ZoologicalJoumal of the Linnean Society, 65: 1 1 1 - 1 18. With 4 figures
February 1979
On the taxonomy of Littorina africana
(Mohsca: Gastropoda)
ROGER N. HUGHES
Department $Zoology, University College of North Wales,
Bangor, Gwynedd, North Wales
Acceptedfor publication April I977
L. africana and L. knysnaensis are regarded as two morphs of a single species which exhibits a genetic
cline along the south-eastern coast of southern Africa. The dark brown morph knysnaensis dominates
the western, cooler end of the cline and is replaced by the pale blue rnorph africana at the warmer
end of the cline. These conclusions are based o n evidence from the latitudinal distributions, the
complete range of intermediate forms regarding shell colour and shell morphology and the lack of
differences in radular morphology, penial morphology or habitat.
K E Y WORDS:-Lillorina
- taxonoiny - clines - ecotypes - South
Africa.
CONTENTS
. . . . . . . . . . .
Introduction
Previous taxonomic status
. . . . . . .
Diagnostic features of L. africana and L. knysnaenris
.
Characters of individuals in the the present collection
. . . . . . . . . .
Shell colour
Shell sculpture
. . . . . . . . .
Shell shape
. . . . . . . . . .
Radula
. . . . . . . . . . .
Penis
. . . . . . . . . . . .
Mantle . . . . . . . . . . . .
Habitat
. . . . . . . . . . .
Discussion
. . . . . . . . . . . .
Proposed classification
. . . . . . . .
Acknowledgements
. . . . . . . . .
References
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Ill
112
112
113
113
I13
11.5
115
115
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11.5
117
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118
118
INTRODUCTION
Littorina africana (Philippi, 1847) and L. knysnaensis (Philippi, 1847) are
dominant organisms in the splash zone of southern Africa. L. knysnaensis extends
from South West Africa to southern Natal while L. africana extends from southern
Mosambique southwards through Natal becoming very infrequent beyond the
Transkei where it overlaps with L. knysnuensis (pers. obs.). A collection of these
forms from many localities between Lambert’s Bay and Cape Vidal (Fig. 1)
included individuals intermediate in colour and shell sculpture and this, together
0024-4082/79/020111-08/$02.00/0
5
111
0 1979 The Linnean Society of London
R. N. HUGHES
I12
with latitudinal changes in the frequency distributions along the south-east coast,
suggested that L . africana and L. knysnaensis belong to a single species exhibiting a
genetic cline. Comparisons of shell colour, shell sculpturing, shell shape, penial
structure and radular morphology are presented together with a proposal that L .
knysnaensis be regarded as a morph of L. africana. A representative series from the
collection is deposited at the British Museum (Natural History) (Acc. No. 2295).
PREVIOUS TAXONOMIC STATUS
All previous taxonomic works on L. africana and L . knysnaensis are reviewed by
Rosewater ( 1970) who places these snails in the subgenus Austrolittorina
Rosewater, 1970 which is characterized by species with a predominantly southern
ocean distribution, conicoturbinate shell, flattened columella and crescentshaped area on the adjacent part of the shell, penis (verge)with a single gland at
its base bearing an accessory flagellum. Philippi (1847) had described a third
form from Natal, L . decollata Philippi, 1847, also figured in Janus (19611, which
Rosewater (1970) regarded as synonymous with L . africana. The synonomy is
confirmed below.
DIAGNOSTIC FEATURES OF L . AFRICANA AND L. KNYSNAENSIS
The following characteristics are listed by Rosewater ( 1970)
L. africana
L. knysnaensis
External ground colour greyishwhite with a diffuse bluishgi-eyband encircling the body
whorl and on anterior portions
of the spire whorls
External colour mahogany brown
in a wide band above peripheral
keel, lighter near suture and o n
the base, with whitish spots and
streaks especially on the base
Aperture niediuin to dark brown
with a prominent white band
near junction of outer lip and
columella and another often
obscure band at junction
of outer lip and body whorl
Shell short-turbinate to
globose
Base somewhat flattened,
separated from upper part
of body whorl by a low,
rather indistinct peripheral
keel
Whorls 3-5 rounded
Aperture dark brown with a
white band near junction of
outer lip and columella
Spire usually much eroded,
considerably less than half the
shell length
Spire usually eroded, less
than half the shell length
Aperture widely oval
Aperture oval
Sculpture consisting of closely
spaced, raised spiral threads
of varying widths, wider threads
usually separated by 2-4 narrow
threads. Sometimes entirely smooth
( L . decollata)
Animal darkly pigmented on edge
of mantle
Sculpture consisting of about
9 spiral striae o n penultimate
whorl of spire persisting onto
body whorl with 15- 1 7 striae
above keel and 9-10 below
Shell turbinate
Base indistinctly flattened,
separated from upper part of
body whorl by a raised peripheral
keel
Whorls 3-5 somewhat flattened
Animal not darkly pigmented
o n edge of mantle
TAXONOMY OF LITTORINA AFRICANA
113
200
\
uakopmund
25"
30"
3 50
Figure 1 , Geographical distribution of L. afrzcana. The circles indicate the proportions of variety
knysnaensis (black) and afncana (white) in the natural populations. Many collecting sites between those
shown on this figure were visited.
CHARACTERS OF INDIVIDUALS IN THE PRESENT COLLECTION
Most individuals could be assigned unambiguously either to the form africanu,
including decolluta (shell numbers 1, 2, 4, 35, Fig. 2) or to the form knysnaensis
(shell numbers 1 1 , 12, 23-26, 44-47, Fig. 2) according to Rosewater's
( 1970) diagnostic characters. However, small numbers of shells with intermediate
colouring or sculpturing were found from the Transkei through Natal.
Shell colour
Certain specimens from Natal have dark brown dashes o r streaks
superimposed on the typical bluish-white africana background colour (shell
numbers 20-22, 29-31, 33-34, 36-39, 41-43, Fig. 2). Others from Port
S t . John's, Transkei showed the africana background colour densely
superimposed by pale brown flecks or spots (shell number 1 7 , Fig. 2). Often, the
bluish-white surface of the shell of africana is pitted or eroded away exposing the
dark grey subsurface (shell numbers 3, 19, Fig. 2). Throughout the range of
knysnaensis are localized populations with a predominance of individuals bearing
pale blue upper margins to the whorls (shell numbers 5-9, 18, Fig. 2). A
specimen of knysnaensis from Liideritz (shell number 16, Fig. 2) has a uniformly
dark background colour superimposed with cream dashes, making it vaguely
similar to L. punctata (Gmelin, 179 1 ) .
Shell sculpture
Many intermediate forms from those with smooth shells and obliterated spires
(decollata, shell numbers 1 , 35, Fig. 2) to those with prominently sculptured shells
and intact spires (africana, shell numbers 4, 40, Fig. 2) were found, suggesting that
L. decollata is synonymous with L. africana. Occasional knysnaensis lack the
pronounced keel on the body whorl (shell numbers 28, 32, Fig. 2) while
occasional africana do have a pronounced keel (shell number 27, Fig. 2).
Figure 2. Varieties of colour and shell morphology in L. afrricana. 1-35. Shells selected to show the
graded series from variety ufncana to variety knysnaensis. 36-47. Small speckled morphs from crevice
haabixat in N a d and j u v d e knymaewir frm the Atlantic coast (bottom row). The shells were
collected from the following localities: 1-12, Amiston; 13-16, Luderitz; 1 7 , Port St. John’s; 18-26,
Uinn&azana estuary; 27, Amanzimtoti: 28, Struis Bay; 29-32, Port Edward; 33, Richard’s Bay; 33,
Port Edward; 35, Utnngazana open coast; 36-39, Umhlanga Rocks; 40, Amiston; 41-43, Cape
Vidal; 44-47, Lambert’s Bay.
TAXONOMY O F LITTORINA AFRICANA
115
Shell shape
Both africana and knysnaensis range from a turbinate to an apparently globose
shell form. Short-turbinate to globose shells are more frequent in africana but
this appearance is due to severe erosion of the spire (shell numbers 1, 35, cf. 4,
Fig. 2). Unusually elongated knysnaensis (shell number 1 6 , Fig. 2) were found at
Arniston and probably represent a pathological condition. Certain specimens of
knysnaensis from Luderitz are much larger than any seen elsewhere and have a
very indistinct colour patterning (shell numbers 13, 14, Fig. 2).
Radula
The radula is well known to b e , a poor taxonomic character among the
Littorinidae. Even among different genera the radulae are remarkably similar. I t
is not surprising, therefore, that no differences were found between the radulae
of africana and knysnaensis (Fig. 3). Both forms have the usual littorinid formula
2.1.1.1.2.
Penis
The penis (verge) of africana and knysnaensis is furnished with a single penial
gland at the base, consistent with their inclusion in the subgenus Austrolittorina.
N o reliable differences in penial shape could be detected in the two forms. The
penis of knysnaensis tended to be unpigmented, relatively short with a concave
edge to the glandular side while that of africana was always pigmented except for
the border and tended to be proportionally longer with a convex edge to the
glandular side (Fig. 4). These trends were reversed in a few individuals.
Mantle
The association of a pigmented mantle edge with africana, noticed by
Rosewater (19701,is confirmed here.
Habitat
Both africana and knysnaensis are splash zone species which overlap completely
in tidal height. All shores on which they were found experienced moderate to
heavy wave action. The latitudinal distributions of knysnaensis and africana are
strikingly different (Fig. 1). The form knysnaensis occurs along the atlantic coast
from Swakopmund and Luderitz in South West Africa (University of Cape Town,
Zoology Museum collection) to the Cape of Good Hope, continuing as the
dominant form along the southern coast of the Cape Province. The form africana
of the type decollata occurs sporadically in frequencies below 0.0 1% from False
Bay to Gonubie Mouth (Fig. 1). Arniston, between Agulhas and Mossel Bay (Fig.
1 ) is the most westerly point where afrricana reached frequencies greater than 0.1%.
Local patches of rock at Arniston supported populations with from 1 to 10%
africana. Similar frequencies of africana were also found at Brenton and Kentonon-Sea. At all these sites the rock is a light buff sandstone forming low
overhanging cliffs due to severe erosion of the intertidal face. At intervening sites
R. N . HUGHES
1 Ib
R
I
I
2
3
2
!I
3
3
2
,
0.Irnrn
,
W
2
3
.Figure 3. Radular teeth of L. ufricana, camera lucida drawings. A. Upper row is variety africuna; lower
row is variety knysnaensis. B. Tooth rows drawn in ritu: upper row is variety knysnaensis; lower row is
variety ufncana. R, Rachidian; 1, lateral; 2, inner marginal; 3, outer marginal.
e.g. Mossel Bay, Jeffrey's Bay, Kidd's Beach, Port Alfred, the rocks are dark and
hard, supporting less than 0.1% afrricana. At Port St. John's and Umngazana in the
Transkei ufricana reached proportions around 50% on all types of rock. The
proportions of africana rose to over 90% in southern Natal (Port Edward) and
finally to 100% in northern Natal (Amanzimtoti). Southport, north of Port
Edward, was the most northerly site where knysnaensis was recorded (less than
0.1%).Certain populations of ufricana from the Transkei through Natal contained
low frequencies of individuals with brown markings.
TAXONOMY O F LITTORINA AFRICANA
A
C
B
117
D
E
D
J
G
H
I
Imm
I
,
Figure 4 . Penial structure of L. afrcrana, camera lucida drawings. Upper row is variety afrricana. Lower
row is variety knysnaensis. A, Arniston, operculum diameter (o.d.1 3.2 mm; B, Richard’s Bay, o.d. 4
mm; C, Umngazana, o.d. 3.2 mm; D, Amanzimtoti, 0.d. 3.4 mm; E, Port Edward, 0.d. 3.6 mm; F,
Arniston, o.d. 4 m m ;G, Knysna Head, 0.d. 3.1 mm; H, Lambert’s Bay, 0.d. 4 mm; I, Lambert’s Bay
o.d. 4.3 m m ; J. Agulhas, o.d. 4.4 mm.
DISCUSSION
The latitudinal distributions of africana and knysnaensis, the complete range of
intermediate forms in shell colour and morphology, and the absence of
differences in radulae, penial morphology or habitat suggest that these forms
represent a dimorphic species showing a genetic cline correlated with latitude
(Fig. 1). I t is unlikely that afiicana and knysnaensis are two species which
occasionally hybridize in the zone of overlap because africana persists in very low
frequencies all along the south coast to the Cape of Good Hope (further
observations might find africana on the Atlantic coast). Moreover, the proportion
of africana increases dramatically on certain types of light coloured rocks at
widely separated localities along the south coast. The form afiicana is regarded as
a pale blue morph dominant at the warmer end of the cline giving way to the
dark brown knysnaensis at the cooler end of the cline. Intermediate colour morphs
are found over the entire geographical range, especially in the transition zone
from the Transkei to Natal, but are always scarce relative to the abundances of
true knysnaensis or africana. The cline hypothesis is corroborated by a similar
colour dimorphism correlated with temperature in L. neritoides (L.) (Hughes,
unpublished data). It is not clear why the pale blue morph does not reappear at
lower latitudes on the Atlantic coast, but this may be correlated with the lower
sea and air temperatures caused by the Benguela current. Details of the
background colour and superimposed patterns suggest that several genes are
R. N . HUGHES
118
involved in the dimorphism. Linkage o r pleiotropic effects are suggested by the
strong association of a pigmented mantle edge and penis and the lack of a sharp
keel on the body whorl with a pale blue background colour and with a lack of
superimposed patterns (africana).
Several other forms o r ecotypes may exist. The normal form of africana seems
distinct from decollata while small, crevice-dwelling individuals with brown flecks
(shell numbers 36-39, Fig. 2 ) collected in Natal are probably a distinct ecotype
analogous to the European L . saxatilis neglecta (Bean). Thes.e small snails closely
resemble the Australian species L . acutispira Smith, 1892, both in appearance and
habit (McFadyen, 1978). Within knysnaensis there is a series from the typical dark
individuals to those with pale blue upper margins to the whorls (shell numbers
5-9, 18, Fig. 2 ) . The latter type is abundant at many localities along the south
coast, e.g. Knysna, and has been collected at Luderitz (U.C.T. Zoology Museum).
I t s distribution may also be correlated with temperature. The population of
africana at Port St. John's contained many large individuals with a dense covering
of' light brown spots (shell number 1 7 , Fig. 2) so that they bear a superficial
resemblance to L . pintado (Wood, 1828). The latter species was not recorded in
the present survey and previous records from South Africa (Rosewater, 1970)
niay originate from confusion with morphs of africana.
PROPOSED CLASSIFICATION
Family
. Genus
Subgenus
Species
Variety
Variety
Littorinidae
Littorina
Austrolittorina
africana
knysnaensis
africana
Gray, 1840
Ferrusac, 1822
Rosewater, 1970
(Philippi, 1847)
ACKNOWLEDGEMENTS
I wish to thank John Field for organizing my visit to South Africa and for the
loan of his car which worked hard in the cause of littorinology.
REFERENCES
JANUS, H., 1961. Die Typen und Typoide sudafrikanischer Meeresmollusken im Staatlichen Museum fur
Naturkunde in Stuttgart. I. Gastropoda. Stuttgarter Beitriige zur Naturkunde, 70: 1-19.
ROSEWATER, J., 1970. The family Littorinidae in the Indo-Pacific. Part 1. The sub-family Littorininae. In R.
Tucker Abbott (Ed.),Indo-Paclfic Mollusca, 2:4 17-506.
McFADYEN, K.E., 1978. Ecology ofPopulations ofthe Intertidal Snail Littorina acutispira Smith. Unpublished M.Sc.
thesis, University of Sydney.