Zoomorphology (1982) 101:17-38
Zoomorphology
© Springer-Verlag 1982
Functional Morphology of the Mouthparts
and Associated Structures
of Pagurus rubricatus (Crustacea:
Decapoda: Anomura) with Special
Reference to Feeding and Grooming
Patrick J. Schembri*
Portobello Marine Laboratory, P.O. Box 8, Portobello, New Zealand
Summary. Pagurus rubricatus is predatory, detrivorous, macrophagous,
and to a small degree, a suspension feeder. The crab searches for small
invertebrates by digging shallow pits in the sediment. During this process
it feeds on detritus obtained either directly from the sediment or scoured
off gravel granules. Particles trapped by the dense setation of the 2nd
and 3rd maxillipeds are brushed off and ingested.
The distribution of the various types of setae on the mouthparts
is mapped and structure of the mouthparts and their setae is correlated
with function. Sediment collected by the pereiopods is brushed off by
the endopodites of the 3rd maxillipeds and transferred to the inner
mouthparts by the endopodites of the 2nd maxillipeds. The basipodites
of the I st maxillae form a filter screen through which particles of suitable
size are pushed by the 2nd maxillae. Rejected particles are discarded
by the exhalant stream via the currents generated by the exopodites
of the maxillipeds. Specialized setae on the 2nd maxillae scour detritus
from the surface of gravel granules applied to these appendages by the
2nd and 3rd maxillipeds. Interlocking setae from different appendages
form a number of screens the main function of which is to retain material
in the buccal region. The exopodite and endopodite of the 1st maxilliped
and the endopodites of the 1st and 2nd maxillipeds form a channel
which funnels the exhalant respiratory current away from the crab. The
main grooming appendages are the endopodites of the 3rd maxillipeds,
however, most of the other mouthparts have a self-cleaning function.
A. Introduction
Hermit crabs have classically been described as omnivorous scavengers or
as detritus-feeders (Thompson 1904; Jackson 1913; Brock 1926; Orton
1927). More recent studies have shown, however, that members of this
* P r e s e n t address."
72, Brared Street, B'Kara, Malta
0340-6725/82/0101/0017/$04.40
18
P.J. Schembri
group employ a variety of feeding techniques including deposit-feeding, macrophagy, predation and suspension feeding (Boltt 1961; Roberts 1968;
Greenwood 1972; Caine 1975, 1980; Gerlach et al. 1976; Schuhmacher
1977; Markham 1977; Kunze and Anderson 1979). While each species appears to have a preferred food source, most are able to feed in a number
of ways and will switch from one feeding technique to another in order
to exploit whatever food is readily available at the time (Kunze and Anderson 1979). This broad repertoire of feeding techniques in a single animal
has led to an interest in the morphology of the feeding apparatus and
in the adaptations for food gathering and processing.
Early purely morphological descriptions of hermit crab feeding structures have now been supplemented by studies on feeding behaviour and
feeding adaptations in a number of species. However, few workers have
attempted a functional analysis of the feeding structures. Greenwood (1972)
has related differences in mouthpart setation between Pagurus novaezelandiae and Stratiotes ( = Paguristes) setosus to differences in feeding habits.
Caine (1975) in his study of the relationships between diet and feeding
mechanism and gastric mill morphology in anomurans found some correlation between the morphology of the mouthparts and chelipeds and feeding
activity for the four species of pagurids he studied. The most detailed study
of hermit crab mouthpart functional morphology is that of Kunze and
Anderson (1979). These authors studied four species of hermit crabs of
the superfamily Coenobitoidea and for each described the structure of the
mouthparts and proventriculus, mapped the distribution of the setae on
the mouthparts and described feeding behaviour. They related structure
to function and discussed their findings in the light of previous studies
on feeding in hermit crabs.
As part of a study on the feeding adaptations of New Zealand hermit
crabs, the functional morphology of the feeding structures of Pagurus rubricatus 1 was investigated.
P. rubricatus was found to be detrivorous, macrophagous, predatory
and to a small extent a suspension feeder. Several important differences
were found between this species and those studied by Kunze and Anderson
(1979). In particular, P. rubricatus has a wider range of feeding mechanisms
than any of the species studied by these authors, the setation of the mouthparts of P. rubricatus is more complex, the distribution of the setae is different and the mechanisms of handling, reduction and ingestion of the food
and of particle selection also differ. One method of feeding used by P.
rubricatus (' gravel-scrubbing') has not been previously described for hermit
crabs.
This paper describes the feeding behaviour and morphology of the
feeding and associated structures of P. rubricatus paying particular attention
to the type and distribution of the setae. A functional analysis of the mouth1 The taxonomy of the New Zealand hermit crab fauna is currently under revision. Pagurus
rubricatus (Henderson 1888) together with P. spinulimanus (Miers 5876) and the Miocene
fossil P. clifdenensis Hyden and Forest 1980, will be transferred to a new genus (Hyden
and Forest 1980)
Functional Morphology of the Mouthparts of a Hermit Crab
19
parts a n d the role their setae play in feeding a n d the associated activities
o f g r o o m i n g a n d generation o f water currents is given, c o m p l e m e n t i n g a n d
extending the observations o f K u n z e a n d A n d e r s o n (1979).
B. Material and Methods
Hermit crabs were collected by trawling off Otago Peninsula, South Island, New Zealand
at depths of 60-90 m. The bottom in this region consists of gravels, sandy gravels and gravelly
sands rich in organic skeletal debris (Andrews 1973; Probert et al. 1979). In the laboratory
the crabs were kept on their natural substratum in holding tanks supplied with running seawater
and fed at irregular intervals on polychaete worms and crushed bivalves.
For observation, individual crabs were placed in small (24 x 19 x 13 cm) 'Perspex' aquaria
containing either mud, sand, gravel or the crabs' natural substratum. At least 5 crabs were
observed on each substratum type. Gross observations of feeding behaviour were made in
a darkroom using a 15 W red lamp as the only source of illumination. Detailed observations
were made using a travelling stereomicroscope. Water currents were traced using suspensions
of either fine mud particles or milk in seawater.
The gross morphology of the buccal apparatus was studied by dissection of animals narcotized in fresh water and then killed and fixed in 70% ethanol. Examination of partial dissections
of the buccal region and animals cut in various planes, cleared in either glycerol or cedar
wood oil and stained with haematoxylin proved useful in working out the relative arrangement
of the appendages and their setation. Some 10 crabs were used for these detailed observations.
Individual mouthparts were dissected out, stained with lignin pink and examined under
a stereomicroscope. Setae were studied using an SEM. For this selected structures were fixed
in 70% ethanol, dehydrated, dried in a critical point drier, then mounted on aluminium stubs
using colloidal graphite, coated with gold and examined in a Siemens Autoscan SEM.
C. Results
L Feeding Behaviour
P. rubricatus is d e t r i v o r o u s a n d p r e d a t o r y . T h e crabs feed o n sediment
by excavating shallow trenches in the s u b s t r a t u m using the m i n o r (left)
cheliped and the walking legs. The e x p a n d e d o u t e r edge o f the p r o p o d i t e
o f the m i n o r cheliped is dug into the sediment and the whole cheliped
then pushed o u t w a r d s away f r o m the crab. The m a n u s functions as a shovel
pushing sediment in f r o n t o f it (Fig. 1A). A t the same time, the dactyls
o f the 2nd a n d 3rd p e r e i o p o d s scoop sediment in f r o m the sides a n d kick
it inwards u n d e r n e a t h the shell and u p w a r d s towards the 3rd maxillipeds
which collect it and transfer it to the o t h e r m o u t h p a r t s (Fig. 1 A). B o t h
pairs o f walking legs are used and the usual sequence o f events is: m i n o r
chela push, right 3rd p e r e i o p o d kick, right 2nd p e r e i o p o d kick, left 3rd
p e r e i o p o d kick, m i n o r chela p u s h ... etc. T h e m a j o r (right) cheliped is rarely
used to p u s h away sediment. As the crabs dig, they m o v e slowly backwards
giving rise to characteristic trenches which m a y be u p to 2 cm deep.
A t intervals, the crabs stop digging and the m i n o r chela is used to scoop
u p pincerfuls o f sediment a n d transfer t h e m to the m o u t h p a r t s . T h e tip
o f the m a n u s is planted firmly in the sediment and the whole cheliped
is flexed such that sediment is collected on the concave ventral surface
o f the m a n u s which is b r o u g h t to lie u n d e r n e a t h the 3rd maxillipeds
(Fig. 1 B). T h e 3rd maxillipeds then transfer the sediment to the o t h e r
20
P.J. Schembri
~
:
~
"
A
J
C
Fig. 1 A-C. Feeding behaviour of Pagurus rubrieatus. A crab feeding on sediment. The minor
chela pushes away surface sediment (arrow). The left 3rd pereiopod kicks sediment towards
the 3rd maxillipeds. B crab brushing off detritus from the concave internal face of the minor
chela using the 3rd maxillipeds. C 'gravel-scrubbing'. A gravel granule is cradled by the endopodites of the 2rid and 3rd maxillipeds while it is brushed by the inner mouthparts. The
maxitlipeds manipulate the granule and cause it to rotate in the direction shown by the arrow
Functional Morphologyof the Mouthparts of a Hermit Crab
21
mouthparts, the left 3rd maxilliped brushing particles from the ventral surface of the manus and the right 3rd maxilliped brushing the dorsal surface
(Fig. 1 B).
Detritus is also obtained by a process best described as 'gravel-scrubbing'. Single pieces of gravel, shell fragments or other skeletal debris are
picked out from the sediment by the minor chela and transferred to the
mouthparts. The 2nd and 3rd maxillipeds manipulate the selected sediment
granule and apply it against the inner mouthparts which perform vigorous
brushing movements, after which the granule is discarded (Fig. 1 C). Pieces
of skeletal material too large to be conveniently handled by the maxillipeds
are crushed into smaller fragments by the major chela and each fragment
is then scrubbed in turn.
Small gastropods and bivalves exposed during the digging activities of
the crab are seized by the minor chela and cracked open by the major
chela. The major chela is then used to hold the prey while the minor chela
tears off pieces of flesh and transfers them to the mouthparts. Fragments
of the cracked shells are transferred to the mouthparts and scrubbed in
the same way as pieces of gravel.
When not foraging thus, P. rubricatus holds the densely setose endopodites of the 2nd and 3rd maxillipeds folded in front of the buccal region
to form a screen. Beating of the exopodites of the maxillipeds creates a
current of water which passes through this screen (Fig. 11). Particles carried
in this current are trapped by the maxilliped setae and periodically brushed
off and ingested.
II. Functional Morphology of the Buccal Structures
The structure of the mouthparts of P. rubricatus and the distribution of
the various setal types on them are shown in Figs. 2-7. Different authors
have used different nomenclatural schemes for decapod setae. The most
widely used appears to be that of Thomas (1970) as modified by Factor
(1978) and this is the scheme used here. In Figs. 2-7 setae intermediate
between two of Factor's types are indicated by a slant line (e.g. E/G).
Setae which have no equivalent in Factor's scheme are indicated by an
asterisk (e.g. A*). To facilitate comparison between the present work and
that of Kunze and Anderson (1979), the equivalent nomenclature of these
authors' setal types 1-8 is given below:
Type 1-type I simple; type 2 = type F1 serrulate; types 3 and 4 are both
variations of type D1 serrate setae; type 5 = t y p e B2 pappose; type 6 =
type A plumose; type 7 = t y p e H1 cuspidate and type 8 are short type D1
serrate setae.
In the following descriptions, the inner surface of an appendage is that
facing the mouth while the outer surface is that opposite. The terms medial
and lateral are used in a morphological sense to distinguish between the
two edges of an appendage when straightened. The medial edge is that
nearest the midline of the body and the lateral edge is that opposite. Upward
22
P.J. Schembri
E
l
/
11°°
Fig. 2. Pagurus rubricatus. Mandibles and right
mandibular palp (inset) in external view. l, left
mandible; mp, mandibular palp; r, right
mandible. The remaining symbol refers to the
setal nomenclature scheme of Factor (1978) (see
text)
C1
I1
H1
end---~ ~/"
ba~
Ilmm
~.~-F1
Fig. 3. Pagurus rubricatus. Right 1st maxilla
in external view. bas, basipodite; cox,
coxopodite; end, endopodite. The remaining
symbols refer to the setal nomenclature
scheme of Factor (1978)
and d o w n w a r d movements refer to movements in the direction of the tip
and the base of the mouthpart respectively.
I l L Feeding
The mouthparts and other associated structures together with their setal
complexes form a number of functionally discrete structural units which
divide the space in front of the mouth into three regions here termed the
posterior, mid and anterior buccal spaces.
The posterior buccal space lies immediately in front of the mouth and
is delimited by the labrum and mandibular palps dorsally, by the molar
process, palp and incisor process of the mandibles laterally and by the
bodywall, paragnaths and setae of the ventral mid-buccal screen (see below)
ventrally (Fig. 8). During feeding the mandibles are normally held slightly
apart giving free access to the mouth. On the distal segment of the mandibular palps are numerous rows of type E triserrate setae which point towards
its tip (Fig. 2). When feeding on fine material the two mandibular palps
Functional Morphology of the Mouthparts of a Hermit Crab
23
F1
(a) E/G;Cl
i
Fig. 4. Pagurus rubricatus. Right
2nd maxilla in external view. has,
basipodite; cox, coxopodite; end,
endopodite; scaph,
scaphognathite. The remaining
symbols refer to the setal
nomenclature scheme of Factor
(1978). Setal fields on the internal
face of the appendage are
indicated by broken arrows. For
the medial edge setae the outer,
middle and inner setal fields are
labelled (a), (b) and (c).
respectively
Fig. 5A, B. Pagurus rubricatus.
A Right 1st maxilliped in external
view. B Coxopodite of right 1st
maxilliped in internal view. bas,
basipodite; cox, coxopodite; end,
endopodite; exo, exopodite; f/,
flagellum. The remaining symbols
refer to the setal nomenclature
scheme of Factor (1978). The
broken arrow indicates a setal
field on the internal face of the
appendage
a C2
g
<y,c,°,
\
"
cox
X
cl
scaph
r|
C3
are applied against each other such that the fields of setae on their morphologically lateral edges intermesh to form a screen which prevents particles
from escaping dorsally from the posterior buccal space (Fig. 9). During
biting the palps together with the labrum hold the food steady while the
mandibles slice through it.
24
P.J. Schembri
The mid-buccal space is delimited by the 1st and 2nd maxillae the basipodites and coxopodites of which form two functionally distinct units (Fig. 8).
Each basipodite of the 1st maxillae bears four rows of type H1 cuspidate
setae on its medial edge (Fig. 12A). The outermost row consists of stout,
widely spaced setae which point medially. Staggered behind these is a double
row of more slender setae which also point medially. Behind this double
row is a single row of setae which point slightly backwards and arranged
in such a way that each inner row seta is approximately in line with an
outer row seta (Fig. 12A). When the left and right basipodites of the 1st
maxillae are applied against each other these rows of cuspidate setae form
a grating in front of the mouth (Figs. 8 and 9), which serves as a filter.
Particles are pushed through the grating by the basipodites of the 2nd
maxillae. Subterminally along their inner faces these bear a row of type E
triserrate setae (Fig. 4), which curve backwards and intermesh with the grating setae of the 1st maxillae (Figs. 8 and 9). With each stroke of the 2nd
maxillae, these triserrate setae push material through the grating and into
the mouth. Because the triserrate setae point slightly upwards, particles
too large to pass through the grating are progressively pushed upwards
until they are discarded via the rejection current. The triserrate setae of
the basipodites of the 2nd maxillae have the additional function of abrading
the food during macrophagous feeding.
Medially the basipodites of the 2nd maxillae bear numerous rows of
specialized simple setae (I* setae) which have recurved and slightly flattened
tips (Fig. 12 B). These are reminiscent of the spoon-tipped setae of ocypodid
crabs (Miller 1961) and have the similar function of scouring off detritus
from the surface of large granules during 'gravel-scrubbing'. Subterminally
along the outer medial edge of the basipodites there is a row of forward
pointing setae which are intermediate between type G triserrulate and type E
triserrate (Fig. 4). These have the double function of forming a screen between the basipodites of the 2nd maxillae and those of the 1st maxilliped
(Fig. 9) and of abrading soft material as the 2nd maxillae beat.
Fields of setae on the coxopodites of the 1st and 2nd maxillae intermesh
with each other and with very long backwardly directed setae from the
coxopodite of the 1st maxilliped to form the floor of the mid-buccal space
and continue backwards through the gap between the mandibles to form
part of the floor of the posterior buccal space (Fig. 8). The coxopodites
of the 1st maxillae are flattened flap-like structures which curve orally
(Fig. 3). Along their medial edges these carry a mixture of long type H2
cuspidate and type E triserrate setae and shorter type C1 and C3 plumodenticulate setae. More ventrally type C4 plumodenticulate setae predominate
(Fig. 3). All these setae intermesh with those of the opposite appendage
and with setae from the coxopodites of the 2nd maxillae. The longest setae
also intermesh with the very long type C3 plumodenticulate setae of the
coxopodites of the 1st maxillipeds and pass backwards into the posterior
buccal space (Fig. 8). Type F1 serrulate setae on that edge of the coxopodite
just beneath the head of the basipodite intermesh with similar setae on
the neck of the basipodite to fill the gap between these two segments (Fig. 3).
Functional Morphology of the Mouthparts of a Hermit Crab
25
On their medial edges the coxopodites of the 2nd maxillae bear two
rows of setae. The outer row consists mainly of type G triserrulate setae
with a few type E triserrate and type C1 plumodenticulate setae (Fig. 4).
These setae point medially and intermesh with those of the opposite appendage. The inner row consists of type D3 serrate setae which curve backwards
and intermesh with the medial edge setae of the coxopodites of the 1st
maxillae and with the very long setae of the coxopodite of the 1st maxilliped
(Figs. 4 and 8). This complex of intermeshing setae forms a screen beneath
the basipodites of the 1st and 2nd maxillae and prevents particles from
falling out ventrally from the mid-buccal space (Fig. 8).
The 1st, 2nd and 3rd maxillipeds delimit the anterior buccal space which,
like the mid-buccal space, may be divided into functionally distinct dorsal
and ventral regions (Fig. 8). The basipodites of the 1st maxillipeds are doorlike structures which bear fields of setae along their medial edges (Fig. 5).
These setae consist of long type H1 and H2 cuspidate, type G triserrulate
and types intermediate between the two. Interspersed amongst these are
shorter type G triserrulate and type C1 plumodenticulate setae. All these
setae curve towards the mouth and intermesh with the corresponding setae
of the opposite basipodite to form a setal screen which separates the anterior
buccal space from the mid-buccal space (Fig. 9). The curvature of the screen
setae and the arrangement of their setules is such that material may pass
through the screen in the direction of the mouth but not in the reverse
direction.
The fingers (i.e. the dactyl, propodite and carpopodite) of the 2nd and
3rd maxillipeds have analogous functions during feeding. Those of the 3rd
maxillipeds transfer material from the chelae and walking legs to the anterior
buccal space while those of the 2nd maxillipeds push this material posteriorly
into the mid-buccal space -through the screen separating these two regions.
In addition, during 'gravel-scrubbing' or macrophagous feeding the fingers
of the 2nd and 3rd maxillipeds firmly press the food or sediment granule
against the inner mouthparts (Fig. 1 C).
The propodite and dactyl of the 2nd maxillipeds bear fields of serrate
and serrulate setae along their morphologically medial edges and on their
inner faces (Figs. 6A and B). These setae are used as combs to brush material
from the fingers of the 3rd maxillipeds. When the endopodites of the 2nd
maxillipeds are folded, the setae on the morphologically medial edges of
the dactyl and propodite intermesh with those of the opposite segments;
the long type G triserrulate setae situated dorsally on the morphologically
lateral edge of the propodite intermesh with the corresponding setae of
the opposite propodite. The two fingers thus form a roof to the anterior
buccal space (Fig. 8). The long cuspidate setae of the dactyls are used to
grip the food during macrophagous feeding.
The fingers of the 3rd maxillipeds have fields of serrate, serrulate and
plumodenticulate setae of a variety of types along both edges of the dactyl,
on the morphologically medial edges of the propodite and carpopodite,
and on the inner faces of all three segments (Figs. 7A and B). These setae
function in scraping material from the pereiopods and transferring it to
Fig. 6A, B. Pagurus rubrieatus. A Right 2nd maxilliped in external view. B Finger of right
2rid maxilliped in internal view. bas.is, basi-ischiopodite; car, carpopodite; cox, coxopodite;
dac, dactylopodite; exo, exopodite; fl, flagellum; mer, meropodite; prop, propodite. The remaining symbols refer to the setal nomenclature scheme of Factor (1978). For the medial
edge setae the outer and inner setal fields are labelled (a) and (b) respectively
F1
.~dac
dac~ ~
D1;D2
f
~,F1.~;~ C1;C3;F2;G .)<'~'7"~,'.~
fl
A
D2;D3
F/
D1;~G
~ "=~,~.~F1;G;E/G F1;F3;D1;D2;C3;E/G
~
A
D2"~~
prop
*
\~/
Fig. 7A, B. Pagurus rubrkatus. A Right 3rd maxilliped in external view. B Endopodite of
right 3rd maxilliped in internal view. bas, basipodite; car, carpopodite; cox, coxopodite; dac,
dactylopodite; exo, exopodite; f/, flagellum; is, ischiopodite; mer, meropodite; prop, propodite.
The remaining symbols refer to the setal nomenclature scheme of Factor (1978). In B setal
insertions on the finger are indicated by dots
27
Functional Morphology of the Mouthparts of a Hermit Crab
mer.mxp3
ba
b~
xp3
pl
p3
Fig. 8. Sagittal section through the buccal region of Pagurus rubricatus showing the relative
arrangement of the mouthparts of the left side. For clarity fewer setae than actually present
are shown, bas.mxl, basipodite of the 1st maxilla; bas.mx2, basipodite of the 2nd maxilla;
bas.mxpl, basipodite of the 1st maxilliped; bas.mxp3, basipodite of the 3rd maxilliped;
car.mxp2, carpopodite of the 2nd maxilliped, car.mxp3, carpopodite of the 3rd maxilliped;
cd, crista dentata; cox.mxl, coxopodite of the 1st maxilla; cox.rex2, coxopodite of the 2nd
maxilla; cox.mxpl, coxopodite of the 1st maxilliped; cox.p1, coxopodite of the cheliped;
dac.mxp2, dactylopodite of the 2nd maxilliped; dac.mxp3, dactylopodite of the 3rd maxilliped;
ip, incisor process; mer.mxp3, meropodite of the 3rd maxilliped; mop, molar process; mp,
mandibular palp; prop.mxp2, propodite of the 2nd maxilliped; prop.rnxp3, propodite of the
3rd maxilliped; ster, 8th thoracic stermite
the other mouthparts (Fig. 1 B). When the endopodites are folded, the
fingers of the 3rd maxillipeds come to lie under those of the 2nd maxillipeds
and between the coxopodites of the chelipeds. The fields of setae on the
inner faces of the fingers intermesh with those of the opposite appendage
while long setae at the tips of the dactyls intermesh with upward pointing
setae from the medial edges of the coxopodites of the chelipeds to form
the outer wall of the anterior buccal space (Fig. 8).
Ventrally, the anterior buccal space is delimited by the coxopodites of
the 1st, 2nd and 3rd maxillipeds. Setae from these segments and from the
8th sternite (i.e. that bearing the 3rd maxillipeds) intermesh to form a floor
to the anterior buccal space (Fig. 8). The coxopodites of the 1st maxillipeds
are shaped like truncated cones (Fig. 5A). On their medial surfaces there
28
P.J. Schembri
scaph
Fig. 9. Transverse section through the buccal region of Pagurus rubricatus in the plane indicated
by the arrows in Fig. 8. bas.mxl, basipodite of the 1st maxilla; bas.mx2, basipodite of the
2nd maxilla; bas.rnxpl, basipodite of the 1st maxilliped; bstr, branchiostegite; bw, body wall;
cd, crista dentata; end. mxl, endopodite of the 1st maxilla; end.mx2, endopodite of the 2nd
maxilla; end.mxpl, endopodite of the 1st maxilliped; exo.mxpl, exopodite of the 1st maxilliped;
exo.mxp2, exopodite of the 2nd maxilliped; exo.mxp3, exopodite of the 3rd maxilliped; lb,
labrum; rn, mandible; mer.mxp2, meropodite of the 2nd maxiUiped; mer.mxp3, meropodite
of the 3rd maxilliped; mp, mandibular palp; pl, cheliped; psmp, proximal segment of mandibular palp; scaph, scaphognathite
is a field of setae of two types (Fig. 5 B). One type are long slender type G
triserrulate which point towards and intermesh with the corresponding setae
of the opposite segment and serve to lock the two coxopodites together.
The other type are very long type C3 plumodenticulate which carve orally
and continue past the coxopodites of the two maxillae and past the mandible
to pass into the mouth (see above and Fig. 8). Along the posterior edge
of the upper (truncated) surface, the coxopodites bear fields of upward
pointing type E triserrate setae which lie underneath the basipodites of the
1st maxillipeds and intermesh with their proximal medial edge setae
(Fig. 5 A). On the anterior edges of the coxopodites there is another field
of type E triserrate setae (Fig. 12C) which point anteriorly and curve medially (Fig. 5 A). These setae intermesh with similar setae from the middle
region of the 8th sternite and with triserrulate and plumodenticulate setae
from the medial edges of the coxopodites of the 2nd and 3rd maxillipeds
to form the floor of the anterior buccal space (Fig. 8).
In addition to the setae already described, most of the buccal appendages
possess two further groups of setae, one situated on the outer face and
pointing anteriorly and the other on the inner face and pointing posteriorly
(Figs. 3-7). The anteriorly pointing setae on the outer face of one appendage
Functional Morphologyof the Mouthparts of a HermitCrab
29
intermesh with the posteriorly pointing setae on the inner face of the adjacent appendage to form a lateral screen between the two appendages which
prevents material from falling out laterally from the buccal spaces (Fig. 9).
Thus, type C1 plumodenticulate setae on the outer face of the basipodite
of the 1st maxilla intermesh with type F1 serrulate setae on the inner face
of the 2nd maxilla; setae intermediate between types G and E on the outer
face of the basipodite of the 2nd maxilla intermesh with type F1 serrulate
setae on the inner face of the basipodite of the 1st maxilliped and type G
triserrulate setae on the outer face of the basipodite of the 1st maxilliped
intermesh with type E triserrate setae on the meropodite of the 2nd maxilliped (Fig. 9). Similarly, type F1 serrulate setae on the outer face of the
coxopodite of the 1st maxilla intermesh with type C1 plumodenticulate setae
on the inner face of the 2nd maxilla and type C2 plumodenticulate setae
on the outer face of the coxopodite of the 2nd maxilla intermesh with
type F1 serrulate setae on the inner face of the coxopodite of the 1st maxilliped.
When the endopodites of the 2nd and 3rd maxillipeds are folded underneath the other mouthparts, type G triserrulate setae on the medial edges
of the meropodite and triserrulate, triserrate and plumodenticulate setae
from the medial edges of the basi-ischiopodite of the 2nd maxilliped intermesh with backward pointing triserrulate, triserrate and plumodenticulate
setae on the medial edges of the meropodite and basi-ischiopodite of the
3rd maxilliped to form a lateral screen between these two appendages
(Fig. 9). This screen is also the lateral wall of the anterior buccal space.
IV. Grooming
The main grooming appendages are the 3rd maxillipeds although most of
the other mouthparts have a self-grooming function. The majority of the
mouthpart setae, particularly those making up the various screens, are covered with setules which often have serrated edges. Particles adhering to
the setae are detached by the setules as the setae slide over each other
during the normal movements of the mouthparts. Because of the orientation
of the setules about the shaft, these detached particles can only move towards the tip of the seta and are progressively carried distally until they
are either ingested or rejected.
The 3rd maxillipeds are responsible for cleaning the eyes, antennae,
antennules, chelipeds, walking legs and anterior part of the carapace. In
the case of the eyes, antennules and antennae, the base of the appendage
is grasped from either side by the dactyls and propodites of the 3rd maxillipeds which are then drawn distally towards the tip of the appendage which
at the same time is pulled in the opposite direction. The aesthatasc setae
of the antennule are cleaned by special type D2 and D3 serrate setae situated
medially on the distal portion of the carpopodites of the 3rd maxillipeds
(Fig. 7 B). The two carpopodites are brought together one on either side
of the antennular flagellum and the aesthatasc setae are then drawn through
these fields of cleaning setae. The inner face of the carpopodites of the
30
P.J. Schembri
fl
I
bstr
end.mxpl
exo.mxp2
lmm
mer.mxp3
bas,mxp3
is.mxp3
exo.mxp3
cox.mxp3
Fig. 10. Lateral view of the buccal region of Pagurus rubricatus showing the relative arrangement of the endopodite of the 1st maxilliped and the exopodites of the 2nd and 3rd maxillipeds
of the right side and the paths traced by their flagella. For clarity the flagellar setae are
not shown, bas.mxp3, basipodite of the 3rd maxilliped; bstr, branchiostegite; cox.mxp3, coxopodite of the 3rd maxilliped; end.mxpl, endopodite of the 1st maxilliped; exo.mxp2, exopodite
of the 2nd maxilliped; exo.mxp3, exopodite of the 3rd maxilliped;f/, flagella; is.mxp3, ischiopodite of the 3rd rnaxilliped; ll, latching setae of the exopodite of the 3rd maxilliped; 12, latching
setae of the exopodite of the 2nd maxilliped; mer.mxp3, meropodite of the 3rd maxilliped
3rd maxillipeds has an additional type of cleaning setae (A* setae; Fig. 7 B).
These resemble type A plumose setae except that they bear short, serrated
setules instead of long filamentous ones (Fig. 12 D).
The pincer of the chelipeds is held vertically between the 2nd and 3rd
maxillipeds. Using the setae on the medial edges of the fingers, these then
brush the pincer - the left pair of appendages brushing one surface while
the right pair brush the opposite surface. The two 2nd maxillipeds work
the distal half of the pincer starting from the base of the dactyl and brushing
towards the tip while the two 3rd maxillipeds work the proximal half. The
remainder of the chelipeds, the walking legs and the anterior part of the
carapace are brushed by the setae of the inner faces of the 3rd maxillipeds.
The 2nd and 3rd maxillipeds clean themselves by rubbing against the opposite appendage.
V. Rejection Currents
Particles are discarded via the strong exhalant current from the branchial
chambers. This current is generated by the beating of the scaphognathites
of the 2nd maxillae in a manner similar to that described for other decapods.
As in other decapods, the edges of the scaphognathite are lined with type A
plumose setae (Fig. 4) which serve both to extend its surface area and act
as a gasket.
The posterior wall of the exhalant channel is formed by the body wall
while posterolaterally it is formed by the branchiostegite (Fig. 9). The exopo-
Functional Morphology of the Mouthparts of a Hermit Crab
31
A
Fig. 11. Anterolateral view of Pagurus
rubricatus showing water currents generated by
beating of the exopodites of the right 2nd and
3rd maxillipeds. For clarity the right cheliped
has been cut (shaded). A, anterolateral current
from left side of body; B, lateral and C,
ventrolateral currents from right side of body;
D, current from surface of substratum; E,
medial current. The exhalant current emerges at
right angles to the plane of the paper at the
point marked X. Note position of the
antennules
dite of the 1st maxilliped slots against the medial edge of the endopodite
of the same appendage such that these two segments form a single structure
(Fig. 5A). Along its lateral edge the endopodite carries type A plumose
setae which intermesh with other setae lining the internal surface of the
branchiostegite (Fig. 9). Setae lining the medial edge of the endopodite intermesh with backward pointing setae from the inner face of the meropodite
of the 2nd maxilliped. Type A plumose setae lining the medial edge of
the exopodite of the 1st maxilliped intermesh with type C1 plumodenticulate
setae lining the endopodite of the 2nd maxilla (Fig. 9). These plumodenticulate setae also bridge the gap between the endopodite and the lateral edge
of the basipodite of the 2nd maxilla. The endopodite of the 1st maxilla
slots against that of the 2nd maxilla and against the bodywall. Thus the
exopodite and endopodite of the 1st maxilliped and the endopodites of
the 1st and 2nd maxillae lock together by means of setae and bevelled
surfaces to form the anterior and anterolateral walls of the exhalant channel
(Fig. 9). This channel serves to funnel water upwards and anterolaterally
away from the crab (Fig. 11).
The flagella of the exopodites of the 2nd and 3rd maxillipeds generate
currents which waft water from the substratum surface immediately in front
of the crab up between the chelipeds and endopodites of the 3rd maxillipeds
and into the exhalant stream. Water is also drawn into the exhalant stream
from the sides of the crab (Fig. 11). Normally, either the left or the right
exopodites beat at any one time. The antennule on the same side as the
beating exopodites dips down and samples the water current coming up
from the substratum surface while the other antennule is held erect and
samples the water coming in obliquely from the side (Fig. 11).
The exopodites of the 2nd and 3rd maxillipeds lie adjacent to each
other and are arranged parallel to the long axis of the body (Figs. 9 and
10). The exopodite of the 3rd maxilliped carries two rows of type D1 serrate
setae (Fig. 7 A) which wrap round the exopodite of the 2nd maxilliped and
latch on to appropriately arranged fields of serrulate and serrate setae on
this appendage (Fig. 10). In turn, type F1 serrulate setae from the exopodite
32
P.J. Schembri
of the 2nd maxilliped (Fig. 6 A) grip the edge of the exopodite of the 3rd
maxilliped (Fig. 10). The two exopodites are thus locked firmly together
and function as one unit, the flagella of the two exopodites beating together
in a frontal plane and describing a small arc (Fig. 10). Type F1 serrulate
setae on the medial edge of the exopodite of the 3rd maxilliped intermesh
with fields of type C3 plumodenticulate setae on the lateral edges of the
meropodite of the 3rd maxilliped to form a screen between the exopodite
and endopodite of this appendage (Fig. 7 A).
The long axis of the endopodite of the 1st maxilliped is inclined at
a small angle relative to the long axes of the exopodites of the 2nd and
3rd maxillipeds, and, being shorter, its flagellum lies below the flagella of
the two exopodites (Fig. 10). The flagellum of the 1st maxilliped beats in
synchrony with the flagella of the 2nd and 3rd maxillipeds but is arranged
such that it generates a current which wafts particles up from the dorsal
region of the mid-buccal space and into the currents generated by the exopodites of the 2nd and 3rd maxillipeds and, via these, into the exhalant stream.
At the lowest point of its stroke the flagellum of the 1st maxilliped comes
to lie across a tuft of long type C3 plumodenticulate setae carried distally
on the inner face of the meropodite of the 2nd maxilliped (Figs. 6 B and
12E). The exact function of these setae is not clear but they appear to
act as a buffer for the flagellum and may also serve to detach particles
trapped in its setae.
Along their edges the flagella of the maxillipeds bear type A plumose
setae (Figs. 5A, 6A, 7A). Each flagellum beats dorsoventrally (Fig. 10).
As the flagellum moves dorsally (upstroke), water resistance acts on the
plumose setae and causes them to spread. As the flagellum moves ventrally
(downstroke), the setae are folded. The upstroke is thus the power stroke
while the downstroke is the recovery stroke. A ventral projection at the
base of each plumose seta just above the point of articulation catches on
a ledge associated with each setal insertion when the setae are fully spread
and prevents them from folding during the upstroke (Fig. 12 F).
VI. Mouthpart Function During Feeding
1. Detritus Feeding. Working alternately the 3rd maxillipeds collect sediment
from the pereiopods using the setae of the dactyls and propodites (Fig. 1 A).
The fingers of the 3rd maxillipeds are then flexed medially such that the
Fig. 12. A Type H1 cuspidate setae of the medial edge of the basipodite of the 1st maxilla.
These setae form a sieve screen in front of the mouth. Outer face of the basipodite is at
right ( x 70). B Modified simple setae from the medial edge of the basipodite of the 2nd maxillae
(I* 'gravel-scrubbing' setae, Fig. 4). Note recurved and slightly flattened tips ( x 400). C Type E
triserrate setae from the outer face of the coxopodite of the 1st maxilliped (Fig. 5A) ( x 220).
D Modified plumose setae from the inner face of the carpopodite of the 3rd maxillipeds (A*
setae, Fig. 7B) ( x 140). E Long type C3 plumodenticulate setae from the internal face of
the meropodite of the 2nd maxilliped (Fig. 6 B). These setae act as a buffer for the flagellum
of the 1st maxilliped ( x 210). F The basal region of type A plumose setae from the flagellum
of the 2nd maxilliped. Note the projection at the base of each shaft (arrows) and the groove
associated with each setal insertion ( x 500)
i~ii ~ ~ i ~
~ i! i~i~ ~
34
P.J. Schembri
distal segments come to lie underneath the other mouthparts (Fig. 1 B).
Also working alternately the dactyls of the 2nd maxillipeds rake off particles
from the setae of the fingers of the 3rd maxillipeds and push them through
the setal screen formed by the basipodites of the 1st maxillipeds and into
the mid-buccal space. Here the vigorous mediolateral beats of the basipodites of the 2nd maxillae tease off particles from the dactyl setae of the
2nd maxilliped. The basipodites of the 1st maxillipeds also perform a small
mediolateral movement which helps to dislodge particles adhering to the
distal segments of the 2nd maxillipeds and to push them posteriorly into
the mid-buccal space. Propelled by the 2nd maxillae fine particles are pushed
backwards through the filter screen formed by the medial edge setae of
the basipodites of the 1st maxillae; larger inorganic particles are pushed
upwards towards the distal tips of the maxillae where they are carried away
by the rejection currents. Throughout this process the basipodites of the
1st maxillae remains static or at most perform a very low amplitude mediolateral vibration. The mandibles, mandibular palps and the labrum similarly
remain static. If however live foraminifera were present, these were passed
into the posterior buccal space where they were cracked open by the molar
processes of the mandibles. The mandibular palps then pushed out the
resulting fragments into the mid-buccal space where they were treated as
other detrital particles.
2. Gravel-scrubbing. Granules of suitable size are grasped by the endopodites
of the 2nd and 3rd maxillipeds which hold them applied against the inner
mouthparts (Fig. 1 C). The basipodites of the 1st maxillipeds and of the
2nd maxillae perform energetic mediolateral movements, those of the 2nd
maxillae being especially vigorous, and scour off detritus from the surface
of the granule using the medial edge setae. Dislodged particles are pushed
posteriorly into the mouth by smaller mediolateral movements of the basipodites of the 1st maxillae. During this process the endopodites of the 2nd
and 3rd maxillipeds manipulate the granule in such a way as to cause it
to rotate such that its surface is brushed all over (Fig. 1 C). When thoroughly
brushed, the granule is discarded and the process is repeated with a fresh
granule.
3. Macrophagous Feeding. Soft material is held between the 3rd maxillipeds
which press it against the inner mouthparts. The fingers of the 2nd maxillipeds work in alternation to push food backwards towards the mouth using
the setae on the dactyl tip. The basipodites of the 1st maxillipeds and both
pairs of maxillae are spread laterally allowing free access to the mouth.
At the same time all three sets of appendages perform rapid mediolateral
movements which cause the food to be abraded through the action of the
setae on their medial edges. Periodically pieces of food are sliced off by
the mandibles. During biting the inner mouthparts stop beating and the
1st maxillipeds and 2nd maxillae are spread laterally; the mandibles open
and the 2nd maxillipeds push the food into the posterior buccal space. Posteriorly to the mandibles the food is grasped by the mandibular palps and
Functional Morphologyof the Mouthparts of a Hermit Crab
35
the labrum. Anteriorly the food is grasped by the basipodites of the 1st
maxillae, by the dactyls of the 2nd maxillipeds and by the crista dentata
of the 3rd maxillipeds. As the mandibles slice through the food, the 2nd
and 3rd maxillipeds and the 1st maxillae pull it outwards. The severed
piece is then pushed posteriorly into the mouth by the mandibular palps
and the labrum.
D. Discussion
Pagurus rubricatus lives on gravelly sediments rich in skeletal material (Probert et al. 1979). Such a heterogeneous substratum offers a variety of food
sources which this hermit crab is well adapted to exploit. Animal food
is clearly the most energy rich of the various foods available and predation
on small invertebrates if probably the most profitable mode of feeding in
that it supplies the maximum gain for effort invested. While searching for
prey however, P. rubricatus feeds on detritus obtained either directly from
the sediment or by scrubbing gravel granules. In this way it further maximizes the return obtained, in terms of energy, for the effort expended in
foraging.
With few exceptions hermit crabs have been found to be able to feed
in a number of different ways and on diverse food sources (see Kunze
and Anderson (1979) for a summary review). As in P. rubricatus this may
be an adaptation to maximize the net rate of energy uptake by exploiting
whatever food happens to be available as the hermit crab ranges over the
substratum searching for its preferred food. It is likely that the success
of hermit crabs as a group is related to their opportunistic feeding habits.
Those species with a limited feeding repertoire are invariably those which
do not encounter a wide spectrum of food types because of the specialized
habitats they live in. Such species include Paguritta harmsi which lives in
attached polychaete tubes (Schuhmacher 1977) or in pits in living coral
colonies (Patton and Robertson 1980); Discorsopagurus schmitti, which lives
in attached polychaete tubes (Caine 1980); Calcinus verrilli which lives in
the attached shells of vermetid gastropods (Markham 1977) and Isocheles
wurdemanni which lives in high wave energy environments (Caine 1978).
All four species feed mainly by filtering particles from the water. Even
these show some flexibility, however, since the last three mentioned also
feed on detritus (Caine 1978; 1980; Markham 1977).
In detrivorous and macrophagous hermit crabs food is collected mainly
by the pereiopods, especially the chelipeds, and sometimes by the 3rd maxillipeds. There is a great variety of form of the chelipeds in different species
of hermit crabs and in some cases this has been related to feeding behaviour
(e.g. Caine 1975). In P. rubricatus the minor chela with its expanded and
flattened outer edge is adapted for digging shallow pits in the substratum
while the concave ventral surface makes an efficient scoop for collecting
sediment (Fig. 1). The strong major chela with its numerous rows of molariform teeth is well adapted for cracking molluscan shells open.
The 3rd maxillipeds also differ in structure from species to species,
36
P.J. Schembri
mainly in the relative development of the crista dentata. This has been
correlated with the degree of involvement of this structure in trituration
of the food in different species; predominantly macrophagous or predatory
forms having larger and more numerous teeth than do detrivorous or filterfeeding species (Caine 1975; Kunze and Anderson 1979). The other mouthparts are very similar in gross morphology in the different species of hermit
crabs, however they differ markedly in both the type and density of setation.
The setation of the mouthparts of P. rubricatus is more complex than
that described for any other hermit crab. This is not surprising considering
the number of feeding techniques used by this species. The same set of
appendages have to function in different ways depending on what type
of food is being processed. For example the medial edge setae of the basipodites of the 1st maxillipeds form a screen separating the anterior and the
mid-buccal spaces during detritus-feeding but function in abrading the food
during macrophagous feeding and help in scouring detritus from gravel
granules during 'gravel-scrubbing'. This multiplicity of functions is probably the reason for the fields of mixed setae found on many of the buccal
appendages. The picture is further complicated by the fact that some of
the mouthparts are used as cleaning organs and feeding and cleaning setae
may occur in close proximity to each other, e.g. on the fingers of the 3rd
maxillipeds (Fig. 7). Setal structure may, however, be correlated with function.
Setae which function in manipulating food, in gripping the food during
cutting and in abrading soft material during macrophagous feeding are
predominantly cuspidate, triserrate, triserrulate and plumodenticulate types.
The cuspidate setae probably function like the prongs of a fork while the
finely serrated setules of the other setal types prevent slippage when grasping
the food and make efficient abrading structures. Setae whose function is
to groom other appendages are mainly serrate types, the strong denticulations on these acting like the teeth of a comb. A variety of setae participate
in forming screens. These are mainly setulated varieties. Screens function
in retaining material in the buccal region by filling the gaps between appendages, and by forming the floor and walls of the various buccal spaces.
Setal screens are also important in suspension-feeding (e.g. the screen formed
by the setae of the endopodites of the 2nd and 3rd maxillipeds and associated
structures) and in particle selection (e.g. the filter screen formed by the
medial setae of the basipodites of the 1st maxillae). Finally, setal screens
function in channelling the exhalant current, carrying rejected material away
from the crab. Serrulate, serrate and plumodenticulate setae, particularly
those forming a part of screens also have a self-cleaning function. Plumose
setae extend surfaces and form gaskets while a number of setal types (serrate,
serrulate, plumodenticulate) serve to lock appendages together. A few setae
carry out specialized functions. These include the cuspidate grating setae
of the basipodites of the 1st maxillae, the gravel-scrubbing simple setae
of the basipodites of the 2nd maxillae and the 'plumose' cleaning setae
of the inner face of the carpopodites of the 3rd maxillipeds (Fig. 7 B).
Kunze and Anderson (1979) have described the function of the mouth-
Functional Morphology of the Mouthparts of a Hermit Crab
37
parts during feeding in Clibanarius virescens and in three other hermit crabs.
This process was similar in all four species. In C. vireseens as in P. rubrieatus
material collected by the chelae is brushed posteriorly by the dactyls of
the endopodites of the 3rd maxillipeds; the 2nd maxillipeds then sweep
this material off the 3rd maxillipeds and transfer it to the inner mouthparts.
The function of the remaining mouthparts is different in the two species.
In C. virescens the setae of the basipodites of the 1st maxillipeds rake off
particles from the endopodites of the 2nd maxillipeds. The basipodites of
the 1st maxillipeds are in turn raked by the endites of the 2nd maxillae.
The 1st maxillae then transfer this material from the endites of the 2nd
maxillae to the mouth. This is completely unlike P. rubricatus where the
basipodites of the 1st maxillipeds form a screen separating the anterior
from the mid-buccal space while the basipodites of the 1st maxillae form
a filter grating in front of the mouth. The 2nd maxillae push particles
through this grating or reject them depending on size. While several authors
have implicated the maxillae as functioning in particle sorting (Roberts
1968; Greenwood 1972; Caine 1975; Kunze and Anderson 1979), the mechanism by which this is achieved has not been previously described. Given
the great similarity in structure of the maxillae in different hermit crabs,
it is likely that particle sorting in most species takes place in an analogous
manner to that described here for P. rubricatus.
Acknowledgements. I am very grateful to Associate Professor J.B. Jillett for providing the
necessary facilities and for his help and interest. Particular thanks are due to Drs. B.G. Williams
and C.L. McLay for critically reading the manuscript and for many useful discussions. I
thank also Mr. W.L. Tubman and Mr. C.S. Heseltine for collecting the crabs, Mr. G. Stokes
for the histological preparations, Mr. D.J. Sanderson for expert photographic assistance and
Mrs. F.M. Wood for typing the manuscript.
The work described in this paper was carried out during the tenure of a University of
Otago Postdoctoral Fellowship and was supported by two University of Otago Research Committee grants for which I am grateful.
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Received April 9, 1982