Description of the mature larva and pupa of Anthonomus santacruzi Hustache (Coleoptera, Curculionidae), a biological control agent of Solanum mauritianum Scop. (Solanaceae), and remarks about its biology
Author
Gosik, Rafał
Author
Sasa, Archbold
Author
Witkowski, Ed. T. F.
text
Zootaxa
2017
4294
5
545
558
journal article
32556
10.11646/zootaxa.4294.5.4
3b35e5dc-6ec2-4d24-bfbf-a12530ed023a
1175-5326
839174
831A0613-4C48-49B6-A68C-C4539C3F9913
Description of the mature larva of
Anthonomus santacruzi
General.
Body elongated, slightly curved (
Fig. 2
), rounded in cross section.
Colouration.
Pale to dark brown head (
Figs 2
,
10
). Thorax and abdomen white to whitish yellow (
Fig. 2
).
Vestiture.
Setae on body thin, yellow or brown, of distinctly different lengths (minute to short or relatively elongate).
Body shape (
Fig. 2
). Prothorax smaller than meso- and metathorax (both with similar size). Spiracle bicameral, located on prothorax. Abdominal segments ĪV subequal in length; VĪVIII with length decreasing gradually posteriorly; IX almost hemispherical; X reduced to four anal lobes; dorsal anal lobe narrow; laterals lobes distinct; and ventral lobe very small. Anus terminal. Abdominal ambulatory ampullae bilobate to circular. Abdominal spiracles I–VIII bicameral, placed mediolaterally.
Chaetotaxy.
(Number of setae is given for only one side of the body.) Prothorax (
Figs 4, 6, 8
) with 9 long and 2 medium
prns1‾11
on a weakly pigmented dorsal sclerite; 2
ps1-2
, and 1 minute
eus
. Mesothorax (
Figs 4, 6, 8
) with 3 long and 2 medium
pds1‾5
(1, 3, and 5 long, 2 and 4 medial); 1 short
as
; 1 medium
eps
; 1 long
ps
and 1 minute
eus
. Metathorax (
Figs 4, 6, 8
) similar to mesothorax. Each thoracic pedal area well separated, and with 2 long
pda1‾2
. Abdominal segments ĪVIII (
Figs 4–9
) with 1 short
prs
; 3 long and 2 medium
pds1‾5
(1, 3, and 5 long, 2 and 4 short); 1 long
sps
; 1 long and 1 minute
eps1‾2
; 1 medium
ps
; and 2 minute
eus
. Abdominal segment IX (
Figs 4
̄9) with 5
ds
(1 minute, 2 and 3 medium, 4 and 5 minute), 2
ps1‾2
(1 long, and 1 minute) and 1 very short
sts
. Abdominal segment X (
Figs 4
̄9) without setae.
Head capsule (
Fig. 10
). Head hypognathous, suboval; endocarinal line present and reaching behind middle of frons. Frontal sutures distinct, extending to antennae. One stemma (st) present and close to antenna. Dorsal setae:
des1‾3
and
des5
elongate;
des4
and
des6
minute.
des1
and
des2
located near to middle part of epicranium;
des3
and
des4
close to frontal suture, or within it;
des5
anterolaterally;
des6
near to side of epicranium (
Fig. 10
). Frontal setae:
fs1
and
fs3
minute;
fs2
absent;
fs4
long, located anterolaterally;
fs5
long, located laterally, close to border of frons (
Fig. 10
). Lateral setae:
les1
very short,
les2
as long as
des5
. Vertical seta (
ves
) very short. Epicranial area with 4 postepicranial setae (
pes1-4
) and 3 pores. Antenna with a membranous and slightly convex basal article bearing one arrow-like sensorium; basal membranous article with 7 sensilla of different types: 2 apullacea (sa), 3 styloconium (ss), and 2 basiconium (sb) (
Fig. 11
).
Mouthparts.
Clypeus (
Fig. 12
a) 3.3 times wider than long with 2 very short posterolateral
cls
, and 1 sensillum (
clss
) between the
cls
; anterior margin of clypeus curved. Labrum (
Figs 12
āc) 1.7 times wider than long, with 3 pairs of piliform
lms1‾3
;
lms1
and
lms2
with similar length and distinctly exceeds anterior margin of labrum,
lms3
very short. Anterior margin of labrum double sinuate. Epipharynx (
Figs 12
b, c) with 3 finger-like
als1‾3
, a pair of pilifrom and relatively elongated
ams
, 2 relatively short and finger-like
mes1‾2
, a pair of sensory pores (snp) outside of labral rods, and a pair of epipharyngeal sensillum clusters (esc). Labral rods (lr) elongate, slightly converging posteriorly, apical part more sclerotized, and basal part slightly enlarged. Mandible (
Fig. 13
) distinctly broad, bifid, with curved teeth of subequal height;
mds
piliform,
mds2
two times longer than
mds1
and located laterally. Maxillae (
Figs 14
̄16); stipes with 1
stps
, 2
pfs
, and 1
mbs
, with one sensillum (sn) close to
mbs
;
stps
and
pfs1–2
relatively long,
mbs
short; mala with 7
dms1‾7,
all
dms
piliform, almost equal in length; 3 medium to short
vms1‾3
;
vms
distinctly shorter than
dms
(
Figs 15
a, b). Maxillary palpi with two palpomeres: I with 1 short
mxps
and two sensilla; length ratio of I and II: 1:0.7; II with one sensillum and a group of conical, cuticular apical processes. Prelabium (
Fig. 16
) heart-shaped, with 1 relatively long
prms
; ligula with sinuate margin and 2 short
ligs1-2
; premental sclerite well visible, Q-shaped, with distinctly elongated basal parts; labial palpi one segmented, palpomere with one sensillum and short, cuticular apical processes. Postlabium (
Fig. 16
) with 3
pms1‾3
;
pms1
located medially, and
pms2
and
pms3
laterally;
pms1
very short, almost conical;
pms3
medium, and
pms2
elongate, distinctly longer than others.
FIGURES 4‒9.
Anthonomus santacruzi
, mature larva, chaetotaxy: 4, 6, 8—thorax and abdominal segment I, 5, 7, 9— abdominal segments V̅X, 4, 5—dorsal, 6, 7—lateral, 8, 9—ventral. Th1–3—pro-, meso- and metathorax, Abd1–9— abdominal segments I̅IX, setae:
as
—alar,
ds—
dorsal,
eps
—epipleural,
eus
—eusternal,
lsts
—laterosternal,
pda
—pedal,
pds
— postdorsal,
prns
—pronotal,
prs
—prodorsal,
ps
—pleural,
sps
—spiracular,
sts
—sternal.
FIGURES 10, 11.
Anthonomus santacruzi
, mature larva: 10—head, 11—antenna. HH—head height, HW—head width, ststemmata, Se—sensorium, sensiliae: sa—apullacea, sb—basiconium, ss—styloconium, setae:
des
—dorsal epicranial,
fs
— frontal,
les
—lateral epicranial,
pes
—postepicranial,
ves
—ventral.
FIGURES 12, 13.
Anthonomus santacruzi
, mature larva, mouthparts: 12—clypeus, labrum, and epipharynx (a—dorsal side, b, c—ventral side), 13—left mandible, clss—clypeal sensorium, esc—epipharynx sensillium clusters, lr—labral rods, snpsensory pore, setae:
als
—anterolateral,
ams—
anteromedial,
cls—
clypeal,
lms—
labral,
mds
—mandibular,
mes—
median.
FIGURES 14–16.
Anthonomus santacruzi
, mature larva, mouth parts: 14—maxillolabial complex, ventral, 15a, b—left maxillia and part of praelabium (a—dorsal side, b—ventral side), 16—maxillae and prelabium, sn—sensillium, setae:
dmsdorsal
malar,
ligs—
ligular,
mbs
—malar basiventral,
mxps—
maxillary palps,
pfs—
palpiferal,
prms—
prelabial,
pms—
postlabial,
stps—
stipal,
vms—
ventral malar.
Description of pupae
Measurements
(in mm). Body length 3.10–4.50; widest part (at the level of the middle legs) 1.30–2.50 (see
Table 1
).
Colouration.
Body white or light yellow. Cuticle smooth.
Body shape (
Figs 3
,
17–19
). Body moderately elongate and rather slender. Rostrum very long (5 times longer than wide). Antennae relatively long and slender. Pronotum 1.7 times wider than long. Mesonotum almost as long as metanotum. Abdominal segments ĪVII of equal length; VIII narrow, IX distinctly smaller than others. Urogomphus elongate; straight; with sclerotized apex.
Male and female rostrum of similar length. The shape of the gonothecae is typical for weevil pupae: divided in females (
Fig. 23
a), undivided in males (
Fig. 23
b).
Chaetotaxy
(
Figs 20
̄23). Setae yellow to dark brown; very long to minute; hair-like, slightly curved. Long setae located on conical protuberances; medium and minute setae without protuberances. Head capsule (
Figs 20, 21
) with 1
vs
, 1
os
, and 1
pas
. Rostrum with 2 pairs of rs;
rs1
medium,
rs2
short.
pas
as long as
rs2
. Pronotum (
Figs 20, 21
) with 2
as1‾2
, 1
sls
, 2
ds1‾2
, and 3
pls1‾3
. Meso- and metanotum (
Fig. 22
) with 3 long setae placed medially. Femoral setae (
fes
) absent. Abdominal tergites ĪVIII with 3 very long setae (
d1‾3
) and a single lateral seta (
l
). All abdominal setae located on small conical protuberances. Abdomianl sternites ĪVIII without setae. Abdominal segment IX with 3 pairs of dorsal setae (
d
); urogomphus with 2 pairs of ventral setae (
v
).
Addendum to key to pupae of selected
Anthonomus
species presented by
Burke (1968)
The species
A
.
monostigma
(described by
Chacón-Madrigal
et al.
2012
),
A
.
vis
(by
Bená & Vanin 2013
), and
A
.
santacruzi
(described in the present work) are herein added to the key of
Burke (1968)
.
(previous steps as in Burke’s [1968] original key)
9. Pronotal setae long and very slender...................................................................... 9a
- Pronotal setae short and stout...........................................................................9b
9a. Urogomphus forked at apex...................................................
Pseudoanthonomus validus
Dietz
-
Urogomphus peaked at apex...................................................
Anthonomus santacruzi
Hustache
9b. Three pairs of basirostral (
pas
) setae present; urogomphus with slightly bifurcate apex......
Anthonomus albopilosus
Dietz
- Basirostral (
pas
) setae absent; urogomphus with strongly bifurcate apex......................
A. monostigma
Champion
(next steps as in original key)
27.
sos
present;
rs
absent.........................................................................
A. tenuis
Fall
-
sos
absent; two pairs of
rs
present...............................................................
A. vis
Clark
Discussion
Pupae of
A
.
vis
(described by
Bená & Vanin 2013
) are similar to those of
A
.
cycliferus
Fall, 1913
, and the larvae of both species are inquilines in galls (
Burke 1968
).
Chacón-Madrigal
et al.
(2012)
remarked that despite the broad range of plant associations seen among Anthonomini, most known
Anthonomus
are monophagous species, and host preferences of the larvae are always more restricted than those observed for adults. It is worth stressing that weevil species regarded as polyphagous often establish strictly monophagous local populations even though other potential host plants were reachable (Gosik 2009).
FIGURES 17‒19.
Anthonomus santacruzi
, pupa: 17—ventral, 18—dorsal view, 19—lateral, Th1–3—pro-, meso- and metathorax, Abd1–9—abdominal segments I̅IX, ur—urgomphus.
FIGURES 20‒23.
Anthonomus santacruzi
, pupa: 20, 21—head and pronotum (20—ventral, 21—lateral), 22—dorsal chaetotaxy, 23a, b—terminalia, ventral (a—female, b—male), ur—urogomphus, setae:
as
—apical,
d
—dorsal,
ds
—discal,
l
— lateral,
os
—orbital,
pas
—postantennal,
pls
—posterolateral,
rs
—rostral,
sls
—superlateral,
vs—
vertical.
FIGURES 24‒27.
Field photos of
Anthonomus santacruzi
and
Solanum mauritianum
: 24—
A
.
santacruzi
on
S
.
mauritianum
inflorescence, 25, 26—
S
.
mauritianum
inflorescences exhibiting
A
.
santacruzi
damaged (brown) buds, 27—
S
.
mauritianum
with inflorescences in the field.
On the other hand, food preferences of adult weevils examined in the laboratory can be quite surprising, e.g.,
Bagous binodulus
Herbst 1795
is regarded as monophagous on
Stratiotes aloides
L. but preferred
Trifolium repens
L. and
Plantago major
L. under laboratory conditions (
Dieckmann 1964
).
The number of larval instars and the average length of head capsules estimated by
Chacón-Madrigal
et al.
(2012)
on
A
.
monostigma
larvae were similar to those observed on
A
.
santacruzi
. The total number of three larval instars (three) and the head widths of mature larvae (~0.50 mm) corresponded with the results of our observations. Also, the setal index of both the larvae and the pupae of
A
.
santacruzi
agree with those given by
May (1993
,
1994
) as typical for
Curculionidae
immatures, and to previously described
Anthonomus
species as well (
Loicáno
et al.
2004
;
Chacón-Madrigal
et al.
2012
;
Bená & Vanin 2013
). Based on larval characters of previously described
Anthonomus
species,
A. santacruzi
is close to
A. rubicosus
(especially with respect to head width, length of
fs1
and
fs3
, the one-segmented labial palpus, and length of
pms
).
Remarks on the development of
Anthonomus santacruzi
Field observations showed that
A
.
santacruzi
has a high fecundity, short generation time, and overlapping generations that facilitate rapid population increases. Similar facts were noted by
Olckers (2003)
, who did the initial biological studies of this weevil. The destructive nature of the larval feeding (within flower buds:
Figs 24
̄27) prevents fruit set, and can thus reduce
S
.
mauritianum
’s extensive seed production (
Florentine
et al.
2003
;
Olckers 2003
;
Witkowski & Garner 2008
).
The knowledge about an insects biology is fundamental not only for their protection (
Trnka
et al.
2015
; Shuhrovec &
Bogusch 2016
) but also for their use in biological control of weeds (
Gosik & Skuhrovec 2011
;
Münzbergová & Skuhrovec 2013
). Potential uses of an insect as a control agent depends on its larval biology (
Skuhrovec
et al.
2008
;
Stejskal
et al.
2014
;
Abela-Hofbauerova
et al.
2011
;
Münzbergová
et al.
2015
). Effective control agents should cause a reduction in the shoot biomass of infected plants or else inhibit their generative abilities. Hence weevil species with larvae that feed on roots or that develop on flower buds are the most effective control agents (
Rowe & Kok 1985
;
Steinger & Müller-Schärer 1992
;
Corn
et al.
2006
;
Koprdova
et al.
2015
). On the other hand, species with larvae that feed on leaves (for example) usually only cause minor damage to plants (
Stejskal
et al.
2014
). Moreover, weevils living ectophytically are relatively more vulnerable to predators (
Skuhrovec
et al.
2017
) and thus less effective as control agents. Moreover, some species (potential biocontrol agents) are in fact less effective control agents because of their high rates of infestation by parasites and parasitoids (
Koprdova & Skuhrovec 2007
). However, parasites or parasitoids of the immature stages of
A
.
santacruzi
were rarely observed. Less than 5% of
A
.
santacruzi
larvae collected during our observations were associated with immatures of an unidentified parasitoid wasp
Pteromalidae (Hymenoptera)
. Hence,
A
.
santacruzi
appears to be a good example of a species that is well adapted to the role of a biocontrol agent.