a comparative study on mouthpart morphology of certain larvae of chironomini (diptera: chironomidae)...
TRANSCRIPT
J . Zool., Lond. (1992) 228, 183-204
A comparative study on mouthpart morphology of certain larvae of Chironomini (Diptera: Chironomidae) with reference to the larval feeding habits
J . s. OLAFSSON
Department of Zoology, University of Bristol, Woodland Road, Bristol BS8 1 UG
(Accepted 14 August 1991)
(With 3 plates and 6 figures in the text)
Mouthparts of six species of chironomid larvae were compared on both an intra- and inter- specific level. The species were: Chironomus riparius, Cryptachironomus defectus gr., Endochirono- mus albipennis, Glypto tendipes pallens, Microtendipes pedelhs and Parachironomus arcuarus. The mouthpart morphology in C. defectus gr. and P . arcuatus is considerably different from the four other species and changes little between instars. Within C. riparius, E. albipennis, G . pallens and M . pedellus there is a considerable difference in the mouthpart morphology between the first instar and the remaining instars. The morphology of the mouthparts of the first instar of C. riparius, E. albipennis, G . pallens and M . pedellus resembles in many ways that found in C . defectus gr. and P . arcuatus.
Contents
Introduction , . . Materials and methods Results . . . . . .
Mandibles . . . . Labrum . . . . . . Premandibles . . . . Head capsule . . . .
Discussion . . . . . . Mandibles . . . . Labrum . . . . . . Premandibles . . . .
Page . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 196 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 196 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 202
Conclusion.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 202 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203
Introduction
The heterogeneity in habitat utilization and feeding ecology of Chironomidae is a well-known phenomenon (Walshe, 1951; Oliver, 1971; Brennan, 1981), and the ability of the larvae to cope with a great range of habitats, from freshwater to saline, is remarkable amongst insects. The larvae of Chironomidae are very well adapted to these heterogeneous habitat requirements, and this is reflected in their feeding behaviour and in the morphology of the larval mouthparts. Their feeding habits allow them to be classified as: carnivores; scrapers; shredders; collectors (deposit and filter- feeders); and parasites (Thienemann, 1954; Steffan, 1965, 1968; Oliver, 1971; Monakov, 1972; Cummins, 1973, 1978).
Present address: Institute of Biology, University of Iceland, Grensasvegur 12, 108 Reykjavik, Iceland
I83 0 1992 The Zoological Society of London
I84 J. S . OLAFSSON
The majority of previous work on mouthpart morphology of chironomid larvae has been based on a taxonomic interest, rather than a direct comparison of the morphological features of the larval mouthparts with reference to the larval ecology. Some authors, including Kalugina (1959, 196 1, 1963, 1974, 1975) and Shilova (1 965, 1968) have done invaluable work by comparing the morphology of the first and last instar of Glyptotendipes, Endochironomus and Parachironomus. However, the majority of studies in this field only deal with larvae of the fourth instar. Our present knowledge of larval food and feeding behaviour is sparse, and is again relevant only to the fourth instar (Burtt, 1940; Walshe, 1951; Hodkinson & Williams, 1980; Leuchs & Neumann, 1990). The only exception is the study by Alekseev (1965) who described the feeding behaviour of the first instar larvae of Chironomus dorsalis Meigen. There is therefore still a major gap in our knowledge about the feeding ecology of the earlier instars, and especially for the first instar larvae.
It has been emphasized how the biology and the morphology of the first instar chironomid larvae differ from the later instars (Dorier, 1933; Charles & East, 1977). Kalugina (1959) states that the first instar larvae are even more similar between species at this stage than they are between conspecific instars. Despite these references, no comprehensive comparison has been carried out on the mouthpart morphology of larvae of various feeding groups either between or within species.
The main aim of this study was to make a qualitative and quantitative comparison of the mouthpart morphology of some lentic chironomid larvae, both at the intra- and interspecific level, with special reference to larval food and feeding behaviour, with emphasis on the first instar.
Materials and methods
Chironomid larvae and egg masses were collected over the period from June until October 1988. Sampling sites were mainly in the Lower Litton reservoir (ST 586554) and the River Chew, Avon, south-west England (ST 595546). The egg masses were collected by hand-net (littoral) or by plankton-net (open water). All the masses were carefully examined to detect intruder larvae or parasites, then each individual mass was placed in a petri dish for rearing. The cultures were kept at 15-18°C and 16L:8D (1ight:dark) periods. As soon as the larvae had hatched they were given a mixture of fine ground organic material and ‘Liqui-fry’ (Liquifry CO. Ltd.). Samples of larvae from each of the cultures were preserved soon after the eggs hatched and as the larvae grew and moulted. All the masses were reared to adult, if possible, and adult males identified to confirm larval identification. Before mounting in Euparal, the undistorted maximum widths of the larval head capsules were measured under a binocular microscope for instar determination. Head capsule width has been widely used for instar analyses and is more precise than, for instance, larval or head-capsule length in determining larval development stage (Czeczuga, Bobiatynska-Ksok & Niedzwiecki, 1968; McCauley, 1974; Carter, 1976; Ward & Williams, 1986).
Various features of the larval mouthparts were selected for morphometrical comparison, with special reference to their possible role or functional importance in feeding. Other features in the larval mouthparts that were less accessible for quantitative comparison were examined by light microscope and scanning electron microscope (SEM). The following characters were measured in addition to the head capsule width (HW): total length of mandibles (ML); maximum length of mandibular apical tooth (AL); and maximum combined width ofinner mandibular teeth (IW) (Table I, Fig. 1). All these features are routinely used in larval taxonomy (Cranston, 1982). Information about arithmetic means of individual characters and ratios can be found in Table 11.
The mouthparts from larvae reared from at least 3 individual egg masses were examined to detect possible genetic variations. At least 10 individuals within each instar were measured, giving a minimum of 30 measurements for each species within each instar. The same specimens were used for qualitative comparison of the mouthparts. All examinations were carried out by Zeiss photo microscope a t 80-1008 x magnification.
TA
BL
E I
Spec
ies
used
for
com
pari
son
and
avai
labl
e in
form
atio
n ab
out h
abita
t ut
iliza
tion,
food
and
feed
ing
habi
ts. K
ey to
the
abbr
evia
tions
use
d in
the
fext
Spec
ies
Hab
itat
Mod
e of
feed
ing
Rec
orde
d fo
od
Ref
eren
ce
CH
l C
hiro
nom
us ri
pariu
s So
ft se
dim
ent
CR
Y
Cry
ptoc
hiro
nom
us
Soft
/san
dy s
edim
ent
Mei
gen
defeclus g
r.'
EN
D
End
ochi
runo
mus
Pl
ants
/sof
t se
dim
ent
G L
Y
PI an
ts/ s
o ft s
edim
ent
MIC
M
icro
tend
ipes
ped
ellu
s So
ft se
dim
ent
PAR
Pa
rach
iron
omus
arc
uotu
s Pl
ants
/sof
t sed
imen
t
albi
pmni
s (M
eige
n)
Gly
p to t
en di
pes
palle
ns
(Mei
gen)
(de G
eer)
Goe
tghe
buer
~ ~~
~~
~
~
Fil t
er/d
epos
it D
ettit
us/a
lgae
Ed
gar
& M
eado
ws
(I96
9),
Car
nivo
rous
O
ligoc
haet
es
Mon
akov
(197
2),
Rae
(198
5),
Ras
mus
sen
(198
4), W
alsh
e (1
951)
Titm
us &
Bad
cock
(1 9
8l),
W
inne
ll 8~
Whi
te (
I 985)
Filte
r D
etri
tus/
alga
e M
onak
ov (1
972)
, Wal
she
(195
1)
Filte
r D
etri
tus/
alga
e Bu
rtt (
1940
), M
onak
ov (1
972)
, .
* .*
W
alsh
e (1
95 1)
Fi
lter/
depo
sit
Det
ritu
s/al
gae
Wal
she
(195
1)
Mix
ed
Mac
roph
ytes
/Pro
tozo
a St
effa
n (1
965,
196
81,
Mon
akov
(197
2)
' Spec
imen
iden
tifie
d as
Cry
ptoc
hiro
nom
us su
pplic
ans
(Mei
gen)
0
r Q 2
I86 J . S . OLAFSSON
HW I
I
I I I
0.01 m m U
FIG. 1. Endochironomus ulbipennis fourth instar showing parameters measured. (a) Ventral view of a head capsule; (b) dorsal view of a mandible; (c ) premandible. P.mnd, pecren mandibuluris; S. int, sera interna.
CHIRONOMID MOUTHPART MORPHOLOGY 187
Further comparison on the larval mouthpart morphology was carried out using Philips 501 Scanning Electron Microscope (SEM). Specimens for the SEM were dehydrated in absolute alcohol, and air-dried or frozen in liquid nitrogen, and freeze-dried under vacuum. All specimens were mounted on stubs, either as whole mounts or dissected with micro-needles, and coated with gold in a Polaron sputter coater.
Morphometrical data were compared by linear regression analyses and then compared for homogeneity of the slopes and intercepts, where appropriate, by using methods described in Armitage & Berry (1987) using multiple regression analyses with ‘dummy’ variables. All the data were log,, transformed to correct for heteroscedasticity .
The following species were included in this comparison and hereafter the abbreviations in the brackets after each species will be used in the text (see Table I): Chironomus riparius Meigen (CHI); Cryptochironornus defectus gr. (CRY); Endochironomus albipennis (Meigen) (END); Glyptotendipes pallens (Meigen) (GLY); Microtendipes pedellus (de Geer) (MIC); and Parachironomus arcuatus Goetghebuer (PAR). Larvae of first instar CRY were not included because of lack of sufficient numbers.
Terminology of morphological features used in this paper is according to Saether (1980).
Results
Mandibles
The mandibles of the first instar larvae of most of the species compared in this paper have a similar structure to those found in later instars of corresponding species. In the first instar of CHI, END, GLY and MIC the mandibles are of a triangular shape (Plate Ig, h) but are elongate and more sickle-shaped in PAR (Plate If). All other species possess a long prominent apical tooth and three inner mandibular teeth, with a dorsal tooth only present in CHI, END, GLY and MIC. All of them bear a fine seta subdentalis, reaching as far as to the second inner mandibular tooth in MIC and PAR but shorter in CHI, END and GLY. However, features developed in later instars such as the pecten mandibularis and seta interna are lacking in all the species.
In the second and third instar, the mandibles have most of the characteristics which can be found in larvae of the fourth instar. At these stages all the species, apart from PAR and CRY, have well-developed pecten mandibularis and seta interna. The pecten mandibularis in CHI, END, GLY and MIC covers more or less the width of the inner mandibular teeth with its setae reaching the tip of the teeth as in END (Plates IIc, d, k, 1, IIIc, f). The seta interna divides into numerous feathery branches, covering approximately 2/3 of the basal part of the mandibles in CHI, END, GLY and MIC (Fig. 1 b). In CRY and PAR the pecten mandibularis is absent and seta interna is simple or coarsely serrated (Plate IIh, IIIk, 1). The apical tooth of CHI, END, GLY and MIC at these stages is not as distinctive and prominent as in the first instar larvae, whereas it still is in both CRY and PAR.
The ratio of the combined width of the inner mandibular teeth to the total length of the apical tooth (IW/AL) in PAR and CRY ranges from being 0.48 to 0.89 throughout all the larval stages, whereas in CHI, END, GLY and MIC this ratio ranges from 1.04 up to 1.8 1. This ratio is more or less constant between instars for PAR and CRY, 0.74-0.89 and 0.48-0.49, respectively, but it increases gradually for the other species throughout the life stages, CHI (1.04-1.32), END (1.21- 1.57), GLY (1.20-1.81) and MIC (1.38-1.80) (Table 11).
Comparison by linear regression analysis of the changes in IW as a function of AL between species and instars of the larvae, demonstrates clearly the difference in biometry of the mandibles between carnivorous/parasitic and algae/sediment feeders (Fig. 2). For the former, the intercept as well as the slope is significantly lower for CRY.
PLA
TE
I. S
cann
ing
elec
tron
mic
rosc
ope p
hoto
grap
hs o
f th
e m
outh
part
s of
firs
t ins
tar c
hiro
nom
id la
rvae
. (a)
End
ochi
rono
mus
albipennis, an
tero
-ven
tral
view
of
larv
al h
ead
caps
ule.
(b)
Chi
rono
mus
ripa
rius
, lab
ral s
etae
. (c)
E. a
lbip
enni
s, la
bral
set
ae a
nd p
rem
andi
ble.
(d)
Gly
pfot
endi
pes p
alle
ns, l
abra
l set
ae a
nd m
andi
ble.
(e
) Mic
rofe
ndip
es pe
dellu
s, la
brum
, men
tum
and
man
dibl
e. (f
) Par
uchi
rono
mus
arc
uuiu
s, la
brum
, men
tum
and
man
dibl
e. (g
) E
. alb
ipen
nis,
vent
ral v
iew
of m
andi
ble.
(h
) G. p
alle
ns, v
entro
-late
ral v
iew
of m
andi
ble.
(i) E
. alb
ipen
nis,
prem
andi
ble
with
an
acce
ssor
y bla
de. A
NT,
ante
nna;
AT,
apic
al to
oth;
BL,
acce
ssor
y bla
de; D
T, d
orsa
l to
oth;
IT, i
nner
man
dibu
lar t
eeth
; LBR
, lab
rum
; MN
D, m
andi
ble;
MN
T, m
entu
m; P
E, p
ecte
n ep
ipha
ryng
is; P
M, p
rern
andi
ble;
Si-S
iii, S
I-SI
II; S
sd, s
eta
subd
enta
lis.
CHIRONOMID MOUTHPART MORPHOLOGY I89
Another way of looking at the data is by plotting the IW/AL ratio against instars and observing the changes in the growth rate. The changes in the IW/AL ratio between instars are very clear, with both CRY and PAR showing the lowest ratio and the lowest allometric growth rate (Fig. 3). Comparison of the above parameters were carried out by ANOVA or t-test between conspecific instars and between species at the same instar. In the case of the transformed IW/AL ratio within the first instars, there were highly significant differences in all cases except between END and GLY (t=0.97, d$=57). A highly significant difference emerged in all cases when this ratio was compared between species at later instars. Comparisons of the IW/AL ratio within species between instars were also significant for all the species except CRY (P= 1.61, d$ = 2 ) .
Further comparison of the morphometry of the mandibles in the light of the ratio of IW against ML (which is here referred to as the functional scraping area of the larval mandible) demonstrates further the distinction between the two feeding groups. As seen before, both CRY and PAR are separated from the other species by having a significantly lower IW/ML ratio (Fig. 4) and the lowest allometric growth rate.
The allometric growth rate of the apical tooth (AL), as a function of the instar, also shows the distinction between CRY and PAR on the one hand, and CHI, END, GLY and MIC on the other hand (Fig. 5). A similar trend appears if the allometric growth rate of the combined width of the inner mandibular teeth (IW) is plotted against instars, where CRY and PAR have the lowest growth rate and the smallest IW value at all instars (Fig. 6). For statistical results see Table 111.
Labrum
The labrum of the first instar larvae has the same basic structure as in the later instars (Plate Ib, d, e, f). The labral setae (i.e. S-I, S-11, S-111, S-IV, chaetulae lateralis, chaetulae media and chaetulae basales) in the first instar larvae of all the species examined are weak or poorly developed or absent. Amongst the deposit/filter feeding species, CHI, END, GLY and MIC, the labral setae are weakly fringed or coarse or, as in PAR, totally bare. The labral lamella is lacking in all of the species. The pecten epipharyngis forms a row of fine setae, as in CHI and GLY (Plate Ib, d), or a trifid lobe as in END and MIC. In PAR, however, it comprises a number of robust lobes.
In the second instar most of these characteristics are well developed in all the species except CRY and PAR, and remain so throughout all the larval stages. In both CRY and PAR all the labral setae are either bare or only serrated distally (Plates IIg, IIIh, i, j). This is also the case for the labral lamella and the pecten epipharyngis if they are present (Table IV).
Premandibles
In the first instar of all the species the basic structure of the premandibles resembles that found in the later instars, except that premandibles in the first instar larvae lack premandibular brushes. All the species, however, possess an accessory blade, finely fringed distally and attached laterally to the premandibles (Plate Ii). This accessory blade is similar in all the species studied. All the species bear two premandibular teeth, except for PAR which has three at this stage.
Larvae of second to fourth instars of CHI, END, GLY and MIC all possess the same basic form of premandibles with a distinctive premandibular brush, and two or three (END, MIC) premandibular teeth (Fig. lc, Plate IIb, j). In CRY the premandibles are relatively larger and more
190 J. S. OLAFSSON
w 4 cl a
3
0
PLA
TE
11. S
cann
ing
elec
tron
mic
rosc
ope p
hoto
grap
hs of
the
mou
thpa
rts o
f chi
rono
mid
larv
ae (f
ourt
h in
star
unl
ess s
tate
d). (
a) C
hiro
nom
us ri
pari
us, a
nter
o-ve
ntra
l vi
ew o
f lar
val h
ead
caps
ule.
(b) C
. riparius, la
brum
, men
tum
and
man
dibl
es. (
c) C
. rip
ariu
s, d
orso
-late
ral v
iew
of m
andi
ble.
(d) C
. rip
ariu
s, do
rsal
view
of m
andi
ble.
(e)
Cryp
toch
irono
mus
defectus
gr.,
ante
ro-v
entr
al vi
ew o
f lar
val h
ead
caps
ule.
(f) C
. deJecrus gr., m
andi
bles
and
a di
stal
end
of p
rern
andi
bk. (
g) C
. defectus
gr.,
labr
al se
tae.
(h
) C. d
efec
rus g
r., v
entra
l view
of m
andi
ble.
(i) E
ndoc
hiro
nom
us al
bipe
nnis
, ant
ero-
vent
ral v
iew
of l
arva
l hea
d ca
psul
e. (j
) E. a
lbip
enni
s, la
brum
and
pre
man
dibl
es. (k)
E. afbipennis, do
rso-
late
ral v
iew
of m
andi
ble.
(1) E
, afb
ipen
nis,
dors
o-la
tera
l view
of m
andi
ble a
nd m
axill
a. A
NT
, ant
enna
; AT
, api
cal t
ooth
; Ch.
lt, ch
aetu
lue
late
ralis
; D
T, d
orsa
l too
th; I
T, i
nner
man
dibu
lar
teet
h; L
BR
, lab
rum
; LL,
labr
al la
mel
la; M
ND
, man
dibl
e; M
NT
, men
turn
; Mx.
plp,
max
illar
y pa
lp; P
E, p
ecte
n ep
lpha
ryng
is;
PM, p
rem
andi
ble;
PM
.br,
prem
andi
bula
r br
ush;
P.m
nd, p
ecte
n m
andi
bulu
ris; S
i-Siii
, SI-
SIII
; S.in
t, se
ta in
tern
a; S
.sd,
seta
sub
dent
alis
.
192 J . S. OLAFSSON
W
4
a
3
0
d
PLA
TE
111.
Sca
nnin
g el
ectr
on m
icro
scop
e ph
otog
raph
s of
the
mou
thpa
rts
of c
hiro
nom
id l
arva
e (f
ourt
h in
star
unl
ess
stat
ed).
(a) G
lypt
oten
dipe
s pal
lens
, ant
ero-
ve
ntra
l vie
w o
f lar
val h
ead
caps
ule.
(b)
G. p
alle
ns, l
abra
l set
ae, m
andi
bles
, lab
ium
and
men
tum
. (c)
G. p
alle
ns, d
orsa
l vie
w o
f man
dibl
e. (d
) M
icro
tend
ipes
ped
ellu
s,
ante
ro-v
entr
al v
iew
of l
arva
l hea
d ca
psul
e. (
f) M
. ped
ellu
s, d
orsa
l vie
w o
f man
dibl
e. (g
) M. p
edel
lus,
late
ral v
iew
of m
andi
ble.
(h) P
arac
hiro
nom
us a
rcua
tus
(sec
ond
inst
ar),
ante
ro-v
entr
al v
iew
of l
arva
l hea
d ca
psul
e. (i
) P.
arc
ualu
s, la
brum
and
men
tum
. (j)
P. u
rcuu
m, l
ater
al v
iew
of l
abru
m a
nd p
rem
andi
bles
. (k) P. a
rcua
lus,
ve
ntra
l vie
w o
f man
dibl
e. (1
) P. a
rcua
rus,
dors
al v
iew
of m
andi
ble.
AN
T, a
nten
na; A
T, a
pica
l too
th; D
T, d
orsa
l too
th; I
T, in
ner m
andi
bula
r tee
th; L
B, l
abiu
m; L
BR,
labr
um; L
L, la
bral
lam
ella
; M
ND
, man
dibl
e; M
NT
, men
tum
; PE,
pec
ten
epip
hary
ngis
; PM
, pre
man
dibl
e; P
. mnd
, pec
ten
man
dibu
lari
s; S
i-Siii
, SI-
SIII
; Sai
nt, se
ta
inre
rna;
S.sd
, set
a su
bden
talis
.
TA
BL
E I1
Arir
hmer
ie m
eans
for
the p
aram
eter
s us
ed fo
r m
orph
omcl
ricd
com
paris
on f S
. E. a
nd a
num
ber of
mea
sure
men
ts be
hind
eac
h m
ean
Inst
ar
HW
C
HI
CR
Y
END
GL
Y
MIC
PAR
__
ML
CHI
CR
Y
END
GL
Y
MIC
PAR
AL
CH
I
CR
Y
EN
D
GL
Y
MIC
PAR
P
I I1
IIT
IV
lnst
ar
I I1
11
1 IV
112-
2Of 1
-13
N: 3
2
107.
17 k0
.78
N: 3
8 12
6-45
f 0-
75
N: 4
5 92
.48
0.59
N
: 46
82-3
3 0.
46
N: 2
6
49-9
5 f 0.
38
N:
30
57.4
8 f 0-
44
N: 3
4
N:
45
N: 46
N: 2
6
65-6
6 f 0.
29
47.9
4 0.
I7
42.5
4 &
0.36
7.57
k0.1
1 N
: 32
8-23
4 0.
09
9*29
_+0.
08
4-57
f 0.
1 I
N: 3
7
N: 44
N: 4
4
N: 2
5 7-
94
0.06
188.
43 f 1.
98
N:
37
155.
67 f 1.
26
N:
24
187-
97
1.62
N
: 28
238.
82 f 1.
88
N44
160.
2 t +
2.50
N
: 24
123.
75 f 0.
95
N 3
5
84.1
1 f0.
95
77.8
0 f 0
52
N:
32
N: 2
2
N 2
7 12
8.41
f0.7
4 N:
43
N: 2
4
N 3
2
98.1
0f0.
73
82-4
0 f 0.
78
65-0
7 & 0.
48
12-4
4 + 0. I
3 N
: 37
N 2
3
N: 2
8
N: 4
3
N 2
4
N: 3
4
17.8
4 f 0.
16
12.7
9 k0.
13
14.9
4 f 0.
26
10.2
6 f 0.
24
11.6
5f 0
.1 7
343.
60 f 3-
09
N:
30
N:
51
N:
38
N:
35
N: 3
7
N:
23
262.
18k
1.51
332.
98 f 2.2
1
442.
29 f 5.
1 I
297.
27 It
2-77
196.
42 f 1-
59
153.
79
1.20
N
: 26
1 2
6.80
& 0-
64
N: 4
4 16
9.05
h 0.
92
N:
38
N:
34
N:
31
104.
02 f 0.
61
N: 2
0
242.
45 5 2.
87
1516
9f 1
-04
19.4
1 f0.43
N: 3
0
N:
51
N:
38
N: 3
5
N:
31
N:
22
28.3
9 f 0.
I8
20. I
9 f 0.
25
25.3
2 2 0.
37
17.1
2 f 0-
34
16.7
2 0.
23
604.
37 k 9.
64
N: 39
N: 2
8 53
9.79
f 5-
64
N 3
4 72
1.14
k 12
-61
N: 2
7
N: 3
6
N: 3
0
444.
76 f 5.
99
477.
98
3.87
308.
1 5 &
2.1 5
269.
01 f 3-
45
N: 3
4 20
7.90
f 2.
73
N: 2
5 27
8.09
& 3
.32
N: 3
2 39
3-14
f 7.
88
N: 2
5 24
6.08
f 2.
29
N: 3
3 16
5.19
f 1.
00
N: 2
9
35.7
2 f 0.
49
N 3
7
N 2
8
N: 3
4
N: 2
6
N: 3
4
N: 3
0
44-69 f 0.
69
33-9
3 f 0-
38
41 +3
5 f 05
7
29.9
2 f 03
0
25.4
3 0.
26
IW
CH
I
CR
Y
EN
D
GL
Y
MIC
PAR
I W/A
L
CH
I
CR
Y
EN
D
GL
Y
MIC
PAR
IWIM
L C
HI
CR
Y
EN
D
GLY
MIC
PAR
7.79
k 0.
10
N: 3
2
9.98
i 0.
I I
N:
38
1 1.0
7 f 0.
06
N: 4
5 8.
96 0-08
N: 44
N: 2
4 5.91 k
0.17
1-04
k 0-
02
N: 32
I .22
f 0.
02
I .20
f 0-
0 1
N: 3
7
N: 44
N: 44
N: 2
4
1.38
0.
03
0.74
& 0.
02
0- I6
0.
002
N:
30
0.17
f 0-
002
N: 3
4
N: 4
5
N: 44
N:
24
0. I7
2 0.
001
0.19
& 0.
002
0.14
h 0.
004
14-0
6 f 0.
17
N: 3
7 8.
70 f 0.
10
N: 2
4 17
.61 f
0.10
N
28
22.2
5k0.
17
N: 4
3 16
-1 3 f 0.30
N: 2
4 8-
51 20
.14
N: 3
4
1.1 3
0.
02
N: 3
7
N: 2
3
N: 2
8
N:
43
N: 2
4
N: 3
4
0.49
f 0.
0 1
1.38
f 0.
02
1.50
0.02
I.59
f0.0
5
0.74
f 0.
02
0.17
f 0X
tU2
0.1
I * 0.0
02
0.18
f 0.
001
0~17
_+0~
001
0.20
f 04
03
0.13
f 0.
002
N: 3
2
N: 2
2
N: 2
7
N: 4
2
N: 2
4
N: 3
2
24.7
8 i 0.2
4 N
: 30
13
.67 f 0.
1 I
N: 51
N: 38
N: 3
5 30
.39
0.3 1
N
: 31
13.2
0 f 0.
22
N: 2
2
2944
f 0.
19
42.1
2 f 0.
45
I .30
& 0.
04
048 f 0.
004
1.47
f 0.
02
1.67
f 0.
02
1-80
f 0.
04
0.79
f 0.
01
N:
30
N: 5
1
N: 3
8
N:
35
N:
31
N: 2
2
0.16
f 0-
002
0.1
I *0.
001
0.1 7
f 0.
001
0.1 7
f 0*
001
0.20
f 0.
002
0.13
f 0.
001
N:
26
N: 44
N: 3
8
N: 3
4
N: 3
0
N: 2
0
47.1
1 5
0.64
N
: 37
N: 2
8
N: 3
3
N:
27
49.2
7 i 0.
58
N:
34
22.4
9 f 0.
23
N: 3
0
22.0
0 0.
27
46.9
2 f 0.
52
74.5
2f 1
.47
1.32
f0.0
2 N
: 37
0.49
fO-0
1 7
N
: 28
0
1.39
~0.
01
N: 3
3 1.
8 1 &
0.0
3 N
: 26
1.66
f0.0
3 N
: 34
0.89
f 0-
0 1
N:
30
2
0.18
* 0.00
2
0.1 I
+o-
001
0.17
f 0.
002
0.17
f 0.
002
0.20
* 0-00
2
0. I4
f 0-
001
N: 3
2
N: 2
5
N:
32
N: 2
5
N: 3
3
N:
29
HW
Wid
th o
f th
e la
rval
hea
d ca
psul
e.
IW C
ombi
ned
wid
th of
the
inne
r m
andi
bula
r te
eth
ML
Len
gth
of th
e m
andi
ble,
from
the
base
of
the
man
dibl
e to
the
tip o
f th
e ap
ical
toot
h A
L L
engt
h of
the
man
dibu
lar a
pica
l too
th.
CHIRONOMID MOUTHPART MORPHOLOGY 195
0 CHI
0 CRY
0 END I GLY
A MIC
A PAR
Chironomus riparius
Cryptochironomus defectus gr
Endochironornus albipennrs
Glyptotendipes pallens
Microtendrpes pedellus
Parachironornus arcuatus
/ /
I i 1 1 I I I 0-5 0.7 0-9 1 .I 1 -3 1-5 1.7
Log. length of apical tooth (pin)
FIG. 2. Regression of combined width of the inner mandibular teeth against length of the apical tooth.
robust than in the other species, with four pairs of coarse teeth increasing in size distally, and bearing a premandibular brush (Plate IIf). PAR, however, which has two pairs of premandibular teeth at these stages, lacks premandibular brushes (Plate IIIj ).
Head capsule
Differentiation in the shape of the head capsule, as seen in the second to fourth instar, between the carnivorous/parasitic and non-carnivorous larvae, is distinctive. In the former, the head capsule has an oval shape if viewed in dorso-ventral plane, and narrows towards the anterior end (Plates Ile, IIIh). In contrast, its shape in the deposit or filter-feeding larvae is more globular (rounded) (Plates IIa, i, IIId), or even broader towards the anterior end, especially in the obligate
196 J . S . OLAFSSON
0 5
0 4
0.C
- - + A I
0
5 1
A
0-2
0 1
0
-*-*-*-*--
o CHI Chironornus ripanus
CRY Cryplochironornus defectus gr o END Endochironornus albipennis
I GLY Glyptotendlpes pallens
a MIC Microlendipes pedellus
A PAR Parachironornus arcualus
I I I 1 1 2 3 4
lnstar
FIG. 3 . Regression of the ratio ofcombined width of inner mandibular teeth and length of the apical tooth against instar.
miners like Glyptotendipes (Plate IIIa). The shape of the head capsule of the first instar larvae, on the other hand, is more similar to that found in later instars of carnivorous/parasitic larvae of conspecific later instars (Plate Ia).
Discussion
Mandibles
The structure and the size of the chironomid mandibles is one of the characteristics commonly used to distinguish between the different feeding groups (Harnisch, 1923; Chernovski, 1949; Thienemann, 1954). The slender and sickle-shaped mandibles are characteristic for the carnivorous/parasitic species, whereas the more triangular and stoutly formed mandibles are generally found within larvae associated with scraping, deposit- or filter-feeding. The size of the
CHIRONOMID MOUTHPART MORPHOLOGY I97
2.C
1.8
1 6
I
E, - 1 4 f
2 P
a, L
- 3
D c g 1 2
m c c
0 - f 0 p 1 .( m _I
0.1
0.1
0.'
o CHI Chrronornus ripanus
CRY Cryptochironomus defectus gr
END Endochironomus albipennrs
I GLY Glyptotendrpes pallens
A MIC Microtendrpes pedellus
A PAR Parachrronomus arcuatus
/ i
a
,
/
/ /
I I I I I I I 1 1.6 1.8 2 0 2.2 2-4 2.6 2.8 3-0
Log. length of mandible (urn)
FIG. 4. Regression of combined width of the inner mandibular teeth against length of the mandible.
mandibular apical tooth and the combined width of the inner mandibular teeth are amongst characters widely used in taxonomy (Cranston, 1982), as well as for separation into different trophic groups (Harnisch, 1923; Chernovski, 1949; Bryce, 1960). The importance of evolving slender and sickle-shaped mandibles with a prominent apical tooth is obvious in the light of the feeding methods found amongst carnivorous larvae (Morgan, 1949; Luferov, 1956) in terms of the ability of piercing into animal tissues. This type of mandible, with prominent apical tooth and diminishing number of inner mandibular teeth, is found in the majority of species within the Tanypodinae which usually are considered to be carnivorous (Oliver, 1971; Coffman, 1978). It is also found in species within other subfamilies which have evolved towards a carnivorous or parasitic mode of feeding. Is it therefore appropriate to consider an increased number or width of the inner mandibular teeth as an adaptation to detritus or algae feeding?
The comparison of the ratio of IW/ML (Fig. 4) demonstrates clearly the differentiation between
198 J. S. OLAFSSON
1-8
1.6
1.4
- - E, 5 1.2 0
m a
L -
I
-c ISI 5 1 0 - 0,
2
0.8
0.6
0.4
o CHI Chrronornus ripanus
CRY Cryptochironornus defectus gr
0 END Endochfronornus albfpennis
m GLY Glyptoiendipes paifens
A MIC Microfendfpes pedellus
A PAR Parachironornus arcuatus
i 2 9 4
lnstar
FIG. 5. Regression of the apical tooth length against instar
the two feeding groups, carnivorous/parasitic and deposit/filter-feeding, the latter group having a significantly greater IW/ML ratio (Table 11). In other words, a relatively greater area of the mandibles is covered by the inner mandibular teeth, which is the functional scraping area for the larvae. The same pattern appears when the IW is analysed as a function of AL (Figs 2 & 3) where the ratios are greater for the deposit/filter-feeding species than for the carnivorous/parasitic species, with an increasing IW as the larvae grow in the former group. Consequently, the value of the IW is in most cases greater than AL (Table 11) and changes in the allometric growth rate are also greater for the same species (Table 111). This lends support to the idea of the importance of the IW in the detritus or algae feeding process, with an increase in the scraping area of the mandibles.
Further comparison of the morphology of the mandibles leads to further distinctions between the two feeding groups. The lack of the dorsal tooth in the carnivorous/parasitic species CRY and PAR (Plates IIf, IIIk, 1) is an advantage if considered as an adaptation for piercing animal tissue. At the same time the advantage of a dorsal tooth for the deposit/filter-feeding species may be seen
CHIRONOMID MOUTHPART MORPHOLOGY
o CHI Chironomus ripanus
CRY Cryptochrronomus defectus gr.
END Endochironomus albipennis
GLY Glyptotendipes pallens /’ a MIC Microtendipes pedellus i A PAR
I I I 1 2 3 4
lnstar
I99
FIG. 6. Regression of combined width of the inner mandibular teeth against instar.
as an adaptation to increase the scraping area of the mandibles, situated at the end of a spoon- shaped mandible (Plates IIc, k, 1, IIIc, f, g) when seen from inside in lateral view.
The presence of numbers of different types of setae in the mandibular region is one of the characteristics for the detritus- or algal-feeding larvae (Chernovski, 1949; Bryce, 1960). The complex, branched, feathery setae (Fig. 1 b) have been suggested by Chernovski (1949) to have the function of cleaning fine particular matter trapped in the labral region. An additional function of these setae, especially seta interna and pecten mandibularis, may be as a sieve, interacting with the labrum and its setae for trapping particles when feeding. Therefore, the absence of these features in the carnivorous species is apparent in the light of the size of food items they ingest.
The absence of the mandibular setae in the first instar of CHI, END, GLY and MIC, however, is more difficult to explain, not least because of a lack of available data on the food and feeding habits at this life stage. Preliminary results on the diet and particle size ingested by the first instar larvae of some common lentic chironomid species show that the larvae are feeding on relatively (in relation
hl
0
0
TA
BL
E
111
Slat
istic
al r
esul
rs fu
r re
gres
sion
ana
lyse
s an
d th
e an
alys
es fo
r ho
mog
enei
ty of
the
slop
es a
nd in
terc
epts
Log
lW/L
og A
L
Log
(IW
/AL
+ ])
/IN
ST
Log
lW
/Log
ML
Lo
g A
Ljl
NST
AR
Lo
g IW
jlN
STA
R
Log
IW
=Log
a+
b *
Log
AL
N= 13
6,9=
0.96
93 **
*
N =
102
, r2=
0.96
79 *
**
Log
(lW
/AL
+ l)
=L
og a
+ b
* Log
INST
L
og I
W= Log
a+
b *
Log
ML
Log
AL
= L
og a
+b
* Lo
g IN
ST
Log
IW=
Lo
g a
+ b
* Log
INST
IW/A
L=
2900
+0~0
201 *
INST
IW
~-0
~90
11+
1~05
77
* ML
AL
= 0
6477
+0-2
221
* lN
ST
IW=0
.627
7+0.
0259
3 * I
NST
N
= 12
0, r2
=0.9
899
***
N=1
36,r
2=0.
9713
***
N
=136
, r2
=098
82 *
**
N=9
1, r
2=0.
9756
***
N
= 1
02, r
'~0.
9692
***
N=1
31, r
2=0-
9924
***
N=
137
. r2=
0.98
30 *
**
N=137, r2
=0.9
899
***
IW=0
.77
9+02
777
* IN
ST
I W =
.-. 0.
656 +
I ,049
5 M
L N
= 1
49, r
=O,
9896
***
s N
= 14
8, j
-0.9
743
***
N =
146
, r 0
,993
6 **
*
N= 13
1, r
2=0~
9915
***
N =
133
, r2 ~
0.9
65
8 ***
N=
133,
r2=0
.987
6 **
* lW
=O.5
5 +O
19
64 *
INST
IW
= -0
.864
5+0.
9932
ML
AL
=0.7
289+
0.16
58 *
lNST
N
=IM
, r2=
0-95
80 **
* N
= I
I I. r
2-O
-977
4 **
* N
= 1
10, r
=0.
9577
***
% 5'
CH
I IW
= -0
. 94
8-b
1,13
96 *
AL
CR
Y
1W= -0.3068+0'9956 *
AL
1 W/A
L - 0.1
700 +
Om07
* IN
ST
IW=
-0-8
617+
0950
5 * M
L A
L=0.
8553
+0.1
987
* lN
ST
1W=0
,533
0 +
0201
5 * I
NST
?
END
1W
=0,0
3 + 1
.083
7 * A
L
N=
136
. r
=0.4
328
***
N=
102
, r2=
0,00
39 N
S IW
/AL=
34
32+0
,011
8 * I
NST
1W
= -0
.717
5+0.
9799
* M
L A
L=0
.704
1+0.
2038
* IN
ST
IW=0
.783
4+0.
2247
* IN
ST
N= 13
6, r
=0,2
543
***
IW/A
L=0,
3146
+0*
0357
* IN
ST
N=
148
. r2=
0.72
87 *
**
N =
133
, r2=
0.28
31 *
**
lW/A
L e
0.22
06 +
0.01 2
4 *
I NST
N
=II
O. r2
=0.3
i31
***
N=1
03,r
2=0.
9690
***
v 0
N-137, r
54 =0.9
732
***
I'
Y'
AL
=O 7
4 5+
0.21
73 *
INST
1W
= -0.
4134
- 1,2
513
AL
N
= 1
48, r
=0,
9758
***
N=
133
, r2=
0.95
63 *
**
IW=
-0-2
824+
1.1
527
* AL
N= 11
0, r2
=0.9
S1S
***
5 G
LY
MIC
1W
=0079l+ 1
.,104
0 * A
t lW
/AL
=0~3
656+
0~01
87 * lN
ST
1W =
- 0.
7992
+ I '0
433
* M L
AL
=0.5
868+
0.21
89 *
INST
1W
=0~7
071+
0~24
99 * lN
ST
PAR
SLO
PE
*I*
INTE
RC
EPT
1..
GLY
>P
AR
=CH
I = M
IC=
EN
DzC
RY
CL
Y >
CH
I = M
IC=
PAR
= EN
D
CH
I =G
LY
= M
IC>
PAR
= EN
D=C
RY
C
HI=
MIC
=GL
Y >
EN
D>C
UY
>P
AR
G
LY >
CH
I > M
IC>
EN
D>
CRY
=PA
R
MlC
> E
ND
>CH
I >G
LY
>P
AR
>CR
Y
MIC
> E
ND
> G
LY
> C
HI >
PA
R
END
> MLC >
CR
Y >
PA
R>
GLY
> C
HI
CR
Y >
GL
Y >
PA
R ;. E
ND
> C
HI >
MIC
E
ND
> GL
Y >
MIC
> CH
I > P
AR
=CR
Y
*** o
r'z'
.P<
0,00
1 N
S or
'='
Not
sig
nific
ant
CHIRONOMID MOUTHPART MORPHOLOGY 20 I
TABLE IV Comparison between certain characters in the mouthparts of the jirst and fourth instar chironomid larvae
Chironomus riparius Cryptochironomus akfectus gr. Endochironomusalbipennis Glyptotendipes pallens Microtendipes pedelfus Parachironomus arcuatus
Chironomus riparius Cryprochironomusdefectusgr. Endochironomusalbipennis Glyptotendipes pallens Microtendipes pedellus Parachironomus arcuatus
Character species
I 3 + - - + ~ b + + c b 2 - I convex I I 3 + - - + c b + + a b 2 - ' convex I 3 + - - + ~ b + + c b 2 - I convex 1 3 + - - + c b + + a b 2 - convex 1 3 - - - + a a + + a - 3 - ' convex
I V 3 + c c b c a + + c b c 2 + convex IV 2 - - a/b b a a + + a b a/b 4 + concave IV 3 + c c b c c + + c b c 3 + convex I V 3 + c c b c a + + c b c 2 + convex I V 3 + c c b c b + + c b c 3 + convex I V 2 - - a b a a + + - a / b - 2 - convex
CT .. 9
I
=1 A E
4" I u
E, 8
4 2 9
to the mouthpart size) large particles (i.e. diatoms) in combination with detritus. In the cases of Procladius and Tunypus, the gut content almost entirely comprises large species of diatoms like Cymatopleura and Surirella (Olafsson, unpubl. data), which in some cases are as long as a quarter of the larval length. This could to a degree explain the lack of, or poorly developed, features like mandibular and labral setae and possession of a prominent apical tooth within the first instars.
Labrum
The divergence in the morphology of the labrum between the two feeding groups is very significant, but less so between conspecific instars (Plates 1-111). The detailed morphology reflects that seen in the mandibles, where certain features like the labral setae are better developed in the deposit/filter-feeding species than in the carnivorous/parasitic ones (Plates 11-111). Bryce (1960)
202 J. S. OLAFSSON
suggests the main function of the labrum in the feeding process is an aid for pushing the food back to the oesophagus. Therefore, it possibly acts to prevent fine particles, including bacteria, falling out while feeding. The seta interna and the pecten mandibularis, in conjunction with those of the labral setae, form a fine-meshed sieve when the labrum is pushed backwards. The lack of these features in the carnivorous/parasitic species possibly reflects their adaptations to the relatively larger food items ingested. The function of the long, slender labral setae found in CRY and PAR (Plates IIf, g, IIIi, j) is difficult to explain other than as homologous to the long retractable antenna in Tanypodinae, adapted for sensing prey.
Premandibles
The function of the premandibles is not well known. From their structure and positions in the labral region, it is likely that they serve both to strengthen the labrum while pushing back food items, as well as to brush away trapped particles from the labral setae and move them towards the oesophagus. In the case of the carnivorous/parasitic species, the premandibles may also play a role in tearing animal tissue while the prey is kept with the prominent apical teeth, thus being functionally homologous to the ligula in Tanypodinae.
Conclusion
There appears to be a very significant difference in the mouthpart morphology between the two larval feeding groups. The differences observed within such closely related species, occupying similar types of habitat, raises the question about the course of the evolutionary divergence and convergence seen within the family of Chironomidae. For instance, the carnivorous species of Chironomini, i.e. Cryptochironomus, may be regarded as having convergent evolution to the larvae of Tanypodinae in terms of feeding and feeding behaviour. Even though the first instar larvae may resemble the later conspecific instars in many ways, they are generally more similar on interspecific level, as indeed has been documented earlier (Kalugina, 1959; Oliver, 1971).
The similarity in the morphology observed between the first instar larvae poses the question whether this is reflected in their microdistribution, as well as in the food and feeding behaviour. No precise information is available concerning either of these problems. However, throughout the chironomid literature, the first instar larvae have generally been cited as planktonic (Oliver, 1971; Davies, 1974, 1976) and as feeding on suspended material (Alekseev, 1965). Preliminary results on the microdistribution and the diet of the first instar larvae of some common lentic species show: first, that they are distributed in the semi-aqueous and mucilaginous top centimetre of the sediment, and secondly, that they are mainly feeding on detritus and diatoms or entirely on large species of diatoms as mentioned earlier (Olafsson, unpubl. data).
The changes in the mouthpart morphology appear to be greater amongst the deposit/filter- feeding species throughout their life-cycle than is observed amongst the carnivorous/parasitic species. This is evident in the fine structure of both the mandibles and the labrum, as well as in the allometric growth rate. That evokes the question whether these changes actually reflect the larval diet, i.e. the particle size ingested. That is, whether, amongst the carnivorous/parasitic larvae, the small changes in the morphology of the mouthparts throughout the larval stages are associated with a constant particle size ingested, in relation to larval mouthpart size. Whereas, in the deposit/ filter-feeding species, those changes occurring throughout the larval stages perhaps account for
CHIRONOMID MOUTHPART MORPHOLOGY 203
increasing demand in efficiency of ingesting relatively smaller particles, in relation to the size of the larval mouthparts (i.e. detritus or diatoms).
The morphology of the mouthparts of the first instar larvae resembles in many ways that found within the carnivorous/parastic species, in terms of morphometry of the mandibles, i.e. IW/AL and IW/ML ratios (Table 11), and the lack of, or poor development of, the setae. Might these similarities be interpreted as an adaptive feature in both cases to relatively large food particles ingested? In other words, the first instar larvae of all species might exhibit raptorial feeding, while the non-carnivorous species develop more specialized feeding strategies like filter-feeding, scraping or deposit feeding in their later instars.
This work has been supported by Foreign Commonwealth Scholarship and student loan from the Student Loan Foundation, Iceland, which the author greatly acknowledges. The author wants also to thank Mr Luscombe for reading the manuscript at the early stage, Dr Hutchinson for statistical advice and D r Wilson for encouragement during the work and useful criticism of this paper.
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