Natalie Baeumler, Gerhard Haszprunar and Bernhard Ruthensteiner

Overlap in appearance of the protonephridia
and the metanephridial system in a mollusc
Natalie Baeumler, Gerhard Haszprunar and Bernhard Ruthensteiner
Fig. 1. Lepidochitona
corrugata, juvenile.
Zoologische Staatssammlung München
Introduction:
As typical for many spiralian taxa, in the polyplacophoran mollusc Lepidochitona corrugata two types of excretory systems are formed during development: first one pair of
anteriorly situated, larval-juvenile protonephridia (head kidneys) and then the posteriorly located, juvenile-adult metanephridial system.
Fig. 2. Surface renderings of serial sections (Amira software) of a larva (A) and of postmetamorphic juveniles (B-G) of
Lepidochitona corrugata.
Protonephridia
Results:
G
Metanephridial system
protonephridial kidney
pericardium
renopericardial duct
efferent nephroduct
metanephridial kidney
terminal portion
F
E
efferent nephroduct
eye
D
C
B
A
100 µm
Metanephridial System
Protonephridia
A
oe
st
dgl
r
dgl
pk
Fig. 3. Protonephridia of Lepidochitona
corrugata. A. Cross section through
whole animal, re-sectioned for TEM in
B-D. Framed areas enlarged in other
figure parts. B. Left protonephridial
kidney. C. Protonephridial lumen. D.
Basal infoldings of protonephridial
kidney cells. E. Terminal portion of right
B
protonephridium with ciliary flame. F.
Ultrafiltration site. For abbreviations
50 µm see below.
B
C
lln
Fig. 4. Metanephridial system of
Lepidochitona corrugata. A. Cross
section through whole animal, resectioned for TEM in B-D. Framed
areas enlarged in other figure parts. B.
Right metanephridial kidney. C.
Metanephridial lumen. D. Basal
infoldings of metanephridial kidney
cells. E. Ventral wall of pericardium. F.
mk
Ultrafiltration site. For abbreviations
50 µm see below.
A
i
B
dgl
re
B
mv
C
va
i
nu
ci
va
C
mi
va
ci
mv
mi
va
C
1 µm
1 µm
D
dgl
D
D
va
D
mu
mi
dgl
va
dgl
dgl
va
mu
bb
E
uf
1 µm
5 µm
1 µm
10 µm
E
F
lp
F
mv
F
uf
pd
us
nu
pd
cf
mu
mi
us
F
mv
bc
bm
1 µm
1 µm
mk
bm
mu
1 µm
1 µm
Abbreviations: bb - basal body, bc - body cavity, bm - basal membrane, cf - ciliary flame, ci - cilium, dgl - digestive gland, i - intestine, lln - left lateral nerve cord, lp - lumen
of pericardium, mi - mitochondrion, mk - metanephridial kidney, mu - muscle fibre, mv - microvilli, nu - nucleus, oe - oesophagus, pd - pedicle, pk - protonephridial
kidney, r - radula, re - rectum, st - stomach, uf - ultrafiltration site, us - ultrafiltration slit, va - vacuole.
Each protonephridium is
composed of three portions
(Fig. 2): 1) The tube-like
terminal portion with the
ultrafiltration sites (Fig. 3E,F),
2) the prominent protonephridial kidney (Fig.3A)
and 3) the efferent nephroduct. The protonephridia
exhibit two remarkable
features: 1) They achieve
their peak level of
development (size, structural
differentiation) after
metamorphosis, thus in the
juvenile life phase (Fig. 2BG). 2) With the protonephridial kidneys the organs
form voluminous, pouch-like
differentiations in the duct,
previously unknown from
molluscan protonephridia
(Fig. 3A-D).
The metanephridial system is
made of the pericardium with
e n c l o s e d h e a r t , pa i r e d
kidneys, paired renopericardial ducts and paired
efferent nephroducts (Fig.
2E-G). Ultrafiltration sites can
be found in the ventral wall of
the pericardium (Fig. 4E,F).
Both organ complexes, the
protonephridia and the
m e ta n e p h r i d i a l s y s t e m ,
overlap in presence for a
substantial period during
juvenile development (Fig. 2)
to ensure continuous function
of excretion.
The protonephridia and the
meta-nephridial system show
striking resemblances in
organization. These include
the composition of the
“kidneys” (Fig. 3A,B, 4A,B) several highly characteristic
cells surrounding a ramified
excretional lumen (Fig. 3C,
4C) that contains single
scattered cilia and is densely
packed with microvilli. The
kidney cells are characterized
by an extensive apical microvillous border, a strong
vacuolization (Fig. 3B, 4B), a
mitochondria-rich cytoplasm, basal nuclei and
extensive basal infoldings
(Fig. 3D, 4D) that probably
represent reabsorptive
differentiations. The
similarities also include the
ultrafiltration sites with slits
between regularly arranged
pedicles (Fig. 3F, 4F).
Conclusions:
The close similarities of components of the protonephridia and of the metanephridial system respectively let the often accentuated differences between both excretory
systems become more and more blurred. These resemblances in organisation indicate that there is a serial (iterative) homology of protonephridia and the metanephridial
system at the level of organs within the Mollusca. Protonephridia might even be present in adult molluscs. The anterior pair of kidneys of adult monoplacophorans that lack a
connection to the pericardium may represent such organs.
This study was kindly supported by the DFG (RU-895/4-1).