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Just how many species of Spirula are there? A morphometric approach


Abstract and Figures

We compare 110 Spirula shells from five geographical areas. Morphometry provides a criterion for determining when shell growth ends (decrease in whorl height). Characteristics of adult shells apparently vary with geographical origin: specimens from Madagascar, New Zealand and Brazil are larger than those from North-West Africa and Australia. These findings challenge the monospecific status of the genus Spirula but fall short of proving the occurrence of more than one species. Supplementary molecular investigations are called for.
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Tanabe, K., Shigeta, Y., Sasaki, T. & Hirano, H. (eds.) 2010. Cephalopods - Present and Past
Tokai University Press, Tokyo, p. 77-84.
Spirula, with its well-developed internal chambered
shell, is one of the most unusual Recent cephalopods.
Empty shells of Spirula can be found in great numbers
on oceanic beaches in the Atlantic, Indian and West
Pacific Oceans (Bruun 1943, Clarke 1966). As with
many other epi- and mesopelagic circumtropical spe-
cies, Spirula’s distribution is patchy, apparently there is
no gene ow around South Africa between the Atlantic
and Indo-Pacific parts of its range (Nesis, 1998). This
observation challenges the classical taxonomic opinion
that only one biological Spirula species exists. Cryptic
species could be relatively easily detected by molecular
analysis but, unfortunately, well-preserved material of
whole Spirula is scarce, and most collections of Spirula
were preserved in formol; and so it is quite rare to nd
ethanol xed tissue on which DNA molecular analyses
can be conducted. A preliminary study of four Spirula
specimens caught near Fuerteventura (Canary Islands,
Spain) and sequences (from the gene bank) of one Spir-
ula from New Caledonia were examined for indications
about the diversity of the geographically fragmented
populations (Warnke, 2007). Fragments of mitochon-
drial genes, 16S rRNA (16S) and cytochrome oxidase
subunit III (COIII) were analysed. The 16S sequences
proved to be nearly identical (99.8–100%) whereas the
nucleotide sequences of COIII revealed moderate di-
vergence (0.7–1.3%) between the sequences of Spirula
from Fuerteventura and New Caledonia. The translated
COIII amino acid sequences displayed substantial di-
vergence (3.9–4.6%), but this result was supported by
single sequence from a single Spirula from New Cale-
donia, so the marked sequence divergence may be an ar-
tefact. In short, the analysis provided no clear answer to
whether there are multiple Spirula species. The present
study proposes further evidence on this issue based on
shell shape and growth. These morphometric analyses
are computed using intrapopulational (i.e. geographi-
cal), interpopulational and ontogenetic investigations.
Taxonomic framework
Since Linnaeus (1758) first defined the species he
termed Nautilus spirula, taxonomic history has re-
corded a rise in the number of reported Spirula species
(see Young and Sweeney, 2007 for a review) before the
eventual return to just the one Spirula spirula (Linnaeus,
1758). The genus Spirula was defined by Lamarck
(1799). It is now generally considered that this genus is
monospecific. Some have suggested the occurrence of
geographical subspecies (Bruun 1943), one in the Atlan-
tic and the other in the Indo-West Pacic (Nesis, 1998),
but evidence for this is still lacking.
Just how many species of Spirula are there?
A morphometric approach
1Laboratoire Biogeosciences, Université de Bourgogne, CNRS, 6 Boulevard Gabriel, F-21000 Dijon, France
(*Corresponding author;
2Freie Universität Berlin, FR Paläontologie, Malteserstr. 74-100, Haus D, 12249 Berlin, Germany
Received May 7, 2008; Revised manuscript accepted November 7, 2008
Abstract. We compare 110 Spirula shells from ve geographical areas. Morphometry provides a criterion for
determining when shell growth ends (decrease in whorl height). Characteristics of adult shells apparently
vary with geographical origin: specimens from Madagascar, New Zealand and Brazil are larger than those
from North-West Africa and Australia. These ndings challenge the monospecic status of the genus Spirula
but fall short of proving the occurrence of more than one species. Supplementary molecular investigations
are called for.
Key words: Spirula, morphometry, ontogeny
Pascal Neige and Kerstin Warnke78
Figure 1. Geographical distribution of Spirula spirula after Okutani (1995) (dark grey) and Reid (2005) (light grey), and location
of sampling areas (each sampling area is indicated on the map by its code and the number of specimens measured). Question marks indicate
imprecise locations. Stars indicate specimens reported by Haimovici et al. (2007). Five main geographical units are dened: NWAF (North-
West Africa), BRA (Brazil), MADA (Madagascar), AUS (West Australia) and NZEL (New Zealand). See Table 1 for further abbreviations.
Main geographical
areas Label n
NWAF West Morocco (coll. Warnke) Mo 7
Fuerteventura (coll. Warnke) Fu 14
Playa del Ingles (coll. Warnke) Ca 6
BRA Caponga Beach (coll. J. Geraldo de Aratanha) BRA-F 3
Canoa Quebrada (coll. M.A. Reis Jr.) BRA-A 10
MADA Port Ostafrika (coll. Museum für Naturkunde, Berlin) PoO 8
Madagascar NW (coll. S. Kiel) MaNW2 10
Manakara (coll. J. Hartmann) MKSE 22
Madagascar SE (coll. J. Hartmann) MaSE 9
AUS South West Australia (coll. K. Bandel) KB 3
NZEL Ninety Mile Beach (coll. F. Riedel) NMB 9
New Zealand (coll. F. Riedel) NZ 9
Table 1. Location and number of specimens used in this study (see also Fig. 1). coll. = collection. n = number of measured speci-
mens for a given locality.
How many species of Spirula? 79
Material and methods
A set of 110 shells was measured in this study. All
were collected from beaches. The specimens measured
were the best preserved ones from a larger sample. They
come from various areas covering a broad span of the
known geographical distribution of Spirula. Five main
geographical areas are dened here based on sampling
localities (see Figure 1 and Table 1): North-West Africa
(NWAF), with specimens from the Canary Islands and
from the coast of Morocco; Brazil (BRA), all specimens
from two localities close to Fortaleza; the Madagascar
area (MADA), with specimens from the east and west
coasts of Madagascar and from Mozambique; South-
West Australia (AUS), with specimens collected not
far from Perth; and the North Island of New Zealand
(NZEL). Because this analysis is based on shells col-
lected from beaches, we cannot exclude the effect of
post-mortem drift. This may be the case particularly
for BRA shells, located outside the known geographi-
cal distribution of Spirula. The results will thus be dis-
cussed (see “Discussion”) on the assumption that ana-
lyzed samples might represent nearby populations.
A new measurement protocol was defined for de-
ciphering shell growth as accurately as possible. The
anterior boundaries of ventral and dorsal sutures (sensu
Naef, 1923) were used as landmarks (Figure 2A). Their
coordinates being known throughout growth (i.e., mea-
sured for each septa), basic trigonometric equations
were used to calculate several parameters with which to
describe the shell (Figure 2B).
A particularly complicated issue is to dene the cen-
tre of the supposed logarithmic spiral of Spirula shell
growth. Several workers have addressed this issue (e.g.,
Landman 1987, Neige 1997 for ammonites). Schindel
(1990) attempted to locate such a starting point for
growth (the apex) when studying gastropod ontogeny.
He concluded that radius measurements included an
oscillating error term arising from mislocation of the
Figure 2. Shell measurements. A. Location of P1 (0;0) and details (left) showing the locations of the successive landmarks. B. Cal-
culated parameters (from landmark coordinates, see main text) used to study shell growth: r is radius, H is whorl height, and α is the angle
between two successive septa.
Pascal Neige and Kerstin Warnke80
Figure 4. Comparative shell growth for the ve main geographical areas (see Table 1 for abbreviations).
Figure 3. Example of individual growth (case of specimen NZ-02). A. radius versus whorl height. This pattern shows
a decrease in whorl height at the end of growth (see main text). B. radius versus α.
How many species of Spirula? 81
apex (see also Neige 1997 for similar considerations on
ammonites). Certain mathematical calculations might
help in defining a theoretical initial growth point of
the spiral but would necessarily assume a perfect loga-
rithmic growth throughout ontogeny. Such mathemati-
cal extrapolation might mask ontogenetic changes in
growth of the shell. Because the present study explores
ontogeny, we prefer to locate the initial growth point at
an anatomical landmark: the dorsal attachment of septa
number 1. By convention, P1 coordinates (dorsal attach-
ment of septa 1, Figure 2A) are x = 0 and y = 0. This
excludes any articial correction of growth parameters,
but produces more prominent articial oscillations dur-
ing early growth stages.
The anterior boundaries of ventral and dorsal sutures
were located using a microscope with transmitted light.
Measurements were made with an optic measuroscope
(Nikon Measuring Microscope MM-60; precision of 1
μm). Measurement error was estimated by measuring
one specimen nine times with complete repositioning
and measurement. Error was very low compared with
differences between specimens from a given locality.
A Kruskal-Wallis test was used to test for differences
in the adult-stage parameters: radius, whorl height,
number of septa and rotational angle. The Kruskal-Wal-
lis test can be applied as a single factor non-parametric
ANOVA case. It is useful for situations where the usual
ANOVA normality assumptions may not apply, which is
the case here because of small sample sizes for Austra-
lia (n = 3) and Brazil (n = 7). This test indicates whether
observed differences between means of a given param-
eter and for several populations are statistically signi-
cantly different. H0 is that observed differences are due
to a sampling effect. H1 is that at least two populations
have statistically different means.
Two complementary analyses were conducted: one
focusing on individual growth; the other comparing the
various growth parameters for the ve main geographi-
cal areas dened here.
The growth parameters of each of the 110 specimens
were investigated. Because the anterior boundaries of
suture attachments were measured for all the septa of
each specimen, growth could be described very pre-
cisely, particularly in terms of whorl height versus shell
One pattern is largely dominant (68 specimens; i.e.,
64.5% of the complete sample). This pattern involves
a characteristic decrease in whorl height at the end of
growth (Figure 3A). Only in three specimens (i.e., 2.7%
of the complete sample) is this decrease followed by a
fresh increase in shell height, and even then it is a tiny
increase limited to only one or two septa. 39 specimens
display no decrease in whorl height during growth.
These are interpreted as juvenile or broken shells. The
decrease in whorl height may be considered as an indi-
cation of the imminent end of growth in Spirula. It is
considered here as a homologous feature, indicative of
a homologous stage of growth. For convenience, this
stage (onset of the end of growth) is termed the ‘adult
stage’ in what follows.
Angle variations between two successive septa are
similar between specimens. Specimen NZ-02 (Figure
3B) is used as an example. A rst phase displays high
values (nearly 55°). These large initial angles can be
explained by the bulbous shape of the first chamber.
Thereafter the angle decreases in the course of growth
to about 20°. A further small decrease in septal angle
occurs at the very end of growth.
Population approach
A population analysis is made on adult shells only
(i.e., those meeting the criterion for the end of growth
defined above) to explore geographical differences in
shell characteristics. The five main geographical areas
are used for that purpose (see Figure 1).
Shells from the same areas display similar patterns
of growth in terms of whorl height increase (Figure 4).
Moreover, the growth of specimens is conservative at
the complete sample scale. The main difference between
specimens from the ve main geographical areas occurs
at the end of growth. On average (see Figure 4), shells
from Madagascar attain the greatest whorl heights at
the end of growth. Shells from New Zealand and from
Brazil display intermediate whorl heights; those from
Area Mean Min Max n
AUS 27 25 29 3
BRA 28.7 25 31 7
MADA 30.5 27 34 28
NWAF 27 24 30 17
NZEL 29 26 34 13
Table 2. Mean, minimum and maximum of septa at adult stage (see
main text for end of growth criterion) for the ve main geographical
areas (NWAF (North-West Africa), BRA (Brazil), MADA (Madagas-
car), AUS (West Australia) and NZEL (New Zealand). n = number of
adult shells.
Pascal Neige and Kerstin Warnke82
North-West Africa and Australia the smallest whorl
heights. These results may be seen differently on graphs
and statistically tested. For that purpose, we calculated
the mean whorl height at the adult stage as defined
above, associated, at this adult stage, with the mean ra-
dius, the mean number of septa and the mean rotational
angle for each of the ve main geographical areas (i.e.,
using individual measurements of radius, number of
septa and rotational angle associated with the maximum
whorl height).
Mean values and associated standard deviations are
presented in Figure 5. This conrms previous observa-
tions about differences in whorl height at the adult stage
between geographical populations (Figure 5A). The pat-
tern for the number of septa is very similar (Figure 5B).
On average, at the adult stage, shells from Madagascar
have 30.5 septa (Table 2). By contrast, at the adult
stage, shells from Australia and North-West Africa have
only 27 septa. The pattern for rotational angle at the
adult stage is less differentiated between geographical
Figure 5. Bivariate plots showing differences in measurements for adult shells only. Means and standard deviations are given
for shells from the ve geographical areas (NWAF (North-West Africa), BRA (Brazil), MADA (Madagascar), AUS (West Australia) and
NZEL (New Zealand).
How many species of Spirula? 83
areas (Figure 5C). Table 3 shows the Kruskal-Wallis test
results for these observations. All comparisons reveal
statistical differences among populations, although the
difference for rotational angle is less marked (p = 0.023).
This study uses a morphometric exploration of shell
growth to propose pointers for investigating species
structuring within Spirula. This should be seen as a rst
step towards a comparative analysis using both morpho-
metric and molecular approaches. However, a number
of ndings are worth discussing:
1. We propose a criterion for detecting the end of
shell growth based on the recognition of a decrease in
whorl height. This ontogenetic pattern is common in the
populations under study (64.5%). It would be interesting
to compare this criterion with others based on the soft
parts of the animal. This criterion has made it possible
to compare shells from different geographical popula-
tions at an equivalent (adult) growth stage.
2. The comparisons revealed differences in measure-
ments between populations at the adult stage. We sta-
tistically tested differences in values of radius, whorl
height, number of septa and rotational angle. Differenc-
es between populations may be relatively large: for ex-
ample the mean number of septa at the adult stage is 27
for North-West African specimens versus 30.5 for shells
from Madagascar. Similarly, whorl height is nearly 5.78
mm for shells from Madagascar versus nearly 4.86 mm
for shells from North-West Africa, a difference of nearly
20%. Schematically, two separate clusters can be recog-
nized: specimens from Madagascar, New Zealand and
Brazil, with larger dimensions at the adult stage, and
specimens from North-West Africa and Australia. It is
difcult to explain this clustering in terms of geography.
It should be remembered that the analyzed popula-
tions contain shells that might have been subjected
to post-mortem drift. Post-mortem drift is a common
phenomenon within recent shelled cephalopods and
has lead to misinterpretation of geographical ranges of
some of them. For example, cuttleshes have been er-
roneously supposed to occur in the Western Atlantic
Ocean because of cuttlebone post-mortem drift (see
Voss, 1974). Analyzes of shell preservation and epizoan
occurrences on Spirula shells collected from the beach
by Dauphin (1979a, b) were inconclusive regarding the
exact geographical origin of the living population, and
thus the possibility of intense geographical drift. As a
result, she favoured a distant origin because of the lack
of any living specimen caught in the area. Similarly,
shells used here for BRA locality are not included in the
known geographical distribution of Spirula spirula (see
Figure 1). However, Haimovici et al. (2007) recently
reported S. spirula along Brazilian coasts (Bahia state)
southward of the beaches studied here. Only few com-
plete specimens have been found (e.g., not only shells
but nor a living population). Thus, the Brazilian shells
used in the present study may have been drifted, but for
a short distance. In addition, the relatively homogenous
distributions of morphological features within popula-
tions compared to statistical differences of morphologi-
cal features among populations suggest that shell popu-
lations reect natural living populations. More work is
needed to clearly determine whether Spirula popula-
tions live along the Brazilian coasts and thus to identify
the exact extent of geographical drift.
The results obtained here clearly challenge the tradi-
tional monospecic status of Spirula. However, they are
only preliminary findings and do not demonstrate the
existence of two or more species. A molecular analy-
sis is now needed. It would be interesting also to use
a similar morphometric approach but based on sexed
specimens to control for any sexual dimorphism. An
alternative hypothesis to the occurrence of two or more
species to account for the observed morphometric dif-
ferences is ecophenotypy. This could also be tested by a
molecular approach. In practice, this will prove difcult
because complete Spirula specimens are seldom caught.
Although limited in geographical scope compared to the
present study, an analogous analysis based on Nautilus
may help interpreting the present results (Tanabe et al.
1990). In spite of their non-overlapping distributions
(live-caught specimens were coming from the Philip-
H p-values
Radius at adult stage, Geographical areas 43.6 <0.0001 ***
Whorl height at adult stage, Geographical areas 49.7 <0.0001 ***
Number of septa at adult stage, Geographical areas 25.9 <0.0001 ***
Rotational angle at adult stage, Geographical areas 11.3 0.023 *
Table 3. Non parametric Kruskal-Wallis test for various data sets (see main text). H is the Kruskal-Wallis test statistic. Results are
given for ex-aequo correction. *: test signicant at 95% condence level; ***: test signicant at 99.9% condence level.
Pascal Neige and Kerstin Warnke84
pines, Fiji and Palau), Nautilus from the three popula-
tions shared quite similar overall shell morphology but
could be distinguished by adult features such as the
dimensions of the shell and total number of septa. Using
such results and some genetic data (from Woodruff et al.
1987), the authors concluded that the three populations
belong to the same wide-ranging species. Based on ge-
netic and morphological exploration of Nautilus coming
from different geographic areas, Wray et al. (1995) con-
cluded similarly that some of the morphological features
used to dene Nautilus species may represent variation
within one widespread species. Applied to the present
analysis, this would mean that observed morphological
differences between populations could represent varia-
tion within a single species. However, it is worth noting
that the geographic variation described here for Spirula
is much more extensive than that for Nautilus. Finally,
new genetic and morphological data are needed before
to determine Spirula species number.
We thank M. Aeppler, J. Geraldo de Aratanha, K.
Bandel, J. Hartmann, S. Kiel, F. Riedel, M.A. Reis
Jr, Ignacio Santana and the Museum für Naturkunde
(Berlin) for kindly providing Spirula shells. Thanks to
Emmanuelle Pucéat for her help in computing trigono-
metric equations to transform landmark coordinates into
distances and angle measurements. We are grateful to
participants at the 7th International Symposium, Cepha-
lopods Present and Past for their discussions during
the meeting. We thank Kazushige Tanabe for his helpful
comments, and Sylvain Gerber, Melanie J. Hopkins and
Michael Labarbera for checking our English. This work
was supported by the DFG WA 1454/2-1 grant from the
Deutsche Forschungsgemeinschaft (DFG) to Kerstin
Warnke. This paper is a contribution to the FED (Forme,
Evolution, Diversité) team of UMR CNRS 5561 Bio-
géosciences, and to GDR MEF (Morphométrie et Evo-
lution des Formes).
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... The species, Spirula spirula (Linnaeus, 1758), commonly known as Ram's horn squid, is one of the most inscrutable cephalopods with an internal loosely coiled chambered shell (Lukeneder, 2016). This species is considered monospecific under the genus Spirula (Lamarck, 1799) and recent findings from chambered shell structure challenge the monospecific status of the genus but fall short of proving the occurrence of more than one species (Neige and Warnke, 2010;Haring et al., 2012;Lukeneder et al., 2008;Lukeneder, 2016). Spirula inhabits subsurface waters of the tropical and subtropical regions with a disjunctive range of geographic occurrence (Nesis, 1998;Lukeneder, 2016). ...
... Spirula inhabits subsurface waters of the tropical and subtropical regions with a disjunctive range of geographic occurrence (Nesis, 1998;Lukeneder, 2016). The internal, loosely coiled, chambered shell of S. spirula starting from a spherical initial chamber, resembles the external chambered shells of Ammonoidea, the extinct cephalopod subclass that flourished for more than 340 million years from the middle Devonian to the end of the Cretaceous period (Bandel and Bolezky, 1979;Neige and Warnke, 2010 Original Article of an internal chambered shell in this species, it has frequently been used as a model species to investigate the palaeo-biology of fossil coleoids (Ohkouchi et al., 2013). ...
... Recently, a video of Spirula sp. in its natural habitat at 861 m depth showed, they floated heads upwards, so the light organ points downwards and helped the animal to camouflage for predators coming from below (Lindsay et al., 2020). The taxonomic status of the species is unresolved Nesis (1998) and Neige and Warnke (2010) suggested using a molecular key to distinguish between the intra and interspecific differences. The current specimen, preserved in formaldehyde, constrained molecular investigation. ...
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This study describes the rediscovery of the largely uncommon, mesopelagic cephalopod, Spirula spirula, from the Arabian Sea. This is the first confirmed record of the species from the seas around India after 80 years of its original record. Four specimens were collected from the Arabian Sea from a depth of 450 m, during the fishery surveys onboard the FORV Sagar Sampada, using a mid-water trawl net. The dorsal mantle length (DML) of the individuals ranged from 27 to 36 mm. Detailed morphometric measurements and previous distribution records are also provided.
... In Sepia, many different species have been described (Norman, 2000), while for the supposedly monospecific Spirula the taxonomic status is still being debated (e.g. Warnke, 2007;Neige & Warnke, 2010;Lukeneder, 2016). Earlier workers have described several species and subspecies of Spirula solely on conchs. ...
... The patchy distribution of the mesopelagic Spirula in Indonesia, Melanesia, Australia, southeast Africa, the Caribbean Sea, the Gulf of Mexico and between the Canary Islands and northwest Africa suggests that there may be more than one extant species. Moreover, based on morphological comparisons, Nesis (1998), Warnke (2007) and Neige & Warnke (2010) argued that there was no gene flow between the Atlantic population and that living in the Indo-Pacific around South Africa. ...
... Individuals of Spirula live for 18-20 months (Clarke, 1970) and their biogeography seems to be limited by water temperature (10-20°C) and depth (100-1000 m), resulting in a disjunctive occurrence near oceanic islands and the continental shelf in tropical and subtropical waters (Neige & Warnke, 2010;Lukeneder, 2016). Specimens from the Indian Ocean (the largest specimens come from the Maldives and Thailand) are larger than those from the Atlantic and the Pacific, and specimens from the Canary Islands are by far the smallest. ...
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Spirula spirula (Coleoidea: Decabrachia) is a unique deep-sea squid with an uncertain taxonomic status. Here, we apply geometric morphometric analyses to precisely describe changes in conch morphology during the course of ontogeny of 21 specimens collected from 12 localities worldwide. These data were used to explore whether the genus is monospecific or comprises several species. Different 2D and 3D conch parameters are presented based on micro-computed tomography data, combining noninvasive imaging techniques with a range of morphometric analyses. Our data imply that Atlantic and Indo-Pacific specimens form two distinct morphological clusters, potentially representing two pseudocryptic species or two populations undergoing divergence (i.e. in the process of speciation). Given the evolutionary trend from straight to more coiled forms, we suggest that S. spirula represents a neotenous form that migrated from the Indo-Pacific towards the Atlantic via the Agulhas leakage, which has been active since the closure of the Strait of Panama (10–3 Ma).
... Data for conch characteristics were obtained from longitudinal-and cross-sections for every 10 degrees (Fig. 1). Following Neige and Warnke (2010), we used the same anatomical landmark (dorsal attachment of the first septum) as the shell centre. Besides morphometry, CT-data are used for volumetric analyses, e.g., chamber volumes and surface areas. ...
... Neglecting intraspecific variability can lead to taxonomic oversplitting or lumping, i.e., modulated taxonomy and taxonomic richness (palaeodiversity; see De Baets et al. 2013a. In the case of Spirula, the actual number of extant species was questioned (Warnke, 2007;Neige and Warnke, 2010). The reason for this was the scattered geographic distribution of seemingly isolated Spirula spirula populations around the globe and the lack of an adequate morphological description of the type material (Hoffmann and Warnke, 2014;Nikolaeva, 2015;Lukeneder, 2016). ...
... The morphological variation of the different populations (ecophenotypes) of specimens of a single species may lead to an erroneous assignment to different morphospecies. In order to solve this, Neige and Warnke (2010) as well as Lukeneder (2016) employed quantitative measurements, e. g., whorl height against radius or diameter and septal spacing/ radius, whorl width against diameter, whorl height/ whorl width against diameter, of different shell parameters and ratios without a robust conclusion on the number of valid species. ...
Here, we report on different types of shell pathologies of the enigmatic deep-sea (mesopelagic) cephalopod Spirula spirula. For the first time, we apply non-invasive imaging methods to: document trauma-induced changes in shell shapes, reconstruct the different causes and effects of these pathologies, unravel the etiology, and attempt to quantify the efficiency of the buoyancy apparatus. We have analysed 2D and 3D shell parameters from eleven shells collected as beach findings from the Canary Islands (Gran Canaria and Fuerteventura), West-Australia, and the Maldives. All shells were scanned with a nanotom-m computer tomograph. Seven shells were likely injured by predator attacks: fishes, cephalopods or crustaceans, one specimen was infested by an endoparasite (potentially Digenea) and one shell shows signs of inflammation and one shell shows large fluctuations of chamber volumes without any signs of pathology. These fluctuations are potential indicators of a stressed environment. Pathological shells represent the most deviant morphologies of a single species and can therefore be regarded as morphological end-members. The changes in the shell volume / chamber volume ratio were assessed in order to evaluate the functional tolerance of the buoyancy apparatus showing that these had little effect. Key words: pathology; parasitism; Spirula; mesopelagic; ecology; predator; buoyancy; cephalopods
... Spirula spirula occurs in open subtropical to tropical oceans from about 30°N to 30°S (d'Orbigny 1843; Clarke 1966Clarke , 1970Clarke , 1986; 10°N to 25°S in the Atlantic and 10°N to 35°S for Indian Ocean in Goud 1985;Nesis 1991;Okutani 1995;50°N to 35°S in Haimovici et al. 2007;Lukeneder et al. 2008;Neige and Warnke 2010;Haring et al. 2012;Hoffmann and Warnke 2014; Fig. 1). Conclusions about its basic ecology and habitat preferences are mainly based on dredging and on fishery data (Chun 1910;Schmidt 1922;Kerr 1931;Bruun 1943;Clarke 1970;Haimovici et al. 2007). ...
... Its patchy distribution range raises further questions about its phylogeography (Fig. 1). Over the last few years, new live catch data (Santos and Haimovici 2002;Perez et al. 2004;Haimovici et al. 2007;Neige and Warnke 2010;pers. comm. ...
... The aim of a recent study by Haring et al. (2012) was to reassess the postulate of species differentiation between the populations from the Atlantic and the Pacific (Warnke 2007) and to Schmidt (1922), Bruun (1943Bruun ( , 1955, Clarke (1966), Goud (1985), Nesis (1987Nesis ( , 1991, Joubin (1995), Reid (2005), Norman (2007), Lukeneder et al. (2008). For comparison see also Okutani (1995), Haimovici et al. (2007), Neige and Warnke (2010), Haring et al. (2012), and Hoffmann and Warnke (2014). Marine regions were classified in accordance with Claus et al. (2014a, b). ...
In September 2014, the 9th International Symposium Cephalopods—Present and Past (ISCPP) and the 5th International Coleoid Symposium were held at the University of Zurich. The numerous contributions from two joint symposia fill more than one special issue. After the first special issue, which was published in 2015 in the Swiss Journal of Palaeontology (Vol 134, Issue 2), the present second special issue also contains contributions from all fields of research on fossil and Recent cephalopod. In this editorial, we provide a short obituary honouring Fabrizio Cecca and report from the three conference field trips.
... Spirula spirula occurs in open subtropical to tropical oceans from about 30°N to 30°S (d'Orbigny 1843; Clarke 1966Clarke , 1970Clarke , 1986; 10°N to 25°S in the Atlantic and 10°N to 35°S for Indian Ocean in Goud 1985;Nesis 1991;Okutani 1995;50°N to 35°S in Haimovici et al. 2007;Lukeneder et al. 2008;Neige and Warnke 2010;Haring et al. 2012;Hoffmann and Warnke 2014; Fig. 1). Conclusions about its basic ecology and habitat preferences are mainly based on dredging and on fishery data (Chun 1910;Schmidt 1922;Kerr 1931;Bruun 1943;Clarke 1970;Haimovici et al. 2007). ...
... Its patchy distribution range raises further questions about its phylogeography ( Fig. 1). Over the last few years, new live catch data (Santos and Haimovici 2002;Perez et al. 2004;Haimovici et al. 2007;Neige and Warnke 2010;pers. comm. ...
... size) vary with different geographic origins. As both Neige and Warnke (2010) and Haring et al. (2012) already noted, the morphology in Spirula cannot operate as the sole proxy for proving the species types within this group of cephalopods. The additional morphometric approach presented herein helps to understand these enigmatic deep-water squids. ...
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The ram’s horn squid Spirula spirula is a unique deep-water marine organism whose life cycle remains enigmatic. Interpretations of its ecology and habitat preferences are currently based solely on dredging, on fishery data, stable isotope data and rare molecular genetic analyses of dead specimens. These methods form the basis to decipher phylogeographic questions of otherwise unobservable deep-sea animals such as S. spirula. Here, new morphological data from internal shells (specimens n = 408, analysed n = 260) are presented from 12 different populations over huge distances, from the Atlantic, Indian and the Pacific Oceans. A monospecific status is assumed for Spirula, with its species S. spirula. The dataset shows a highly variable shell morphology including size distribution within distinct populations. Populations from the Indian Ocean are larger than those from the Atlantic and the Pacific. Specimens from the northern Indian Ocean (Maldives, Sri Lanka, Thailand) are larger than specimens from the eastern Indian Ocean (Mauritius, Tanzania) and the south-eastern Indian Ocean (western Australia). Specimens from the eastern Atlantic (Canary Islands) are smaller than those of the western Atlantic (Brazil, Tobago). The Canary Islands yielded by far the smallest specimens, while the largest specimen comes from Thailand. Specimens from the locality at eastern Australia (south-west Pacific) have an intermediate size range. Morphologic and geographic data suggest a geographically induced size differentiation within S. spirula. Preliminary findings on conchs mirror the known (from soft parts) existence of two sexual dimorphs in Spirula. The next step would be to collect more material from other localities. A more detailed morphometric approach based on specimens from which the sexes are known is required to enable a detection of the presence of sexual dimorphism by morphometric analyses on internal shells of Spirula.
... Although live observations of Spirula are very rare, there have been important advances in our understanding of its shell structure and function [11,12], life history and biogeography [13,14] and phylogeny and systematics [15][16][17]. Still, live observations offer researchers a unique opportunity to directly examine the behavioral responses of organisms about which behavior otherwise has to be merely surmised. ...
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The ram’s horn squid Spirula spirula (Linnaeus, 1758) is the only extant cephalopod with an internal calcareous, chambered shell that is coiled, making it the sole living representative of the once speciose order Spirulida [...]
... This species is a small-sized mesopelagic cephalopod (Coleoidea, Decabrachia), rarely observed in its natural environment. It is considered as a monospecific genus (Haring et al., 2012;Neige and Warnke, 2010) and even a monospecific order, whose shell exhibits peculiar characteristics. Some of them are reminiscent of the distantly related Nautilus, such as planispiral coiling and a chambered shell where chambers are separated by concave septa and communicate via a siphuncle, a primordial morphology (plesiomorphic character) within cephalopods. ...
Molluscs are one of the most diversified phyla among metazoans. Most of them produce an external calcified shell, resulting from the secretory activity of a specialized epithelium of the calcifying mantle. This biomineralization process is controlled by a set of extracellular macromolecules, the organic matrix. In spite of several studies, these components are mainly known for bivalves and gastropods. In the present study, we investigated the physical and biochemical properties of the internal planispiral shell of the Ram's Horn squid Spirula spirula. Scanning Electron Microscope investigations of the shell reveal a complex microstructural organization. The saccharides constitute a quantitatively important moiety of the matrix, as shown by Fourier-transform infrared spectroscopy. Solid-state nuclear magnetic resonance spectroscopy identified β-chitin and additional polysaccharides for a total amount of 80% of the insoluble fraction. Proteomics was applied to both soluble and insoluble matrices and in silico searches were performed, first on heterologous metazoans models, and secondly on an unpublished transcriptome of Spirula spirula. In the first case, several peptides were identified, some of them matching with tyrosinase, chitinase 2, protease inhibitor, or immunoglobulin. In the second case, 39 hits were obtained, including transferrin, a serine protease inhibitor, matrilin, or different histones. The very few similarities with known molluscan shell matrix proteins suggest that Spirula spirula uses a unique set of shell matrix proteins for constructing its internal shell. The absence of similarity with closely related cephalopods demonstrates that there is no obvious phylogenetic signal in the cephalopod skeletal matrix.
... Voss (1974) was the first to dispute the occurrence of cuttlefish in the western Atlantic, stating that one record referred to misidentified animal remains, and others are attributed to sepions transported over thousands of miles. Lu (1998: 213) also refers to 'sepions carried over long distances by ocean currents', and Neige and Warnke (2010) warn of post-mortem drift bias in their study of Spirula. ...
Post-mortem drift is a common phenomenon within living shelled cephalopods (Nautilidae, Sepiidae and Spirulidae) and has led to the misinterpretation of geographical ranges in some species. In this study, the distributional ranges of reliably identified cuttlefish and beach-collected sepions (cuttlebones) from the Australian Museum, Museum Victoria and the Museum and Art Gallery of the Northern Territory collections were compared to determine the extent of sepion drift. In 12 of the 24 species examined, the distributions of dry sepions extended beyond the currently known ranges of the living populations as ascertained from the collection of intact animals. In some cases, this was in the order of hundreds of kilometres. These discrepancies are discussed in relation to the known depth ranges of each species, sepion morphology and oceanography. The results suggest that a cautionary approach should be taken in interpreting distributional data, particularly when using electronic databases that are likely to comprise sepion and whole animal locality information. Sepion distributions alone may be indicative of drift outside the true range of a species, or may suggest wider distributions of cuttlefish populations than are currently understood based on available information. Sepion drift is postulated to be the more likely explanation.
Les mollusques, l’un des embranchements les plus diversifiés au sein de des métazoaires, sont reconnus pour leur capacité à élaborer une structure minéralisée : la coquille. Chez ces organismes, le processus de biominéralisation est génétiquement contrôlé et réalisé en domaine extracellulaire. Il fait intervenir une matrice organique calcifiante. Cette dernière, partiellement occluse au sein de la structure coquillière, est composée de protéines, de glycoprotéines, de lipides et de polysaccharides sécrétés par l’épithélium externe calcifiant du manteau. Cette matrice constitue la « boîte à outils moléculaires » pour la minéralisation de la coquille. Depuis sa découverte, elle a surtout fait l’objet d’études chez les bivalves et les gastéropodes, laissant dans l’ombre une autre classe de mollusques tout aussi importante, les céphalopodes.Les céphalopodes représentent une classe majeure de mollusque, dont une partie seulement des représentants actuels possède une coquille minéralisée, interne ou externe. L’histoire macroévolutive du groupe indique, depuis les formes ancestrales jusqu’aux formes les plus dérivées, une tendance générale à la réduction de la coquille, à son internalisation, voire à sa disparition complète. Si les relations de parentés entre les formes minéralisantes du clade semblent plutôt bien établies, les mécanismes moléculaires de formation coquillière restent encore très mal connus. Il est donc opportun de se demander si les représentants à coquille du clade possèdent des « boîtes à outils moléculaire » similaires pour fabriquer leurs coquilles ? Ce projet propose de répondre à cette question en explorant la biominéralisation coquillière de trois céphalopodes actuels, par l’utilisation d’approches biochimiques et protéomiques de la matrice coquillière, couplée à des analyses microstructurales.Le premier modèle étudié est la spirule Spirula spirula (Spirulidae), petit céphalopode pélagique dont le cycle de vie demeure encore très mal documenté. Les analyses de RMN à l’état solide et de FT-IR suggèrent que les polysaccharides constituent une part importante de la matrice organique coquillière. La protéomique, et les analyses in silico sur des modèles métazoaires hétérologues et sur le transcriptome récemment acquis de S. spirula révèlent de nombreux peptides ; la majeure partie d’entre eux ne correspondant à aucune protéine coquillière déjà identifiée au sein du clade des mollusques et/ou des céphalopodes. Ces observations suggèrent que la spirule possède un répertoire coquillier unique qui ne semble pas porter un signal phylogénétique.Le deuxième modèle est le céphalopode Argonauta hians (Argonautidae), à coquille externe non-homologue de celle des autres céphalopodes/mollusques puisque sécrétée ici par la première paire de bras dorsaux de l’animal. La matrice acido-soluble apparaît comme majoritaire et semble essentiellement protéique. La faible proportion de sucre est majoritairement constituée de glycosaminoglycanes sulfatés. La protéomique génère de nombreuses séquences peptidiques et identifie quelques protéines, non partagées par d’autres mollusques, ce qui suggère le recrutement d’outils moléculaires uniques chez l’argonaute pour la calcification de sa coquille.Le troisième modèle, qui fait l’objet d’une étude toujours en cours, est la seiche commune Sepia officinalis (Sepiidae). Les premiers résultats montrent la prépondérance de la matrice acido-insoluble, à signature FT-IR chitineuse. L’observation microscopique d’os de seiche et de préparations histologiques montre un contact étroit entre tissus organiques et minéralisés, et suggère une minéralisation bidirectionnelle, avec pour origine la couche interne prismatique du bouclier dorsal.Nos résultats sur les trois modèles sont discutés dans le cadre de l’évolution de la biominéralisation des céphalopodes.
The ontogenetic trajectories of septal spacing between succeeding chambers of two phylloceratid ammonoids, Hypophylloceras subramosum and Phyllopachyceras ezoense, from the Haboro and Kotanbetsu areas, north‐western Hokkaido, Japan, were analysed. The ontogenetic trajectories of septal spacing of H. subramosum demonstrate a general trend with large intraspecific variation: two cycles of increasing to decreasing spacing followed by almost constant spacing. The large intraspecific variation can be subdivided into three types, making this species polymorphic. The ontogenetic trajectories of septal spacing of P. ezoense also show intraspecific variation, but with a different trend: one cycle of increasing to decreasing spacing and an increasing trend after that. The intraspecific variation can be subdivided into two types, which suggests that this species is dimorphic, possibly sexually dimorphic. Dimorphism is supported by two observations: (1) the difference in the ontogenetic trajectories of septal spacing is only seen in the later ontogenetic stages; and (2) the two types co‐occur with comparable abundance throughout all stratigraphic horizons. Detailed analyses of ontogenetic trajectories of septal spacing may reveal polymorphism in other ammonoid clades.
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The complete ontogenetic development (protoconch to adult) of Creniceras renggeri (Oppel) is reconstructed by morphometrical studies of its shell (protoconch, ammonitella, whorl expansion rate, whorl height, siphuncle, septal spacing, crenulation and adult size). The embryonic stage is equated with eggdevelopment. Hatching occurred at about 568 μm (end of ammonitella) where probably only two septa were secreted. No larval stage is assumed. Post-embryonic development exhibits no drastic morphological changes. This is interpreted as a constant mode of life from hatching to sexual maturity.
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Morphological features of Nautilus from the Philippines, Fiji and Palau are compared from a taxonomic viewpoint on the basis of live-caught animals. In spite of their widely separated distributions, animals from the three populations share quite similar overall shell morphology, ontogenetic shell variation, and radular and jaw structures. Shell coloration and sculpture, and the shape of radular teeth, all of which have been used in previous taxonomic studies, are also markedly variable even in specimens of individual populations, and their ranges of variation overlap among the three samples. The three samples can be distinguished mainly by adult features, such as the dimensions of the shells and total number of septa, which are probably attributed to the difference in their pre-reproductive ages. Judging from these observations and available genetic data, it is suggested that the Palau population, previously distinguished as N. belauensis and the other two populations belong to the same, wide ranging species, N. pompilius, or otherwise they are closely related sibling species, N. belauensis and N. pompilius respectively.
Despite exhaustive investigation of present-day Nautilus, the phylogenetic relationships of the five or six recognized species within this genus remain unclear. Mitochondrial and nuclear DNA sequence data plus a suite of morphological characters are used to investigate phylogenetic relationships. Systematic analysis of the morphological variation fails to characterize described species as independent lineages. However, DNA sequence analysis indicates that there are three geographically distinct clades consisting of western Pacific, eastern Australian/Papua-New Guinean, and western Australian/Indonesian forms. The morphologically and genetically distinct species Nautilus scrobiculatus falls outside the three geographically recognized assemblages. Members of the genus Nautilus also exhibit low levels of sequence divergence. All these data suggest that Nautilus is currently undergoing diversification, which may have begun only several million years ago. These data also suggest that some of the morphological features used to define Nautilus species may simply represent fixed variations in isolated populations within the same species.
Some problems of cephalopod biodiversity are discussed. Many squid species are represented by 2–4 intraspecies groupings that may be wholly or partly sympatric, but differ in spawning season and size at maturity. They may be genetically distinct stock units, but their taxonomic status remains unresolved. Discovery of a biochemical or molecular key to distinguish between intra- and interspecific differences may help to solve the problem of subspecific taxa in cephalopods, as stated by G. L. Voss in 1977. Electrophoretic study of allozyme differentiation is a good method for clearing up relationships between taxa within a family, but this method cannot be used in situations when the concept of subgenus or subfamily is necessary. The problem of suprafamilial taxa needs urgent attention. However, restructuring only one family or group of families leaving others unrevised may lead to skewing the entire system. Examples are splitting the Enoploteuthidae into three families (as proposed by M. R. Clarke in 1988) and raising the rank of the Sepiidae and the Sepiolidae to ordinal, a proposal by P. Fioroni in 1981. In such cases the method of common level should be applied: subdivisions in a large taxon shall be separated by approximately similar characters. Many attempts to select natural groups of families, for example in the Oegopsida, failed primarily because they were based on analysis of a single organ or system of organs when study of other organs/systems may lead to different natural groupings. The use of molecular techniques in cephalopod phylogeny may be profitable, but initial attempts have led to results that are not easily interpretable. The evolution of Recent Cephalopoda has probably proceeded with such large variations in rates among different clades that it is impossible to construct a non-contradictory system based on any single organ or system. No single organ/system-of-organs nor single methodology currently exists that will solve every problem in taxonomy. An integrated approach, based on analysis of as many organs and different taxa as possible, is necessary to construct an accurate picture and not a mosaic of dispersed random pieces.