~oologicalJournal of the Linnean Sociely (1993), 107: 93-106. With 6 figures
Changes in the composition of the auditory
bulla in southern Solomon Islands populations
of the grey cuscus, Phalanger orientalis
breviceps (Marsupialia, Phalangeridae)
CHRISTOPHER A. NORRIS
University Museum €9 Department of <oology, Parks Rd, Oxford OX1 3P W
Receiued Nosember 1991, accepted for publication February 1992
The auditory bulla is a much-scrutinized taxonomic charactrr of mammals, which is generally
regarded as showing a high degree of structural consistency within higher taxa. Observations of
bulla variability in populations of the marsupial Phalanger ortenlalis from the Solomon Islands
demonstrdtr ronsiderablr flexibility in bulla makeup, with variable incorporation of the squamosal
into the tympanic floor. Studies of the ontogeny of the bulla in Phalanger show the presence of three
ossiliration centres, including an entotympanic. Squamosal invasion of one of these ossificiation
centres is seen as a possible result of inbreeding, arising from the mode of colonization of the
Solomon Islands by this species. This suggests that, under certain conditions, considerable
morphological plasticity may be induced within the selective constraints of bulla function.
ADDITIONAL KEY WORDS:- Geographical variability
CONTENTS
Introduction . . . . . . . . . . . .
Materials and methods
. . . . . . . . .
Results . . . . . . . . . . . . .
Bulla ossification in Phalanger orienlalis orientalis . . .
Squamosal bulla variants: description and distribution .
Discussion
. . . . . . . . . . . .
The formation of squamosal bullae
. . . . .
The entotympanic
. . . . . . . . .
The significance of bulla variability in Phalanger orientalis
Conclusions . . . . . . . . . . . .
Acknowledgements . . . . . . . . . .
References
. . . . . . . . . . . .
Key to abbreviations used in figures . . . . . .
Appendix . . . . . . . . . . . . .
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93
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INTRODUCTION
The auditory bulla is the ventral wall (or floor) of the mammalian tympanic
cavity. Van der Klaauw (1931) described the bulla as a bony or cartilaginous
;tructure, although more recent studies (Novacek, 1977; MacPhee, 1981) have
tended towards a view of the bulla as a membranous structure, which may
undergo varying degrees of ossification. Placental mammals show considerable
0024-4082/93/020093
+ 14 SOS.OO/O
93
0 1993 The Linnean Society of London
94
C. A. NORRIS
Figure 1. Diagrammatic representation of the basic types of tympanic regions in extant therian
mammals. All figures show a posterior view of the right hand bulla. A, Ossified entotympanic bulla
(Scandentia, most Chiroptera, most Edentata, Pholidota, .plesiomorphic Carnivora, most
Pinnipedia, Hyracoidae); B, ectotympanic bulla (Dermoptera, Lagomorpha, Rodentia, Cetacea,
derived Carnivora, odobenid Pinnipedia, Proboscidea, Perissodactyla, Artiodactyla); C, petrosal
bulla (primates); D, basisphenoid (most Lipotyphla) or alisphenoid (Marsupialia) bulla; E,
cartilaginous bulla (dashed lines) (three genera of megachiropteran bats, one edentate and one
viverrid genus); F, composite bulla (Macroscelida); G, bulla absent (Sirenia, Tubulidentata).
(Reproduced, with permission, from Novacek, 1977).
variability in the composition of the auditory bulla (Winge, 1895; Van Kampen,
1905; Bondy, 1907), with a number of elements of the basicranium becoming
incorporated in the tympanic floor. These elements fall into two categories:
outgrowths of the constant bones of the basicranium, known as tympanic
processes, and a class of independent ossifications, of questionable taxonomic
significance, traditionally referred to as entotympanics. In spite of this variability
in bulla composition, there is a high degree of structural consistency within
major higher taxa (Fig. l ) , as a result of which the bulla has been frequently
employed as a character in studies of mammalian systematics and evolution.
In contrast to the placentals, marsupials, with the exception of the
Vombatomorphia (Aplin & Archer, 1987), are generally considered to possess
only a single type of bulla. This is formed from the alisphenoid, occasionally
supplemented by the ectotympanic and the petrosal. I n didelphine marsupials
the ossified bulla is small, formed from a poorly developed alisphenoid tympanic
wing (Fig. 2A), with the remainder of the bulla predominantly membranous. I n
many other groups of marsupials, however, the bulla is a more substantial
structure, and in the Phalangeridae it forms a flattened bony lamella (Fig. 2B),
which may show some inflation.
-
AUDITORY BULLAE IN CUSCUSES
95
A
Figure 2. Basicranial regions of marsupials. A, Didelphis virginiana, left-hand side; B, Phalange,
orientalis, right-hand side; C , Vombatus ursinus, right-hand side.
Until recently, little variation in the composition of this structure had been
observed in marsupials. However, in 1989, Flannery (personal communication)
discovered specimens of the grey cuscus (Phalanger orientalis) from the southern
Solomon Islands which possessed auditory bullae formed from the squamosal.
MATERIALS A N D METHODS
Fifty specimens of the Solomon Islands’ subspecies of the grey cuscus
P. orientalis breviceps were examined for structural anomalies of the auditory
region. This material was drawn from the collections of the Natural History
Museum, London, and the Australian Museum, Sydney, and is listed in the
96
C. A. NORRIS
4 NIaaan Atoll
Figure 3. The Solomon Islands. Inset shows total range of Phalanger orientalis (in black): the broken
line encloses the total range of phalanger (smsu Tate, 1945).
Appendix. Additionally, in order to understand the formation of the bulla in
P. orientalis, it was necessary to construct a growth series for this species.
Insufficient numbers of juvenile specimens of P. orientalis breviceps were available
in the sample, and thus another subspecies was used. I n order to minimize the
potential effects of geographical variability, individuals from a large collection
from a limited geographical area were used, in this case a series of the nominate
subspecies P. orientalis orientalis from the islands of Ambon, Buru and Ceram in
eastern Indonesia. Specimens were arranged in order of successive tooth
eruption.
The terminology used follows Archer (1976) with additions from MacPhee
(1981). Specimen numbers prefixed by 'BMNH' are from the collections of the
Natural History Museum, whilst those prefixed 'My are from the Australian
Museum.
The 'Solomon Islands' is here taken to be the geographic entity, containing
both the Solomon Islands themselves, and the North Solomons Province of
Papua New Guinea (Fig. 3).
RESULTS
Bulla ossijication in Phalanger orientalis orientalis
Bulla ossification occurs at a comparatively late stage in the ontogeny of
P. orientalis: in the earliest growth phases observed, when M3 had just erupted,
AUDITORY BULLAE IN CUSCUSES
A -
B
97
0
C
D
5mm
u
Figure 4. Basicrania showing stages of bulla ossification in Phafanger orientalis orienlafis. A, BMNH
20.7.26.32 (M’ fully erupted): 1, antero-mesial centre of ossification; 2, antero-lateral centre of
ossification. B, BMNH 32.7.20.5 ( M 3 partially erupted). C , BMNH 10.3.4.62 [Right bulla] (MI
partially erupted). D, BMNH 11.7.12.51 (M4 fully erupted), bulla fully ossified.
the bulla was still predominantly membranous. Three incipient areas of
ossification could be observed at this stage: in the antero-mesial corner, lateral
to the foramen ovale; in the antero-lateral corner, mesial to the glenoid fossa and
postglenoid process; and a t the caudal edge of the bulla, antero-lateral to the
posterior lacerate foramen (Fig. 4). T h e former two areas were periosteal
continuations of the alisphenoid. The latter area was not associated with any of
the surrounding bones of the basicranium, and appeared to be an independent
ossification within the bulla membrane, thus falling within Van der Klauw’s
(1931) definition of an entotympanic. These areas appeared to be more or less
fixed with respect to the bulla, and could be seen as ‘centres’ of ossification for
the bulla. Subsequent ossification of the bulla proceeds with caudal and mesial
growth of the antero-lateral alisphenoid process. There is lateral growth of the
antero-mesial alisphenoid process, and some expansion of the entotympanic. The
process of ossification is comparatively rapid, and by the time of partial
appearance of M4 i t is no longer possible to distinguish the separate elements on
the tympanic floor (Fig. 4A-D).
98
C. A. NORRIS
A
0
lOmm
Figure 5. The basicranium of BMNH 1939.3136: a specimen of Phalanger orientalis breuiceps from
Cuadalcanal, Solomon Islands, showing asymmetric incorporation of the squamosal into the right
auditory bulla A, Photo; B, ink drawing with captions.
AUDITORY BULLAE IN CUSCUSES
A.
99
B.
0
5 m
Figure 6. Specimens of Phalunger orientalis breviceps showing varying degrees of incorporation of the
squamosal into the bulla. A, BMNH 35.9.2.3. (left bulla only): displacement ofsquamosal from strut
defining ventral edge of foramen ovale to medial position on roof of trigeminal canal. B, M8672
(right bulla only): restriction of squamosal contribution to an antero-lateral inclusion.
Squamosal bulla variants: description and distribution
A range of squamosal bulla variants were observed in specimens of P. orientalis
breviceps, differing primarily in the respective contributions of squamosal and
alisphenoid to the tympanic floor. In the most commonly encountered condition,
the squamosal/alisphenoid suture was displaced mesially along the margin of the
glenoid fossa to contact the lateral margin of the eustachian foramen, in the
region of the bony ‘strut’ forming the ventral margin of the foramen ovale
(Fig. 5). Both alisphenoid and squamosal contributed to this strut, but the
alisphenoid contribution to the bulla was restricted to a small inclusion along the
lateral margin of the foramen ovale. Less frequently, the alisphenoid was
displaced from the strut, with the suture between alisphenoid and squamosal
bisecting the roof of the trigeminal canal (Fig. 6A). Other conditions observed
involved smaller squamosal contributions to the bulla: in BMNH 34.9.1.3 the
squamosal formed a band along the lateral margin of the bulla, whereas in
M8672 there was only a very small inclusion of the alisphenoid just mesial to the
postglenoid process (Fig. 6B). In addition to variation within the bulla, there
was also variability between the bullae of the same individual; in some cases,
formation of the squamosal bulla was asymmetric, with the ‘normal’ alisphenoid
bulla being present on the other side of the skull (Fig. 5).
Variability in bulla composition was strongly linked to geographical
distribution, with squamosal bulla variants being entirely confined to three
islands; Malaita, Makira and Guadalcanal (Fig. 3 ) . Individuals from Malaita
( N = 7 ) and Makira ( N = 6) showed consistent formation of a ‘fully’ squamosal
bulla on both sides of the skull. The Guadalcanal population, however, showed
I00
C. A. NORRIS
great variability in bulla formation. Of 11 individuals sampled from
Guadalcanal, two possessed a squamosal bulla on both sides of the skull; two on
the right hand side only; one showed full formation of the squamosal bulla on the
left hand side, but only partial on the right; and three specimens possessed the
alisphenoid bulla on both sides. All specimens examined from the Nggela
( N = l ) , New Georgia [Ghizo] ( N = 2), Choiseul ( N = 3), Ysabel ( N = 4),
Shortland [Alu] ( N = 3), Bougainville ( N = 8), Buka ( N = 1 ) and Nissan Atoll
( N = 3) populations possessed the alisphenoid bulla on both sides of the skull.
DISCUSSION
T h e formation of squamosal bullae
Expansion and fusion of the ossified areas during the growth of the animal
means that the entotympanic and separate alisphenoid elements cannot be
distinguished in the adult bulla. However, their eventual positions may be
reflected in those individuals from the Guadalcanal population of P . orientalis
which show both alisphenoid and squamosal elements in the bulla. In
individuals where the bulla is predominantly squamosal, the limitation of the
alisphenoid to a small area lateral to the foramen ovale would appear to reflect
the position of the antero-mesial centre of ossification: in those individuals with
an increased alisphenoid contribution, the presence of a squamosal element
along the lateral margin of the bulla might reflect a distribution arising from the
antero-lateral centre of ossification. This would suggest that there are two factors
involved in the formation of the squamosal bulla variant. There is an initial
growth of the squamosal into the area of the antero-lateral centre of ossification,
leading to the formation of a squamosal tympanic process. Subsequently, the
squamosal grows through the fibrous membrane of the primary tympanic floor
in a periosteal manner, as described by MacPhee (1981). However, the extent of
this growth with respect to that of the squamosal is variable, and presumably
arises from the interplay of the rates of ossification of the antero-lateral and
antero-mesial centres. It would appear that, as is stated by MacPhee (1981), the
fibrous membrane of the tympanic floor is exerting formative influence on the
structure of the bulla, with respect to the origin and direction of ossification,
regardless of the identity of the participating elements.
The most likely candidate for the precursor of the squamosal tympanic wing
in P. orientalis is the squamosal entoglenoid process. This structure, which forms
the mesial boundary of the post-glenoid foramen, varies considerably in size and
degree of pneumatization both within and between phalangerid taxa. This
variation may be the source of some of the systematic confusion that surrounds
the Phalangeridae (Flannery, Archer & Maynes, 1987; Springer et al., 1990) and
is at present being reviewed by the author. In P. orientalis the entoglenoid process
varies from a small, tubercular structure, to a fully pneumatized mesial wing,
contributing to the anterior wall of the hypotympanic sinus. A possible scenario
for the incorporation of the squamosal into the tympanic floor would thus begin
with growth of the squamosal entoglenoid process onto the primary tympanic
floor, in advance of alisphenoid growth in this region.
Incorporation of the squamosal entoglenoid process into the bulla occurs in
the placental Lipotyphla, where it is associated with a small tympanic process of
AUDI‘I‘OKY BULLAE IN CUSCUSES
101
the alisphenoid, and in a number of other placental groups small ridges of the
squamosal may be found overlapping the anterior margin of other bulla
elements (MacPhee, 1981 ). Amongst marsupials, enclosure of the anterior
portion of the tympanic cavity by the squamosal has been used by a number of
authors (Tedford et al., 1977; Archer, 1984; Woodburne, 1984; Aplin, 1987) to
define a grouping which Aplin & Archer (1987) term the infraorder
Vombatomorphia. This group comprises the living Vombatidae, and the extinct
Diprotodontidae, Palorchestidae, Wynyardiidae, Ilariidae and Thylacoleonidae.
In these groups, the bulla is largely unossified postero-medially, and the anterior
portion is formed from two distinct, but fused squamosal elements: the
entoglenoid process, and a ‘tympanic process’ (Aplin, 1987), which lies in a more
mesial position (Fig. 2C). In all members of the Vombatomorphia, the
alisphenoid lies well forward of the tympanic cavity. Despite the common
presence of the squamosal in the bulla, the vombatomorph condition is very
different to that seen in the Solomons’ populations of P . orientalis, where, despite
the change in composition, the gross morphology of the bulla remains very
distinctively phalangeriform.
The entolympanic
The enigmatic structures known as entotympanics are found in a number of
groups of placental mammals, but their existence in the marsupial tympanic
floor is the subject of some disagreement. Carlsson (1926) and Wood Jones
(1949) noted the presence of an entotympanic in the dasyurid genera Dasycercus
and Dasuroides respectively, and Segall (1969a, b, 1970, 1971) has reported the
occurrence of the structure in Didelphis, Caluromys, Isoodon and Dromiciops. A low
septum on the inside of the bulla wall, termed the ‘septum sphenoideum’, was
taken by Segall (1971) to signify the division between the tympanic wing of the
alisphenoid and the entotympanic. The existence of this septum in a number of
phalangeroid genera was cited by Segall (1971) as evidence of the existence of
entotympanics in these groups. This view has not, however, met with wide
approval. Archer ( 1976: 228), in his exhaustive review of the marsupicarnivore
basicranium, failed to find any evidence of the existence of entotympanics in the
seven marsupial families studied. MacPhee (1979: 38) stated ‘I know of no
convincing embryological evidence for the oft-repeated assumption that
entotympanics participate in the marsupial tympanic floor’, and Novacek (1977:
144), whilst not denying the possible existence of the structure, described it as
‘rare’. The generally accepted view, therefore, has been that entotympanics are
placental neomorphs, with an undemonstrated possibility that they may occur in
other mammalian groups (MacPhee, 1979).
The presence of an apparent entotympanic in Phalanger, and its position on the
tympanic floor, would appear to confirm Segall’s observations. One possible
explanation for the apparent absence of entotympanics is the groups studied by
Archer (1976) would be that the entotympanic is an independent derivation in
some marsupial lineages. There is, however, a broader question, concerning the
homology of entotympanics. Their patchy distribution across mammalian
lineages, and their apparent variety of developmental characteristics (MacPhee,
1979) suggests that the term ‘entotympanic’ may encompass a broad range of
non-homologous independent ossifications of the tympanic floor, and that the
102
C . A. NORRIS
utility of entotympanics as a character for the study of mammalian systematics
may depend on the results of more detailed studies.
The signiJicance of bulla variabilig in Phalanger orientalis
Beyond the question of how the squamosal bulla is formed in P. orientalis
breviceps there is the more vexing question of why a character which is apparently
stable over much of the species’ range (and, indeed, throughout most of the
Marsupialia) has undergone such a radical change. Possibly the most surprising
observation is not the shift from alisphenoid to squamosal bulla, but the startling
variability of bulla composition in the Guadalcanal population, in contrast to
the almost total consistency of the neighbouring populations. Selective
hypotheses to explain this distribution become problematic when faced with a
population in which a variety of structural intermediates coexist, and a single
individual can possess both types of bulla. Even in the absence of this variable
population, it would be difficult to support a hypothesis based on natural
selection. The work of Fleischer (1978) suggests that the auditory function of the
bulla is related to the maintenance of a constant, optimal volume in the
tympanic region: there is little evidence to suggest that the structure of the bulla
components exerts any influence on hearing (MacPhee, 1981 ) . Where a selective
influence may be seen is in the gross morphology of the bulla, which is
maintained regardless of structural variability.
One possible explanation for the high levels of variability on Guadalcanal
might be developmental instability resulting from a high frequency of
inbreeding. Inbreeds show a great reduction in genetic variance, but an
increased susceptibility to environmental sources of variation; if the increased
environmental variance offsets the reduced genetic variance, then the inbred
population may be more phenotypically variable than a non-inbred stock
(Falconer, 1981). Such variability obviously depends on the extent of the
environmental component in the development of the character in question, and
is probably not an effect of inbreeding per se, but rather a consequence of the
more frequent fixation of deviant genotypes that cross a ‘threshold of
abnormality’ in inbreeds (Wright, 1977).
The possibility of inbreeding in the Guadalcanal population is lent some
credence by recent evidence concerning the probable colonization history of
P. orientalis in Melanesia. Archaeological data suggest that the species arrived in
the Solomon Islands between 6000 and 1800 years BP (Flannery & Wickler,
1990). In combination with other recent arrival dates for the species in Timor
(5000-4000 years BP: Glover, 1986) and New Ireland (10 OOO+ years BP:
Flannery & White, 1991) this lends support to the idea that much of the
peripheral range of P. orientalis has arisen as a result of human introduction
(Flannery, 1989). Out of all the species of Phalanger, many of which are kept as
pets, or for food throughout modern Melanesia, P. orientalis is the only one
known to produce twins regularly. This leads Flannery & White (1991) to
propose that, of all the marsupials in the region, this species may be especially
suited for deliberate translocation: the tendency to produce twins increasing the
probability of successful colonization from a small founding stock. Presumably,
however, there would also be an increased probability of sibling crossbreeding,
leading to inbred populations.
AUDITORY BULLAE IN CUSCUSES
I03
There is also the possibility that marsupials may be more susceptible to
environmental effects than are placentals, by virtue of their reproductive
strategy. Much of the development of the cranium in marsupials, and in
particular the ossification of the otic region, occurs after the birth of the neonate:
in other words, outside the mother’s body. Presumably, therefore, the
environmental component in the development of marsupial characters, and
particularly late-developing characters such as the ossified bulla, may be greater
than that for equivalent characters in placentals.
I t is tempting to view the change, from a variable population on
Guadalcanal to a predominantly squamosal population on Malaita and
Makira, in terms of a founder effect, involving individuals possessing an entirely
squamosal bulla colonizing either Malaita or Makira (or both) from
Guadalcanal. T h e problem with such biogeographical theories is the limitation
imposed by the small sample sizes available for this study. Without more
specimens from the ‘central’ islands of New Georgia, Choiseul and Ysabel, it is
impossible to state categorically that bullae from these populations are largely
invariant. Furthermore, larger samples from Malaita and Makira might reveal
less consistency in the occurrence of the squamosal bulla than appears at present
to be the case.
CONCLUSIONS
MacPhee (1981) describes the membrane of the primary tympanic floor as
‘the stage upon which many of the significant events of tympanic floor ontogeny
are enacted’. T h e freedom with which the ‘players’ are seen to move on this
stage in the Solomon Islands’ populations of Phalanger orientalis is perhaps not so
remarkable: the classical view of sutures as inviolable entities has long been
recognized as an oversimplification (Hoyte, 1966). What is remarkable is the fact
that such freedom has not previously been recorded, especially given that the
type specimen of P. orientalis breviceps (BMNH 55.1 1.7.14: Thomas, 1888) is a
specimen from Makira, possessing squamosal bullae. These phenomena may be a
result of a unique set of circumstances in the Solomons’ populations, or there
may be other examples of such developmental plasticity as yet unrecognized.
T h e conclusion, so far as the auditory bulla is concerned, is that these
observations suggest that considerable flexibility of composition can be permitted
within the selective constraints of function, even within a single individual. This
may imply that the candidacy of the bulla as a taxonomic character for
mammalian systematic studies should be treated with some caution.
ACKNOWLEDGEMENTS
I am most grateful to the Natural History Museum, London and the
Australian Museum, Sydney, for permitting me access to their collections. Dr T.
Flannery has been the source of much help and encouragement, and first drew
my attention to the existence of these bulla variants. Drs P. Ahlberg, T. S.
Kemp and J. Searle read the manuscript, and provided many useful suggestions,
and I have benefited from discussion with a number of colleagues, notably Drs P.
Holland, R. Presley and A. Read. This work was supported by a Senior Fiddian
Scholarship from Brasenose College, Oxford.
104
C. A. NORRIS
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I ,
AUDITORY BULLAE IN CUSCUSES
KEY TO ABBREVIATIONS USED IN FIGURES
Inclusion of alisphenoid in squamosal bulla
Alisphenoid
Tympanic wing of alisphenoid
Basioccipital
Entotympanic
Ectotympanic
Foramen ovale
Glenoid fossa
J:
J u d
M:
Mastoid wing of periotic
P:
Petrosal wing of periotic
PGP:
Postglenoid process
PLF:
Posterior lacerate foramen
POCPT: Paroccipital
SEP:
Entoglenoid process of squamosal
SQ
Squamosal
STW:
Tympanic wing of squamosal
TY:
Tympanic
AI:
ASPH:
ATW:
BOCPT:
E:
ECT:
FO:
GF:
105
106
C. A. NORRIS
APPENDIX
Specimens examined
Phalanger orientalis orientalis
Ceram
BMNH 20.7.26.3
BMNH 10.3.4.6
BMNH 10.3.4.61
Ambon
BMNH 32.7.20.5
BMNH 11.7.12.51
BMNH 72.3.5.7
Buru
BMNH 10.3.3.50
BMNH 22.8.26.9
Total number of specimens in growth series = 8
Phalanger orientalis breviceps
Nissan Atol
BMNH 1939.3122
M 17206
M I4566
Buka
MI9821
Bougainville
M5586-88
M5753-55
M6489-90
Shortland Islands
BMNH 87.1.18.20-22
Choiseul
M 19751-52
M20729
New Georgia
BMNH 4.4. I 1.2
BMNH 1939.3139
Ysabel
BMNH 1939.3140
BMNH 1939.3142
M3690
M3692
Nggela (Florida Islands) BMNH 1939.3133
Guadalcanal
BMNH 88.1.5.41-42
BMNH 34.9.1.2-3
BMNH 1939.313437
M19749-50
M20946
Malaita
M8666-72
MI9753
Makira (San Cristobal)
BMNH 35.9.2.3
BMNH 55.11.7.6
BMNH 55.1 1.7.14’
BMNH 56.7.7.6
BMNH 1939.3136
M20949
Total number of specimens from Solomon Islands
= 50
*Holotype of ‘Phalangcr brcviceps’ (Thomas, 1888).
BMNH Natural History Museum, London; M, Australian Museum, Sydney.