment, dorsolateral view (14), cuticle pad: cpd. Maxillary palp (15), knob sensilla: k1,
k2; papilla sensilla: p1, p2, p3. Anterior spiracles (16). Posterior spiracles (17), the arrow show the hair of spiracular slit.
idahonensis Steyskal, A. michaeli Goeden, and A. ferruginea
(Doane), anterior spiracles are also absent, but in secondand third-instar larvae these are flattened and recessed, and
consist of two or five ovoid papillae (Goeden & Teerink,
1996a, Goeden & Teerink 1996c, Goeden & Norrbom 2001,
Goeden & Teerink 1997a). The condition of having recessed
anterior spiracles in second- and third-instar larvae could be
a juvenile trait originated by hetrochronic larval development
or neoteny that reduces the rate of morphological develop
of these structures, such as has been postulated by De Beer
(1951), Hardy (1954), and Gould (1977).
The cephalic segment of first-instar larvae of R. limbata
have six elongated dorsolateral cuticular folds; and the
prothorax anteriorly flattened and circumscribed by four
rows of posteriorly directed minute acanthae. The prothorax,
posteriorly, bears a smooth longitudinal cuticular fold.
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Frías - Morphology of Immature Stages in the Neotropical Nonfrugivorous Tephritinae Fruit Fly Species...
Fig. 20. Third-instar larva of R. limbata inside chamber.
Fig. 18. Chambers of R. limbata in the tips of the branches
of B. linearis.
Fig. 19. Chamber of R. limbata.
Second- and third-instar larvae have the cephalic segment
covered with numerous folds and rugose cuticular pads,
dorsolaterad and laterad of the mouth lumen; prothorax
anteriorly smooth, with minute acanthae, and posteriorly with
abundant, elongated, and rounded cuticular pads.
Studies on Nearctic gallicolous Tephritinae species
in different tribes and genera such as Tephritis baccharis
(Coquillett) (Goeden & Headrick 1991)(tribe Tephritini),
Aciurina idahoensis Steyskal (Goeden & Teerink 1996a),
Aciurina semilucida (Bates) (Goeden & Teerink 1996b), A.
ferruginea (Doane), A. michaeli Goeden & Teerink (Goeden
& Teerink 1996c) (tribe Eurostini Foote, Blanc & Norrbom),
Procecidochares kristineae Goeden & Teerink, and P.
lisae Goeden & Teerink (Goeden & Teerink 1997a) (tribe
Ditrycini Foote, Blanc & Norrbom) show that first-instar
larval cephalic segments are smooth and without rugose
pads. The cephalic segment of second- and third-instar larvae
of these Nearctic species are smooth, lacking rugose pads
or with few elongated rugose pads compared to R. limbata
larvae. The prothorax of second- and third-instar larvae of
these Nearctic species are smooth and without rugose pads,
with the only exception being Procecidochares anthracina
(Doane) that has rugose pads on the dorsal half of the
prothorax (Goeden & Teerink 1997b). Third-instar larvae
of Procecidochares blanci Goeden & Norrbom have rugose
pads that circumscribe the anterior halves of the prothorax,
and second-instar larvae are circumscribed by many round,
oval or elliptical, flattened and rugose pads of different sizes
(Goeden & Norrbom 2001).
The numerous cuticular folds and pads on the cephalic
segment and prothorax of R. limbata could be an apomorphic
or adaptative trait for the unique behavior of building the
larval chamber with their salival secretions. R. limbata larva
feed on host plant apical meristem branch tissues and sap,
therefore, a highly convoluted cuticle might increase the
contact surface area with the salivary secretions liberated by
the larvae. This liquid surrounds the larva and invades the
folds of the rugose cuticular pads and may act as a means
to create the frothy bubbles in the liquid secretions. When
the secretions come into contact with the atmosphere the
secretion harden to form the larva chamber which constitutes
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Neotropical Entomology 37(5)
21
22
23
24
mip
lip
25
26
ia
al
Figs. 21- 26. Third-instar larva of R. limbata. Cephalic segment and prothorax, anterior view (21). Cephalic segment, dorsal
view (22). Cephalic segment and prothorax, lateral view (23). Antennomaxillary sense organ, medial and lateral integumental
petals (24), medial integumental petals: mip, lateral integumental petals: lip. Caudal segment (25), intermediate area: ia, anal lobe:
al. Posterior spiracles (26), the arrow show the cuticle fold that surrounded the spiracular slit.
an important microhabitat to protect the larva and puparium
from environmental extremes. During winter, pupal diapause
takes place inside this chamber as has been described by
Aljaro et al. (1984).
First-, second-, and third-instar larvae posterior spiracles
of R. limbata have three spiracular openings. In other
tephritidae species, the number of posterior spiracular
openings increase from two to three, from first to second
and third instars (Snodgrass 1924, White & Elson-Harris
1992), with the only exception being the first instar of the
gallicolous Nearctic Tephritinae species Aciurina semilucida
which have three spiracular openings similar to R. limbata
(Goeden & Tererink 1996b).
In first- and second-instar larvae of R. limbata, each group
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Frías - Morphology of Immature Stages in the Neotropical Nonfrugivorous Tephritinae Fruit Fly Species...
Acknowledgments
I thank Denise Selivon for translating the abstract to
Portuguese and to Marcela de Santiago for reviewing the
English of manuscript. I would also like to thank Bernhard
Merz for financial in travel and lodging support during the
Third Tephritoid Taxonomist’s Meeting in the Muséum d’
Histoire Naturelle Genéve, Suisse, 19-24 July 2004, where
this paper was present. Also I thank Marisol Frías Landeta for
helping me with the preparation of computer based graphic
figures, and Dr. David Headrick for reviewing the manuscript.
Supported by project FIBAS,11-04, DIUMCE.
References
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Fig. 27. Puparium of R. limbata inside chamber.
of ventral, dorsal, and lateral bundles of posterior spiracles
has one single unbranched hair. Third-instar larvae of R.
limbata do not have hairs on posterior spiracles, and the
peritreme is surrounded by a wide cuticular fold. These traits
have not yet been described in other tephritid larvae.
In fruit flies, first instars of the Trypetinae species
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Received 10/XI/05. Accepted 29/VII/08.