PALAIOS, 2013, v. 28, p. 373?385
Research Article
DOI: 10.2110/palo.2012.p12-082r
DO SPICULES IN SEDIMENTS REFLECT THE LIVING SPONGE COMMUNITY?
A TEST IN A CARIBBEAN SHALLOW-WATER LAGOON
MAGDALENA ?UKOWIAK,1* ANDRZEJ PISERA,1 and AARON O?DEA 2
1Institute of Paleobiology, Polish Academy of Sciences, ul. Twarda 51/55, 00-818 Warsaw, Poland, mlukowiak@twarda.pan.pl, apis@twarda.pan.pl;
2Smithsonian Tropical Research Institute, Center for Tropical Paleoecology and Archeology, PO Box 2072, Balboa, Republic of Panama, odeaa@si.edu
ABSTRACT
We compared sponge spicules occurring in surface sediments with those of
a living sponge community in a shallow-water reef environment of Bocas
del Toro archipelago, Panama, with the goal of evaluating how faithfully
spicular analysis reflects the living sponge community. Most megasclere
morphotypes present in living species are also found in sediment. On the
contrary, microscleres are underrepresented in the sediment samples.
Apart from spicules that belong to taxa that live at present in the area,
some morphotypes found in the sediment have no equivalent in the known
living community. Forty species of living sponges have been recognized in
the study area, but 9 (22%) do not produce mineral spicules and,
therefore, are not recorded in sediment. Sediment spicules suggest the
presence of 22 taxa, thus, loss of information in the process of fossilization
is average to considerable, with most living taxa identified also with
sediment spicules. Some morphotypes are abundant in sediment (i.e.,
ovoid spicules) even though the sponges bearing them are rare or absent,
thus suggesting either preferential preservation or recent disappearances
of taxa producing them. As transport did not play a significant role during
the fossilization process, spicular analysis?when all limitations and
constraints are considered?is a tenable tool in the reconstruction of
former sponge communities, but not of the share of various sponge species.
Spicular analysis may also help reveal the presence of cryptic and
excavating species that are often overlooked in traditional studies.
INTRODUCTION
Since the Precambrian, sponges have been important members of
coastal marine benthic ecosystems (D??az and Ru?tzler, 2001; Wulff,
2001; Gochfeld et al., 2007; Love et al., 2009). They provide structure
and shelter for a wide array of other organisms, are themselves
important food items, filter large quantities of water, and provide a
vital role in the stability of reefs by gluing fragments of reef rubble
together and, thus, providing a stable medium (5substrate) for the
settlement of other organisms (Wulff, 1984).
Understanding changes in sponge communities over time is,
therefore, of considerable interest. Sponges, however, rapidly disinte-
grate and rarely fossilize whole. Fortunately, their mineral skeletal
elements called spicules are often preserved in sediments after the death
and disintegration of the sponge organism, and spicules have characters
potentially enabling the composition of a living sponge community to
be reconstructed.
The general issues concerning fidelity of the fossil record have been
studied in numerous papers (e.g., Schopf, 1978; Olszewski and Kidwell,
2007; Lloyd et al., 2012), but they never concentrated on sponges. While
spicular analysis has successfully been used by paleontologists to
explore the composition of ancient sponge faunas and their associated
environments (e.g., Hinde and Holmes, 1892; Koltun, 1960; Reif, 1967;
Mostler, 1990; Wiedenmayer, 1994; Pisera, 1997; Pisera et al., 2006, and
references therein), the use of spicule assemblages as a proxy for
inferring changes in more recent sponge communities has so far
received little attention. Inoue (1984, 1985) used spicules in Holocene
sediments to reconstruct changes in sponge communities in Sagami Bay
(Japan), and freshwater sponge spicules preserved in Holocene lake
sediments have been analyzed by Harrison et al. (1979), Hall and
Herrmann (1980), Harrison (1988), Volkmer-Ribeiro and Turcq (1996),
Gaiser et al. (2004), Parolin et al. (2007, 2008), and Volkmer-Ribeiro
et al. (2007).
One major obstacle to the use of spicular analysis to reconstruct
ancient sponge communities is that the relationship between living
sponge communities and the assemblages of spicules in sediments has
yet to be fully explored. The purpose of this paper is to reveal how
faithfully sponge spicules in sediments reflect the living sponge
community in a shallow marine lagoon in the southwestern Caribbean.
Limitations and Concerns of Spicular Analysis
Although some sponges possess only organic skeletons, most have
skeletons composed of small, mineral elements made of opaline silica or
calcium carbonate called spicules. The morphology and arrangement of
spicules vary considerably and they are the basis for sponge
classification. Some sponges may have solid, fused, or articulated
skeletons that may be preserved intact, but most shallow-water tropical
sponges, which belong principally to the class Demospongiae, have
skeletons consisting of loose spicules that disintegrate rapidly following
death. Spicules, thus, become incorporated into sediment and often
form the main component of particulate silica on reefs (Ru?tzler and
Macintyre, 1978). As only those sponges that produce spicules have a
good chance of being preserved as fossils, an important component of
the living sponge community is lost in the process of fossilization.
Furthermore, the presence of spicules in sediment that are not observed
in nearby living sponges might arise in several ways, including
incomplete sampling of natural special patchiness of temporal
variability in living populations. The spicules may also reflect the
former presence of living sponges that are unlikely to reoccupy the area
owing to environmental change then.
The morphological types of sponge spicules, the number of spicule
morphotypes, and the quantity of spicules can vary greatly among and
within species. Although spicule types are taxonomically important
they are not all constrained to clades, with some morphotypes repeated
across families and even orders. Many sponge species produce several
spicule types, and little is known about the proportions of different
spicule types among species and within individuals of the same species.
The size of the sponge individual also influences the number of spicules.
These conditions complicate the use of spicule assemblages to
evaluate sponge diversity and species composition, and in fact make
strict quantitative analysis impossible. Loose, disassociated spicules in
surface sediment represent an unknown number of sponge taxa of
unknown biomass. Additionally, selective preservation or the removal
of spicules by postmortem transportation are likely biasing factors
considering the small sizes of microscleres (10?150 micrometers) and
* Corresponding author.
Published Online: July 2013
Copyright G 2013, SEPM (Society for Sedimentary Geology) 0883-1351/13/0028-0373/$3.00
natural waters that are undersaturated with respect to silica. Thus only
a qualitative approach to spicular analysis of sponge communities
seems reasonable (cf. Inoue, 1984).
MATERIAL AND METHODS
Setting
The Bocas del Toro archipelago, on the northwestern Caribbean
coast of Panama, consists of a series of mangrove- and reef-fringed
islands with lagoons having semirestricted exchange with the open
Caribbean Sea and receiving large quantities of freshwater from the
adjacent humid tropical mainland (Fig. 1). Of the 640 reef-associated
sponge species that have been recorded in the wider Caribbean (Wulff,
2001), 130 have been found in the Bocas del Toro region (Guzma?n and
Guevara, 1998, 1999; Collin et al., 2005; D??az, 2005; D??az et al., 2007;
Gochfeld et al., 2007). Of these, 106 have siliceous spicules.
The Casa Blanca reef (Fig. 1) lies in the Isla Co?lon (Colon Island)
within the Almirante Bay of the Archipelago and represents a diverse,
well-developed patch reef (e.g., Collin et al., 2005). The coral-sponge
community in this region has seen recent deterioration with reduced
coral cover and increasing macroalgae due to various factors, with the
latter including e.g., increasing concentrations of organic pollutants
(Gochfeld et al., 2007).
Approach
A polygon was demarcated (9u21935.90N/82u169380W, 9u21938.60N/
82u16940.90W, 9u21941.50N/82u16943.60W) within which three 5 3 5 m
quadrats were randomly located at the Casa Blanca sandy patch reef.
All three quadrats were at a depth of around 5?6 m. Surveys were made
by SCUBA in June 2011. Three quadrats were used in the survey to
reduce the influence of the patchiness in the sponge distribution. Within
each quadrat the living sponge fauna was surveyed (by visual inspection
and photography), living sponge samples of each recognized species
collected, and a surface (1-cm-deep) sediment sample recovered by
scoop to permit a comparison of living sponge and sediment spicule
assemblages. For the terminology of spicule morphotypes used in this
paper see Boury-Esnault and Ru?tzler (1997) and Hooper and Van Soest
(2002).
Living Sponge Survey
Within the three 25 m2 quadrats, every individual sponge observed
via SCUBA survey was identified to the lowest possible taxonomic level
based on morphology (Guzma?n and Guevara, 1998, 1999; Guzma?n,
2003; Collin et al., 2005; D??az, 2005; Gochfeld et al., 2007) and counted
following the approach to determine physiological independence as
proposed by Wulff (2001). Abundance of each sponge taxa within each
quadrat was estimated volumetrically and by the number of individual
sponges (herein termed biomass), and placed within five volumetric
classes arbitrarily chosen by the authors but with respect to observed
size distribution of sponge individuals in nature. Underwater photo-
graphs and voucher specimens were taken of some of the sponges for
subsequent identification in the laboratory.
In the laboratory, samples of living sponges were macerated using
two boiling cycles in concentrated household bleach, Clorox (5.95%
sodium hypochlorite) to remove organic material including sponge
fibers. Following this maceration, free spicules were recovered and
placed on microscope slides for identification. Various spicule
morphotypes were further studied using Scanning Electron Microscopy
(SEM) to complete identification at the Institute of Paleobiology,
Warsaw, Poland.
Spicules in Sediment Samples
In each quadrat a ,30 cm3 sample of surface sediment was collected
down to a depth of ,1 cm in the sediment from which 1 gram of dry
sediment was further analyzed. The three sediment samples were
subsequently dried, weighed, and macerated by treating them in 30%
hydrogen peroxide to remove small particles of organic material and to
help clean and separate sponge spicules, including microscleres up to
FIGURE 1?Schematic map of the study area.
374 ?UKOWIAK ET AL. PALAIOS
,150 micrometers in size (if possible) and megascleres that reach the size
of centimeters (Van Soest et al., 2012). Nevertheless, the division into
micro- and megascleres is not a strict one and there were some spicule
morphotypes assigned as microscleres (e.g., geodiid sterrasters) having
size within the megasclere range. Spicules were then handpicked from the
dried residues under binocular microscope. Morphological spicule types
were isolated, mounted on SEM stubs and identified using SEM. The
spicule assemblages are deposited in the Institute of Paleobiology, Polish
Academy of Sciences, Warsaw, under ZPAL Pf.24.
RESULTS
Living Sponge Diversity and Abundance
Forty living sponge species were recorded in the three quadrats in the
Casa Blanca lagoon environment, which represents approximately a
third of the 130 species that have ever been encountered alive across the
Bocas del Toro archipelago by previous workers (Guzma?n and
Guevara, 1998, 1999; Guzma?n, 2003; Collin et al., 2005; D??az, 2005;
Gochfeld et al., 2007; Tables 1?2). Thirty-one of these 40 species bear
spicules and thus have potential to be recorded in sediments.
Living Sponge Biomass
The three largest biomass contributors in the quadrats were Aplysina
fulva, Amphimedon compressa, and Niphates erecta. The above species
of sponges, whose volumes varied from 6060 cm3 to 7340 cm3, were
assigned to the fifth volumetric class and comprised 44% of all sponge
biomass. In the next most voluminous class there were 11 sponge
species assigned: Mycale (Mycale) laevis, Verongula rigida, Chondrilla
caribensis, Aplysina cauliformis, Cliona sp., Placospongia intermedia,
Ircinia strobilina, Iotrochota birotulata, Monanchora arbuscula, Xestos-
pongia muta, and Aiolochroia crassa which constituted ,35% of a total
sponge biomass. In this class the volume of sponges ranges from
910 cm3 to 2380 cm3. Seven smaller biomass constituents: Cliona
delitrix, Haliclona sp., Agelas sp., Neofibularia nolitangere, Ircinia sp.,
Spirastrella sp., and Neopetrosia rosariensis, were placed in the third
class of volume ranging from 270 cm3 to 570 cm3 (,6% of total
biomass). The next nine sponge species: Aplysina lacunosa, Mycale
(Arenochalina) laxissima, Plakortis angulospiculatus, Ircinia felix,
Mycale sp., Cliona varians, Clathria sp., Xestospongia sp., and
Cinachyrella alloclada, were placed in the second biomass class (,4%
of total biomass) in which volume varied from 160 cm3 to 200 cm3.
Finally, the biomass rapidly decreases (from 90 cm3 to 10 cm3) and the
remaining ten sponge species, including: Neopetrosia carbonaria,
Niphates caycedoi, Lyssodendoryx (Lissodendoryx) colombiensis, Ha-
lichondria sp., Oceanapia peltata, Neopetrosia proxima, Dragmacidon
reticulatum, Spongia sp., Tedania (Tedania) ignis, and Myrmekioderma
sp., had minor significance and were assigned to the first class and
constitute hardly 1% of total sponge biomass.
Apart from the sponges discussed above, we found also 85 small
individuals that belonged mostly to the first and second volumetric class, and
to which taxonomic assignment was not established mostly due to their very
small size. These individuals constituted about 10% of all sponge biomass.
Frequency of Spicule Types in Sediments
Spicules were dominated by monaxons, tetraxons, or polyactines that
belong to nonlithistid demosponges?the highly distinctive spicules of
lithistid and hexactinellid sponges were rare. Almost half of the spicules
(49.4%) are sterrasters and/or selenasters (Table 3). The next most
abundant morphological spicule types are oxeas and/or strongyles
(18.7%), spherical microscleres (anthasters, spherasters), which com-
prise 4.6%, and styles (1.7%). All other types constitute ,1% of the
total spicule assemblage (Table 3).
We also included in our analysis the category broken (this constituted
21.9%) because we know that they are mostly fragments of monaxial
spicules, and to a lesser degree, tetraxons, and thus they can be used in
further analysis.
DISCUSSION
Caveats: Taxonomic Assignment of Sediment Spicules
The ovoid microsclere spicules called sterrasters and selenasters that
dominate in the spicule assemblage (Figs. 2N?O) belong unambigu-
ously to the sponge families Geodiidae (order Astrophorida) or
Placospongiidae (order Hadromerida). More precise identification,
however, was not possible under a binocular microscope because of
their small size and similar morphology. The next most abundant types
of spicules?oxeas and/or strongyles and styles (Figs. 2A?E)?occur in
a very wide range of sponge families or even orders and, thus, cannot be
assigned to any living sponge taxa in the local fauna. Three different
morphotypes can nonetheless be distinguished within this group, and
these undoubtedly belong to different taxa.
The spherical spicules from the next most abundant morphogroup?
microsclere anthasters and spherasters (Figs. 2R, X)?may belong to
the family Geodiidae (order Astrophorida), Spirastrellidae, Placospon-
giidae (order Hadromerida), and/or Chondrillidae (order Chondro-
sida). However, in the case of such ovoid spicules they cannot be
differentiated more finely using a binocular microscope because of their
morphological similarity and small size. There were at least two
different types of spherasters present, however, and one type of
anthaster microscleres.
Rarer spicule types, such as tylostyles (Figs. 2K?M), are equally
difficult to assign to narrower taxonomic units because they may occur,
for example, in Spirastrellidae, Suberitidae, Clionaidae, Crambeidae,
and Microcionidae. At least three separate morphological types are
present, however, most probably belonging to different species.
The long-shafted triaenes (Fig. 2H), which may belong to the family
Geodiidae, were also observed in the sediment. There are two species of
living geodiids reported from this region?Geodia papyracea and Erylus
formosus?and the triaenes found in this study probably belong to E.
formosus based on their size. This conclusion is supported by the
presence of flat, discoidal microscleres called aspidasters (0.4% of
spicule assemblage; Figs. 2P?Q) that closely resemble those occurring
in living specimens of this species from Bocas del Toro (D??az, 2005),
although E. formosus was not found in our living surveys.
Besides triaenes of geodiid affinity, some other morphotypes were
noted, for example, the long and slender dichotriaenes (Fig. 2G) that
belong most probably to the family Pachastrellidae Carter, 1875.
Moreover, some triods and oxeas with split ends that occur in this
family were also found (Figs. 2C, W).
The rare sigma microscleres (Figs. 2S, Y) occur in a wide range of
sponge families making their assignment to specific taxa untenable. In
contrast, the calthrops (Fig. 2BB) can be more confidently assigned to
the family Pachastrellidae, and some of them, such as the very
characteristic triaenes with strongly branched clads as well as short-
shafted dichotriaenes (with branched clades) (Figs. 2T?V, AA),
undoubtedly belong to the pachastrellid genus Triptolemma Sollas,
1888 (order Astrophorida). They especially resemble those known from
Triptolemma endolithicum Van Soest, 2009, an encrusting species that
grows on lithistid demosponges of the genus Corallistes Schmidt, 1870.
This species has been reported from the Colombian coasts of South
America and the Southern Caribbean, but this is its first record in the
Bocas del Toro region. We did not find characteristic microscleres from
this species, but this may be because of their small size, dissolution, and
sampling bias.
We also observed rare but characteristic tuberculated acanthoxeas
(Fig. 2I) that clearly belong to Alectona Carter, 1879 (Alectonidae:
PALAIOS SPICULAR ANALYSIS 375
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si
gm
as
,t
ox
as
O
ce
an
ap
ia
no
do
sa
(G
eo
rg
e
&
W
ils
on
,1
91
9)
ox
ea
s
O
ce
an
ap
ia
ol
er
ac
ea
(S
ch
m
id
t,
18
70
)
st
ro
ng
yl
es
Si
ph
on
od
ic
ty
on
co
ra
lli
ph
ag
um
R
u?t
zl
er
,1
97
1
sh
or
t
sl
en
de
r,
cu
rv
ed
ox
ea
s,
10
0?
20
0
mm
Si
ph
on
od
ic
ty
on
cf
.b
re
vi
tu
bu
la
tu
m
Pa
ng
,1
97
3
ox
ea
s
C
al
yx
po
da
ty
pa
(d
e
L
au
be
nf
el
s,
19
34
)
ox
ea
s
i.
p.
,t
ox
as
C
ha
lin
id
ae
C
ha
lin
ul
a
m
ol
itb
a
(d
e
L
au
be
nf
el
s,
19
49
)
sh
or
t
ve
st
ia
lt
o
ci
ga
r-
sh
ap
ed
ox
ea
s,
2?
10
0
mm
C
ha
lin
ul
a
ze
ae
de
W
ee
rd
t,
20
00
ox
ea
s
H
al
ic
lo
na
sp
.
sm
oo
th
di
ac
tin
es
,o
xe
as
,o
r
st
ro
ng
yl
es
,
80
?2
50
mm
i.
p.
,s
ig
m
as
,t
ox
as
,r
ap
hi
de
s,
or
m
ic
ro
xe
as
H
al
ic
lo
na
(R
hi
zo
ni
er
a)
cu
ra
ca
oe
ns
is
(V
an
So
es
t,
19
80
)
ox
ea
s
H
al
ic
lo
na
(R
en
ie
ra
)
im
pl
ex
ifo
rm
is
(H
ec
ht
el
,1
96
5)
ox
ea
s
H
al
ic
lo
na
(R
.)
m
an
gl
ar
is
A
lc
ol
ad
o,
19
84
ox
ea
s
H
al
ic
lo
na
(R
.)
m
uc
ifi
br
os
a
de
W
ee
rd
t
et
al
.,
19
91
ox
ea
s
H
al
ic
lo
na
(R
.)
tu
bi
fe
ra
(G
eo
rg
e
&
W
ils
on
,1
91
9)
ox
ea
s
H
al
ic
lo
na
(H
al
ic
ho
cl
on
a)
va
ns
oe
st
i
de
W
ee
rd
t
et
al
.,
19
99
sl
ig
ht
ly
cu
rv
ed
ox
ea
s
H
al
ic
lo
na
(S
oe
st
el
la
)
tw
in
ca
ye
ns
is
de
W
ee
rd
t
et
al
.1
99
1
ox
ea
s
H
al
ic
lo
na
(S
.)
ve
rm
eu
le
ni
de
W
ee
rd
t,
20
00
sl
en
de
r
ox
ea
s
H
al
ic
lo
na
(S
.)
ca
er
ul
ea
(H
ec
ht
el
,
19
65
)
ox
ea
s
H
al
ic
lo
na
(S
.)
pi
sc
ad
er
ae
ns
is
(V
an
So
es
t,
19
80
)
ox
ea
s
H
al
ic
lo
na
n.
sp
.
ox
ea
s
N
ip
ha
tid
ae
A
m
ph
im
ed
on
co
m
pr
es
sa
D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
sl
ig
ht
ly
be
nt
ox
ea
s,
m
ul
tit
el
es
co
pe
d,
or
st
ro
ng
yl
ot
e
ap
ic
es
,1
00
?1
70
mm
A
m
ph
im
ed
on
vi
ri
di
s
D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
ox
ea
s
A
m
ph
im
ed
on
er
in
a
(d
e
L
au
be
nf
el
s,
19
36
)
ox
ea
s
i.
p.
,t
ox
as
N
ip
ha
te
s
ca
yc
ed
oi
(Z
ea
&
V
an
So
es
t,
19
86
)
ox
ea
s
st
ig
m
at
a,
p.
o.
a.
N
ip
ha
te
s
er
ec
ta
D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
ox
ea
s
376 ?UKOWIAK ET AL. PALAIOS
O
rd
er
F
am
ily
Sp
ec
ie
s
M
ac
ro
sc
le
re
sp
ic
ul
es
ty
pe
s
M
ic
ro
sc
le
re
sp
ic
ul
e
ty
pe
s
C
al
ly
sp
on
gi
da
e
C
al
ly
sp
on
gi
a
(C
la
do
ch
al
in
a)
va
gi
na
lis
(L
am
ar
ck
,
18
14
)
to
xa
s
C
al
ly
sp
on
gi
a
(C
.)
ar
m
ig
er
a
(D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
)
no
sp
ic
ul
es
C
al
ly
sp
on
gi
a
(C
al
ly
sp
on
gi
a)
pa
lli
da
H
ec
ht
el
,1
96
5
ox
ea
s
C
al
ly
sp
on
gi
a
(C
.)
fa
lla
x
D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
i.
p.
,t
ox
as
Sp
ir
op
ho
ri
da
T
et
ill
id
ae
C
in
ac
hy
re
lla
al
lo
cl
ad
a
(U
lic
zk
a,
19
29
)
lo
ng
pr
ot
ri
ae
ne
s,
am
ph
itr
ia
en
es
,
ox
ea
s,
fu
si
fo
rm
,s
ha
rp
ly
po
in
te
d
si
gm
as
pi
re
s
C
in
ac
hy
re
lla
ap
io
n
(U
lic
zk
a,
19
29
)
ox
ea
s,
st
yl
es
,a
m
ph
itr
ia
en
es
,
pr
ot
ri
ae
ne
s,
ty
lo
st
yl
es
si
gm
at
as
,r
ap
hi
de
s
H
ad
ro
m
er
id
a
Sp
ir
as
tr
el
lia
da
e
Sp
ir
as
tr
el
la
sp
.
ty
lo
st
yl
es
sp
ir
as
te
rs
in
tw
o
si
ze
ca
te
go
ri
es
Sp
ir
as
tr
el
la
co
cc
in
ea
(D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
)
ty
lo
st
yl
es
sp
ir
as
te
rs
Sp
ir
as
tr
el
la
ha
rt
m
an
i
B
ou
ry
-E
sn
au
lt
et
al
.,
19
99
ty
lo
st
yl
es
sp
ir
as
te
rs
Sp
ir
as
tr
el
la
m
ol
lis
V
er
ri
ll,
19
07
ty
lo
st
yl
es
sp
ir
as
te
rs
D
ip
la
st
re
lla
m
eg
as
te
lla
ta
H
ec
ht
el
,1
96
5
ty
lo
st
yl
es
an
th
as
te
rs
,o
xy
as
te
rs
Su
be
ri
tid
ae
T
er
pi
os
m
an
gl
ar
is
R
u?t
zl
er
&
Sm
ith
,1
99
3
ty
lo
st
yl
es
w
ith
fla
tt
en
ed
-lo
ba
te
or
lu
m
py
,w
ri
nk
le
d
st
yl
es
P
ro
su
be
ri
te
s
la
ug
hl
in
i
(D
??a
z
et
al
.,
19
87
)
ty
lo
st
yl
es
Su
be
ri
te
s
au
ra
nt
ia
cu
s
(D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
)
ty
lo
st
yl
es
in
tw
o
si
ze
ca
te
go
ri
es
i.
p.
,c
en
tr
ot
yl
ot
e
m
ic
ro
st
ro
ng
yl
es
C
lio
na
id
ae
C
lio
na
de
lit
ri
x
P
an
g,
19
73
sl
ig
ht
ly
cu
rv
ed
ty
lo
st
yl
es
sp
ir
as
te
rs
or
ra
ph
id
es
C
lio
na
va
ri
an
s
(D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
)
ty
lo
st
yl
es
an
th
os
ig
m
as
C
lio
na
ca
ri
bb
ae
a
C
ar
te
r,
18
82
ty
lo
st
yl
es
to
xa
s,
sp
ir
as
te
rs
C
lio
na
te
nu
is
Z
ea
&
W
ei
l,
20
03
ty
lo
st
yl
es
sp
ir
as
te
rs
C
lio
na
ap
ri
ca
Pa
ng
,1
97
3
ty
lo
st
yl
es
sp
ir
as
te
rs
C
lio
na
sp
.
ty
lo
st
yl
es
ra
ph
id
es
or
sp
ir
as
te
rs
Sp
he
ci
os
po
ng
ia
ve
sp
ar
iu
m
(L
am
ar
ck
,
18
15
)
ty
lo
st
yl
es
si
gm
as
pi
re
s,
sp
ir
as
te
rs
C
er
vi
co
rn
ia
cu
sp
id
ife
ra
(L
am
ar
ck
,
18
15
)
st
yl
es
,s
tr
on
gy
le
s,
ty
lo
st
yl
es
sp
ir
as
te
rs
T
et
hy
id
ae
T
et
hy
a
af
f.
se
yc
he
lle
ns
is
(W
ri
gh
t,
18
81
)
st
ro
ng
yl
ox
ea
s,
st
yl
es
,s
ph
er
as
te
rs
,o
r
ox
ys
ph
er
as
te
rs
ty
lo
st
er
s,
st
ro
ng
yl
as
te
rs
,
or
ox
ya
st
er
s
T
et
hy
a
ac
tin
ia
de
L
au
be
nf
el
s,
19
50
st
yl
es
sp
he
ra
st
er
s
T
he
on
el
lid
ae
D
is
co
de
rm
ia
di
ss
ol
ut
a
Sc
hm
id
t,
18
80
de
sm
as
:m
as
si
ve
te
tr
ac
lo
ne
s
w
ith
br
an
ch
ed
an
d
tu
be
rc
ul
at
ed
zy
go
m
es
an
d
sm
oo
th
ra
ys
,o
xe
as
sl
en
de
r
fu
si
fo
rm
an
d
sl
ig
ht
ly
cu
rv
ed
or
be
nt
ac
an
th
o-
xe
as
(s
pi
ne
s
ar
e
ho
ok
lik
e)
,m
as
si
ve
ac
an
th
or
ha
bd
s
Pl
ac
os
po
ng
iid
ae
P
la
co
sp
on
gi
a
in
te
rm
ed
ia
So
lla
s,
18
88
ty
lo
st
yl
es
of
tw
o
si
ze
cl
as
se
s
m
ic
ro
sc
le
re
s
se
le
na
st
er
s,
sp
ir
as
te
rs
,
sp
he
ra
st
er
s,
an
d
sp
he
ru
le
s
Po
ec
ilo
sc
le
ri
da
C
ra
m
be
id
ae
M
on
an
ch
or
a
ar
bu
sc
ul
a
(D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
)
ty
lo
st
yl
es
si
gm
at
os
e
ch
el
ae
,s
pi
ne
d
m
ic
ro
xe
as
M
ic
ro
ci
on
id
ae
C
la
th
ri
a
sp
.
ty
lo
st
yl
es
,s
ty
le
s,
ac
an
th
os
ty
le
s
is
oc
he
la
e
an
d
to
xa
s
w
ith
sm
oo
th
or
sp
in
ed
po
in
ts
C
la
th
ri
a
(T
ha
ly
si
as
)
ve
no
sa
(A
lc
ol
ad
o,
19
84
)
ty
lo
st
yl
e,
ac
an
th
ot
yl
os
ty
le
s,
sp
ir
as
te
rs
,t
ox
as
C
la
th
ri
a
(T
.)
sc
ho
en
us
(d
e
L
au
be
nf
el
s,
19
36
)
su
bt
yl
os
ty
le
s
is
oc
he
la
e,
to
xa
s
C
la
th
ri
a
(C
la
th
ri
a)
m
ic
ro
ch
el
a
(S
te
ph
en
s,
19
16
)
ac
an
th
os
ty
le
s,
su
bt
yl
os
ty
le
s
is
oc
he
la
e
C
la
th
ri
a
(M
ic
ro
ci
on
a)
ec
hi
na
ta
(A
lc
ol
ad
o,
19
84
)
st
yl
es
is
oc
he
la
e
C
la
th
ri
a
cf
.(
M
ic
ro
ci
on
a)
fe
rr
ea
(d
e
L
au
be
nf
el
s,
19
36
)
su
bt
yl
os
ty
le
s
is
oc
he
la
e,
to
xa
s
A
ca
rn
id
ae
A
ca
rn
us
ni
co
le
ae
V
an
So
es
t
et
al
.,
19
91
ty
lo
te
s
w
ith
sw
ol
le
n
m
ic
ro
sp
in
ed
ba
se
s,
st
yl
es
sm
oo
th
,
sl
ig
ht
ly
cu
rv
ed
at
ce
nt
er
,c
la
do
ty
lo
te
s
in
tw
o
si
ze
cl
as
se
s
ox
ho
rn
s,
th
in
de
ep
ly
cu
rv
ed
an
d
ac
co
la
da
to
xa
s,
pa
lm
at
e
is
oc
he
la
e
R
as
pa
ill
id
ae
E
ct
yo
pl
as
ia
fe
ro
x
(D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
)
st
yl
es
or
ac
an
th
os
ty
le
s,
rh
ab
do
st
yl
es
D
es
m
ac
el
lid
ae
N
eo
fib
ul
ar
ia
no
lit
an
ge
re
(D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
)
di
ac
tin
al
m
eg
as
cl
er
es
si
gm
as
,m
ic
ro
xe
as
,r
ap
hi
de
s,
co
m
m
at
a
B
ie
m
na
ca
ri
be
a
Pu
lit
ze
r-
F
in
al
i,
19
86
st
yl
es
,3
60
?7
00
mm
,a
br
up
tly
be
nt
ne
ar
th
e
ro
un
de
d
en
d
si
gm
as
,m
ic
ro
xe
as
,
co
m
m
at
a
an
d
ra
ph
id
es
M
yc
al
id
ae
M
yc
al
e
(M
yc
al
e)
la
ev
is
(C
ar
te
r,
18
82
)
st
yl
es
,s
ub
ty
lo
st
yl
es
,
ox
ea
s
an
is
o-
an
d
is
oc
he
la
e,
ro
se
tt
es
,s
ig
m
as
,t
ox
as
,
ra
ph
id
es
;m
ic
ro
ac
an
th
ox
ea
s
M
yc
al
e
(A
re
no
ch
al
in
a)
la
xi
ss
im
a
(D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
)
sp
in
ul
at
e,
pa
lm
at
e
an
ch
or
at
es
,b
ih
am
at
es
M
yc
al
e
(C
ar
m
ia
)
m
ic
ro
si
gm
at
os
a
A
rn
dt
,1
92
7
su
bt
yl
os
ty
le
s
an
is
oc
he
la
e,
si
gm
as
M
yc
al
e
(C
.)
m
ag
ni
rh
ap
hi
di
fe
ra
V
an
So
es
t,
19
84
ty
lo
st
yl
es
an
is
oc
he
la
e,
tr
ic
ho
dr
ag
m
at
as
M
yc
al
e
(A
eg
og
ro
pi
la
)
ca
rm
ig
ro
pi
la
H
aj
du
&
R
u?t
zl
er
,1
99
8
su
bt
yl
os
ty
le
s
an
is
oc
he
la
e,
to
xa
s
M
yc
al
e
(A
.)
ci
tr
in
a
H
aj
du
&
R
u?t
zl
er
,1
99
8
su
bt
yl
os
ty
le
s
an
is
oc
he
la
e,
si
gm
as
M
yc
al
e
(A
.)
an
gu
lo
sa
(D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
)
su
bt
yl
os
ty
le
s
M
yc
al
e
(A
.)
ar
nd
ti
V
an
So
es
t,
19
84
su
bt
yl
os
ty
le
s
si
gm
as
,r
os
et
es
M
yc
al
e
cf
.(
A
eg
og
ro
pi
la
)
am
er
ic
an
a
V
an
So
es
t,
19
84
su
bt
yl
os
ty
le
s
an
is
oc
he
la
e,
si
gm
as
M
yc
al
e
sp
.
(m
yc
al
o)
st
yl
es
,r
ar
el
y
re
pl
ac
ed
by
ox
ea
s
an
is
oc
he
la
e
T
A
B
L
E
1?
C
on
tin
ue
d.
PALAIOS SPICULAR ANALYSIS 377
O
rd
er
F
am
ily
Sp
ec
ie
s
M
ac
ro
sc
le
re
sp
ic
ul
es
ty
pe
s
M
ic
ro
sc
le
re
sp
ic
ul
e
ty
pe
s
C
oe
lo
sp
ha
er
id
ae
L
ys
so
de
nd
or
yx
(L
is
so
de
nd
or
yx
)
co
lo
m
bi
en
si
s
Z
ea
&
V
an
So
es
t,
19
86
st
ro
ng
yl
es
si
gm
as
,c
he
la
e
L
is
so
de
nd
or
yx
(L
.)
is
od
ic
ty
al
is
(C
ar
te
r,
18
82
)
st
yl
es
,t
yl
ot
es
si
gm
as
,c
he
la
e
T
ed
an
id
ae
T
ed
an
ia
(T
ed
an
ia
)
ig
ni
s
(D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
)
ty
lo
st
yl
es
,
st
yl
es
,w
ith
sm
oo
th
or
m
ic
ro
sp
in
ed
ba
se
s
ra
ph
id
es
D
es
m
ac
id
id
ae
D
es
m
ap
sa
m
m
a
an
ch
or
at
a
(C
ar
te
r,
18
82
)
sl
en
de
r
ox
ea
s
an
ch
or
at
e
is
oc
he
la
e
an
d
si
gm
as
Io
tr
oc
ho
tid
ae
Io
tr
oc
ho
ta
bi
ro
tu
la
ta
(H
ig
gi
n,
18
77
)
st
yl
es
or
ox
ea
s,
or
on
ly
st
ro
ng
yl
es
bi
ro
tu
la
s
C
ho
nd
ro
si
da
C
ho
nd
ri
lli
da
e
C
ho
nd
ri
lla
ca
ri
be
ns
is
R
u?t
zl
er
et
al
.,
20
07
sp
he
ra
st
er
s
C
ho
nd
ro
si
a
co
lle
ct
ri
x
(S
ch
m
id
t,
18
70
)
ox
ea
s
si
gm
as
,m
ic
ro
xe
as
,
co
m
m
at
a,
ra
ph
id
es
H
al
ic
ho
nd
ri
da
A
xi
ne
lli
da
e
D
ra
gm
ac
id
on
re
tic
ul
at
um
(R
id
le
y
&
D
en
dy
,1
88
6)
st
yl
es
an
d/
or
ox
ea
s,
w
ith
te
le
sc
op
ed
tip
s
i.
p.
,r
ap
hi
de
s
in
tig
ht
ly
pa
ck
ed
tr
ic
ho
dr
ag
m
at
a
P
til
oc
au
lis
w
al
pe
rs
i
(D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
)
st
yl
es
in
tw
o
si
ze
ca
te
go
ri
es
,o
cc
as
io
na
lly
ox
ea
s
or
an
is
ox
ea
s
H
al
ic
ho
nd
ri
id
ae
H
al
ic
ho
nd
ri
a
sp
.
ox
ea
s
H
al
ic
ho
nd
ri
a
(H
al
ic
ho
nd
ri
a)
lu
te
a
A
lc
ol
ad
o,
19
84
ox
ea
s
H
al
ic
ho
nd
ri
a
(H
.)
m
ag
ni
co
nu
lo
sa
H
ec
ht
el
,1
96
5
ox
ea
s
H
al
ic
ho
nd
ri
a
(H
.)
m
el
an
ad
oc
ia
de
L
au
be
nf
el
s,
19
36
ox
ea
s
D
es
m
an
th
id
ae
P
et
ro
m
ic
a
(C
ha
la
de
sm
a)
ci
oc
al
yp
to
id
es
(V
an
So
es
t
&
Z
ea
,1
98
6)
m
on
oc
re
pi
d
de
sm
as
,l
ar
ge
,u
su
al
ly
be
nt
,o
xe
as
,s
tr
on
gy
lo
xe
as
an
d
an
is
or
ha
bd
s
D
ic
ty
on
el
lid
ae
Sv
en
ze
a
ze
ai
(A
lv
ar
ez
,V
an
So
es
t
&
R
u?t
zl
er
,1
99
8)
sh
or
t
st
yl
es
,w
ith
ox
eo
te
en
di
ng
s,
ox
ea
s
Sc
op
al
in
a
ru
et
zl
er
i
(W
ie
de
nm
ay
er
,1
97
7)
st
yl
es
H
et
er
ox
yi
da
e
M
yr
m
ek
io
de
rm
a
sp
.
ox
ea
s
or
ac
an
th
ox
ea
s,
st
ro
ng
yl
es
,
st
yl
es
ra
ph
id
es
in
tr
ic
ho
dr
ag
m
at
a
H
om
os
cl
er
op
ho
ri
da
Pl
ak
in
id
ae
P
la
ko
rt
is
an
gu
lo
sp
ic
ul
at
us
(C
ar
te
r,
18
82
)
di
od
s
ce
nt
ro
ty
lo
te
or
w
ith
kn
ob
by
-k
no
tt
y
ce
nt
er
s,
tr
io
ds
,s
om
et
im
es
ca
lth
ro
ps
di
ac
tin
al
P
la
ko
rt
is
ha
lic
ho
nd
ri
oi
de
s
(W
ils
on
,1
90
2)
ox
ea
s
P
la
ki
na
st
re
lla
on
ko
de
s
U
lic
zk
a,
19
29
no
nl
op
ho
se
di
od
s,
tr
io
ds
,a
nd
/o
r
ca
lth
ro
ps
,u
su
al
ly
in
3
si
ze
cl
as
se
s
O
sc
ar
el
la
sp
.
no
sp
ic
ul
es
A
ge
la
si
da
A
ge
la
si
da
e
A
ge
la
s
sp
.
ve
rt
ic
ill
at
e
ac
an
th
ox
ea
s
an
d
ac
an
th
os
ty
le
s
A
ge
la
s
di
sp
ar
D
uc
ha
ss
ai
ng
&
M
ic
he
lo
tt
i,
18
64
ve
rt
ic
ill
at
e
ac
an
to
xe
as
an
d
ac
an
th
os
ty
le
s
A
ge
la
s
cl
at
hr
od
es
(S
ch
m
id
t,
18
70
)
ve
rt
ic
ill
at
e
ac
an
to
xe
as
an
d
ac
an
th
os
ty
le
s
A
ge
la
s
co
ni
fe
ra
(S
ch
m
id
t,
18
70
)
ve
rt
ic
ill
at
e
ac
an
to
xe
as
an
d
ac
an
th
os
ty
le
s
ra
ph
id
es
A
st
ro
ph
or
id
a
G
eo
di
id
ae
G
eo
di
a
pa
py
ra
ce
a
H
ec
ht
el
,1
96
5
ox
ea
s
an
d
pl
ag
io
-,
or
th
ot
ri
ae
ne
s
st
er
ra
st
er
s,
ox
ya
st
er
s
E
ry
lu
s
fo
rm
os
us
So
lla
s,
18
86
tr
ia
en
es
(p
la
gi
ot
ri
ae
ne
s,
or
th
ot
ri
ae
ne
s)
an
d
ox
ea
s
m
ic
ro
rh
ab
ds
an
d
as
pi
da
st
er
s
H
al
is
ac
ri
da
H
al
is
ar
ci
da
e
H
al
is
ar
ca
ca
er
ul
ea
V
ac
el
et
&
D
on
ad
ey
,1
98
7
no
sp
ic
ul
es
H
al
is
ar
ca
sp
.
no
sp
ic
ul
es
D
en
dr
oc
er
at
id
a
D
ar
w
in
el
lid
ae
A
pl
ys
ill
a
gl
ac
ia
lis
(M
er
ej
ko
w
sk
i,
18
78
)
no
sp
ic
ul
es
C
he
llo
na
pl
ys
ill
a
er
ec
ta
T
su
rn
am
al
,
19
67
no
sp
ic
ul
es
C
al
ca
re
a
C
la
th
ri
na
pr
im
or
di
al
is
(H
ae
ck
el
,1
87
2)
no
sp
ic
ul
es
T
A
B
L
E
1?
C
on
tin
ue
d.
378 ?UKOWIAK ET AL. PALAIOS
Hadromerida). They closely resemble those of Alectona wallichii Carter,
1874 (compare with Vacelet, 1999, and Pisera et al., 2006). This species
was not previously reported in Bocas del Toro, which may be because
alectonids are excavating sponges occupying chambers and cavities and
can easily be overlooked (Ru?tzler, 2002). Thus far, A. wallichii has been
recorded only from Hawaii, Madagascar, and southern African coasts
(Vacelet, 1999; Ru?tzler, 2002), and this is the first occurrence in the
Caribbean. Interestingly, A. wallichii was also recognized in the fossil
record of Miocene of Portugal (Pisera et al., 2006) and Eocene of
Australia (?ukowiak, 2013).
The characteristic amphitriaene spicules that belong to Samus
anonymus Gray, 1867 (Fig. 2CC) of the monogeneric family Samidae
Sollas, 1888 were relatively common. This is the first record of this
species in the Bocas del Toro archipelago. S. anonymus is globally
distributed and was earlier reported from northeastern Brazil,
Australia, Sri Lanka, Singapore, Florida, Palau Islands, West Africa,
Mediterranean, Colombia, and Curac?ao (Van Soest et al., 2011).
Samids are shallow-water excavating sponges making small holes and
corridors in corals and coralline algae (Van Soest and Hooper, 2002)
and, thus, because of their cryptic mode of life, may easily have been
overlooked in previous surveys in Bocas.
Monaxons are not usually characteristic enough to be assigned to a
particular taxon, but there are some exceptions such as the oxeas with
tubercles on their tips that were observed in our sediment samples
(Fig. 2F). They probably belong to the halichondrid Myrmekioderma.
The species Myrmekioderma rea de Laubenfels, 1934 is known from
TABLE 2?Species, spicule types and biomass of the investigated sponges. In the volumetric classes, column I, II, III, IV, or V denotes volumetric class (I 5 volume ,21 cm3,
II 5 volume 21?140 cm3, III 5 volume 141?240 cm3, IV 5 volume 241?560 cm3, V 5 volume .560 cm3); number of sponges of each species\average volume of individuals in
each class; the share of biomass of each species (given in percents) of a total investigated sponge biomass.
Species Spicule types
Volumetric classes
I II III IV V % of all biomass
Amphimedon compressa Slightly bent oxeas, multitelescoped or strongylote apices 11\110 50\4000 17\3230 - - 15,80
Aplysina fulva No spicules 28\280 74\5920 4\760 - - 14,98
Niphates erecta Oxeas 9\90 39\3120 15\2850 - - 13,04
Mycale (Mycale) laevis Styles, subtylostyles, oxeas, aniso- and isochelae, microsclere
rosettes, sigmas, toxas, raphides; microacanthoxeas
27\270 24\1920 1\190 - - 5,12
Verongula rigida No spicules 4\40 13\1040 2\380 - - 4,48
Chondrilla nucula Spherasters 5\50 19\1520 1\190 - - 3,79
Aplysina cauliformis No spicules 3\30 7\560 5\950 - - 3,31
Cliona sp. Tylostyles, raphides, or spirasters 32\320 14\1120 - - - 3.10
Placospongia intermedia Tylostyles of two size classes, microscleres selenasters,
spirasters, spherasters, spherules
5\50 12\960 2\380 - - 2.99
Ircinia strobilina No spicules 1\10 4\320 5\950 - - 2.76
Iotrochota birotulata Styles or oxeas, or only strongyles, birotulas 1\10 3\240 5\950 - - 2.58
Monanchora arbuscula Tylostyles, sigmatose chelae, spined microxeas 6\60 6\480 3\570 - - 2.39
Xestospongia muta Oxeas, sometimes styles, strongyles - - - 2\1040 - 2.24
Aiolocroia crassa No spicules 2\20 4\320 3\570 - - 1.96
Cliona delitrix Slightly curved tylostyles, spiraster microscleres, or raphides 3\30 2\160 2\380 - - 1.23
Haliclona sp. Smooth diactines, oxeas or strongyles, 80?250 mm, i.p.,
microsclere sigmas, toxas, raphides, or oxeas
24\240 4\320 - - - 1.21
Agelas sp. Verticillate acanthoxeas and acanthostyles 2\20 6\480 - - - 1.08
Neofibularia nolitangere Diactinal megascleres, microsclere sigmas, microxeas,
raphides, commata
- 3\240 1\190 - - 0.93
Ircinia sp. No spicules - 4\320 - - - 0.69
Spirastrella sp. Tylostyles, microsclere spirasters in two size categories 4\40 1\80 1\190 - - 0.67
Neopetrosia rosariensis Oxeas, strongyles, styles - 1\80 1\190 - - 0.58
Aplysina lacunosa No spicules 1\10 0 1\190 - - 0.43
Mycale (Arenochalina) laxissima Spinulate, palmate anchorates, bihamates - - 1\190 - - 0.41
Plakortis angulospiculatus Diods, triods, sometimes calthrops, diactinal microscleres 3\30 2\160 - - - 0.41
Ircinia felix No spicules - - 1\190 - - 0.41
Mycale sp. Mycalostyles, rarely replaced by oxeas, anisochelae
microscleres
2\20 2\160 - - - 0.39
Cliona varians Tylostyles, anthosigma microscleres 1\10 2\160 - - - 0.37
Clathria sp. Tylostyles, styles, acanthostyles, microsclere isochelae, and
toxas
1\10 2\160 - - - 0.37
Xestospongia sp. Oxeas, sometimes styles, strongyles - 2\160 - - - 0.34
Cinachyrella alloclada Long protriaenes, amphitriaenes, oxeas, fusiform, sharply
pointed, sigmaspire microscleres
- 2\160 - - - 0.34
Neopetrosia carbonaria Oxeas, styles, strongyles 1\10 1\80 - - - 0.19
Niphates caycedoi Oxeas, p.o.a. sigmata microscleres - 1\80 - - - 0.17
Lyssodendoryx (L.) colombiensis Strongyles, microsclere sigmas, chelae - 1\80 - - - 0.17
Halichondria sp. Oxeas - 1\80 - - - 0.17
Oceanapia peltata Oxeas, microsclere sigmas, toxas 6\60 - - - - 0.13
Neopetrosia proxima Oxeas, stylote, strongylote forms 1\10 - - - - 0.02
Dragmacidon reticulatum Styles and/or oxeas, with telescoped tips, i.p., raphides
microscleres
1\10 - - - - 0.02
Spongia sp. No spicules 1\10 - - - - 0.02
Tedania (Tedania) ignis Tylostyles, styles, with smooth or microspined bases, raphide
microscleres
1\10 - - - - 0.02
Myrmekioderma Oxeas or acanthoxeas, strongyles, styles, raphide microscleres 1\10 - - - - 0.02
Unrecognized 48\480 37\2960 8\1520 2\1040 - 10.68
PALAIOS SPICULAR ANALYSIS 379
eastern and southern Caribbean (Puerto Rico, Venezuela, Bahamas,
Barbados; Van Soest et al., 2011) but is here noted for the first time
from Bocas del Toro region. Usually these sponges inhabit relatively
deep water (46?83 m) (D??az et al., 1993), in contrast to our finding them
from a shallow water of 6 m depth. Such taxonomic assignment of
subfossil spicules is supported by the fact that we also found a living
specimen of this species during our study.
The small, pointed acanthoxeas (Fig. 2J) belong to the tetillid genus
Acanthotetilla Burton, 1959, which has not previously been reported
from this area, although Acanthotetilla gorgonosclera Van Soest, 1977,
was reported from Barbados (compare with Van Soest and Ru?tzler,
2002). The acanthoxeas found in the sediment are almost identical with
those of A. gorgonosclera (see Van Soest, 1977).
The only lithistid demosponge spicules found were discotriaenes
(0.05%) (Fig. 2DD), which were likely from the theonellid genus
Discodermia du Bocage, 1869. They may belong to Discodermia
dissoluta Schmidt, 1880, which is reported from Caribbean shallow
waters (Van Soest et al., 2011).
Two surprising occurrences in our sediment samples were the toothed
anchorate basalia (0.01%) (Fig. 2Z) of hexactinellid sponges, which are
very similar to those occurring in the family Pheronematidae Gray,
1870 (Hexactinellida: Amphidiscophora). These spicules may belong to
Pheronema annae Leidy, 1868, because these sponges were reported
from the Caribbean and Northern Gulf of Mexico. These hexactinel-
lids, however, inhabit rather deep waters from around 90 to 5000 m
(Tabachnick and Menshenina, 2002). Their occurrence in the water few
meters deep may reflect shoreward postmortem transportation of
spicules via e.g., sponge grazers or onshore storm transport of entire
sponges. Hurricanes do not affect the Bocas region.
We have found 95 taxonomically undetermined individuals that are
assigned mostly to the first and second classes (except 8 individuals
assigned to third class and 2 of fourth class). These individuals may
belong to species other than those mentioned here, e.g., the encrusting
taxa whose spicules have been observed in the sediment, but are not
recognized in the living sponge community.
Thus, based on the spicule morphotypes found in sediment we can
distinguish ,22 different sponge taxa including Samus anonymus,
Placospongia intermedia, Triptolemma endolithicum, Alectona wallichii,
Pheronema annae, Discodermia dissoluta, and probably Myrmekioderma
sp., Acanthotetilla gorgonosclera and Cinachyra sp.. Additionally, at
least two species of geodiids were recognized (probably Erylus formosus
and Geodia papyracea). Other morphotypes of spicules indicate the
presence of Chondrilla caribensis (and maybe one other taxon with
spherical spicules), as well as one with anthasters (probably Diplastrella
megastellata). The presence of three different morphotypes of both
oxeas and tylostyles suggests the presence of at least six further sponge
species. The presence of strongyles and styles and some spicules of the
sponges belonging to the family Pachastrellidae were also observed.
Relationship between Living Sponges and Sediment Macroscleres and
Ovoid Microscleres
Considering the calculated biomass of living sponges in the study
area, oxeas and/or strongyles and styles are the types of spicules
expected to be most abundant in the sediment because of the
dominance of living biomass by Amphimedon compressa, Niphates
erecta, and Mycale (Mycale) laevis. Such spicules comprise only ,20%
of all nonfragmental spicules found in the sediment, however. This
discrepancy may be due to the fragility of these relatively long, thin, and
slender spicules, resulting in frequent breakage and, therefore, loss from
our study. Indeed, most spicules in broken condition (Table 3) are
probably fragments of monaxial spicules such as oxeas and/or
strongyles, styles, and to a lesser degree, tetraxons. If those fragments
were added to the clearly identifiable spicules of this type, then they
would constitute 42% of the total sedimentary assemblage. One would
then conclude that the most common sponges in the living assemblage
are among the commonest spicule types in the sampled quadrats.
Even with this possible correction, however, the most abundant
spicule morphotypes found in the sediment were sterraster and
selenaster microscleres (49% of assemblage). The abundance of these
spicule types does not correspond with the biomass of living sponges
possessing these types, namely Geodia papyracea and Placospongia
intermedia, which, although documented from the Bocas del Toro
region by D??az (2005) and Gochfeld et al. (2007), were either not found
(Geodia) or moderately frequent (Placospongia, Table 2). The unex-
pected predominance of these ovoid-shaped spicules in sediment might
have several causes, including lower rates of postmortem transportation
out of the local habitat (e.g., Ru?tzler and Macintyre, 1978), lower rates
of postmortem destruction (e.g., owing to lower surface area to volume
ratios than elongate spicules), and/or preferential removal of other
spicule types by winnowing. This supposition of postmortem bias is
supported by the fact that, in the studied area some additional spicule
types that characterize these two sponge species are very rare from
sediment (triaenes constitute only 0.4% of all spicules and tylostyles
0.7%). The abundance of those spicule types is thus more comparable
to the relative abundance of these two genera among living sponges.
Notably, as another factor in the overrepresentation of selenasters or
sterrasters in sediment, both Geodia and Placospongia are characterized
by extremely heavy (thick and dense) ectosomal armor formed by these
spicules, respectively. This density of spicules exceeds that known in any
other here-considered sponges. Thus, interpretation of the frequency of
these spicule morphotypes in the sediment must be done with utmost
caution.
A similar situation arises with aspidaster microscleres from the
geodiid Erylus formosus. They were present in sediments but very rare
(0.4%). Although the genus Erylus was not found during our study of
living sponges, it was observed by other authors (e.g., Collin et al.,
2005) in the study area. The most parsimonious explanation of our
findings is that sponges bearing such spicules have been present in the
past in the study area, and have only recently disappeared.
Tylostyles should be the third most abundant in the sediment,
according to the biomass of living sponges, and so their frequency
reflects more or less their biomass. Just like in the previous case, the
frequency of spherasters belonging to Chondrilla sp. seems to
correspond with the number of spherical spicules placed in the category
anthasters and/or spherasters (the third most frequent). One must
remember, however, that in this category are placed also spherical
anthasters. These spicule types belong most probably to Diplastrella
TABLE 3?Total numbers of spicule morphotypes found in the sediment, their
taxonomic attribution if possible (in parenthesis), and their proportional
abundance (%).
Spicule morphotype Number of spicules %
Sterrasters (Geodiidae) or selenasters
(Placospongiidae) 9685 49.38
Oxeas or strongyles 3665 18.7
Anthasters or spherasters 903 4.6
Styles 331 1.69
Calthrops 196 1
Tylostyles 127 0.65
Acanthoxeas (Alectona) 87 0.44
Aspidasters (Erylus) 82 0.42
Amphitriaenes (Samus) 82 0.42
Triaenes 70 0.36
Branched triaenes (Triptolemma) 65 0.33
Triods 27 0.14
Discotriaenes 9 0.05
Anchorate basalia (hexactinellid) 2 0.01
Sigma microscleres 2 0.01
Sigmaspire microscleres 1 0.005
Broken (mostly monaxonic styles and oxeas) 4279 21.82
380 ?UKOWIAK ET AL. PALAIOS
FIGURE 2?Spicule morphotypes present in sediments. A) Strongyle. B) Style. C) Oxea type I. D) Oxea type II. E) Oxea type III. F) Acanthoxea. G) Triaene type I. H) Triaene
type II. I) Acanthoxea. J) Acanthoxea microclere. K) Tylostyle type I. L) Tylostyle type II. M) Tylostyle type III. N) Selenaster. O) Sterraster. P) Aspidaster type I. Q)
Aspidaster type II. R) Spheraster. S) Sigma. T) Short-shafted triaene type I. U) Short-shafted triaene type II. V) Short-shafted triaene type III. W) Triod. X) Anthaster. Y)
Sigmaspire. Z) Anchorate basalium. AA) Mesodichotriaene. BB) Calthrop. CC) Amphitriaene. DD) Discotriaene. Coll. number ZPAL Pf.24.
PALAIOS SPICULAR ANALYSIS 381
megastellata, which is known from Bocas del Toro but was not found
during the present study. The other problem is that some tunicate
ascidians have spicules with similar morphology and sizes (distinguish-
able only under scanning electron microscope; see for example
?ukowiak, 2012) and may also be placed mistakenly in this category,
further complicating the picture.
Spiraster microscleres that occur only in sponges of the third and
fourth volumetric group do not reflect the situation in sediment because
no spiraster spicules were found in the sediment during this study. The
less frequent according to biomass are triods, calthrops, and triaenes
that occurred only in the fourth category.
In the case of the amphitriaenes of Samus, acanthoxeas of Alectona,
and triaenes of Triptolemma, the fact that these taxa were not
recognized among living sponges can be explained by their cryptic
and/or encrusting nature. The fact that lithistid discotriaenes were
found in the sediment and not among living sponges may be associated
with the general rarity of lithistids in shallow water. The presence of
deep-water hexactinellid spicules in the sample is rather surprising, but
can be explained perhaps by storm detachment and transport of living
sponges from deeper water.
The frequency of occurrence of microscleres in sediment seems to be
a separate case. Here, we treated ovoid and spherical spicules separately
FIGURE 3?Spicule morphotypes present in living sponges. A) Strongyle. B) Style type I. C) Style type II. D) Oxea type I. E) Oxea type II. F) Oxea type III. G) Acantoxea.
H) Diaene. I) Triaene. J) Raphide. K) Microxea. L) Tylostyle type I. M) Tylostyle type II. N) Tylostyle type III. O) Selenaster. P) Spiraster microsclere. Q) Spheraster.
R) Sigmaspire. S) Anisochelae. T) Isochelae. U) Birotula. V) Sigma.
382 ?UKOWIAK ET AL. PALAIOS
because of their suspected different behavior during the postmortem
transport and deposition and their much larger size than typical
microscleres. The rare appearance of microscleres (only one sigma and
sigmaspire) may be the result of selective dissolution of this type of
spicules because of their relatively high surface/volume ratio. Caribbean
surface seawater down to 50 m is characterized by a pH of ,7.95
(Doney, 2006), which is sufficiently high for dissolution of amorphous
sponge silica. The low frequency of microscleres may also be an effect
of preferential winnowing and transport, due to their very small size;
however, the transport seems not to play a significant role. Their small
size may also cause their loss during maceration and washing of
sediment samples, or their being overlooked even under the binocular
microscope.
CONCLUSIONS
We have identified 23 different morphological types of spicules
occurring in the living specimens that were found in the studied area,
and 15 of them were also identified in the sediment samples (see
Figs. 2?3). There are 4 morphotypes, however, that occur in the
sediment but have no equivalents in living sponges recognized during
the present study: euasters, sterrasters, discotriaenes, and anthasters.
The sponges to which these types belong have been reported from the
Bocas del Toro region by other authors, and thus their absence alive in
our quadrats may follow only from spatial patchiness in sponge
distribution. We have also found other spicule morphotypes?
anchorate basalia, amphitriaenes, small acanthoxeas, and various
plakinastrellid triaenes?that have no equivalents at all in the sponge
fauna of the studied area, either encountered by us or by previous
workers in the Bocas del Toro region.
The observed differences between the spicules generated by living
sponges and those encountered in sediments may be explained by
several biological and sedimentological factors that are not mutually
exclusive. These include live-dead differences arising from small size,
which promotes (1) selective removal in the face of dissolution,
winnowing, and transport; (2) sampling bias in the sediment samples;
(3) incomplete sampling of the living owing to patchiness in sponge
communities or short-distance transport of sponges during storms; and
also (4) recent disappearance of taxa in the living fauna bearing these
spicule types, either under natural or anthropogenic forces.
Our investigation demonstrates that the frequency of various
macrospicule types in the sediment reflects well the frequency of living
sponges having a particular type of spicules. On the other hand, the
frequency of microscleres in sediment is much lower compared to their
frequency in the living sponge communities. One can speculate that
their scarcity or absence is caused by their small size, which promotes
their dissolution and/or winnowing, or by the sampling bias.
1. Forty species of living sponges from 28 genera were observed in
surveys of three 5 3 5 m quadrats on Casa Blanca reef in Bocas del
Toro. Of these, nine (22.5%) do not produce mineral spicules and are
thus lost in the process of fossilization.
2. The most common spicule types in living sponges, according to
frequency, are oxeas, strongyles, and styles. The most common spicule
types in the sediment are small ovoid spicules (sterrasters and selenasters),
oxeas, anthasters and/or spherasters, and styles. Less frequent are calthrops
and tylostyles. This demonstrates that the frequency of various macro-
spicule types in the sediment reflects well the frequency of living sponges
having a particular type of spicules. On the other hand, the frequency of
microscleres in sediment is much lower (or they are even totally absent)
compared to their frequency in the living sponge communities. One can
speculate that it is caused by their small size that promotes their dissolution
and/or preferential removal or the sampling bias.
3. Apart from spicules that belong to taxa living at present in the
area, we have found also other types of spicules characteristic for
sponges not found at all living at present in the area. Most probably
this may be caused by a local extinction of the taxa producing this type
of spicules, or the effect of patchiness in distribution of the sponges.
Only four species have no equivalents in the living community but they
may be hidden among 95 taxonomically undetermined small individ-
uals. Spicular analysis is also a useful tool for revealing the presence of
cryptic and excavating sponges that are otherwise difficult to spot, and
thus overlooked in traditional faunistic studies.
4. Generally, most morphological types of megasclere found in living
sponges had been recognized in the sediment, indicating that despite of
the loss of information caused by nonpreservation of the species
without mineral spicules, spicular analysis, when all limitations are
considered, is a good tool in reconstruction of the taxonomic
composition of former (subfossil) sponge assemblages, but not the
frequency of various sponge species. Thus, it can be used to estimate
diversity changes in sponge communities through time.
ACKNOWLEDGMENTS
This paper is a part of the Ph.D. project of M? and was possible
thanks to support of the Institute of Paleobiology, Polish Academy of
Sciences, a Short Term Fellowship from the Smithsonian Tropical
Research Institute, and a PalSIRP Sepkoski Grant to M?. The Institute
of Paleobiology also funded AP. The National System of Investigators
(SNI) of the National Research of the National Secretariat for Science,
Technology and Innovation of Panama (SENACYT) funded AO.
Recursos Minerales kindly gave permission to collect sediments. We
would like to thank Gabriel Jacome, Plinio Gondola, Felix Rodriguez,
Alexa Fredston-Hermann, Brigida de Gracia, and all the team at the
Bocas Research Station for their support. Special thanks are to
Alexander Wolfe, University of Alberta (Canada), for linguistic
improvements of the manuscript. The authors appreciate also
comments and helpful suggestions by Susan Kidwell and the
anonymous reviewer.
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ACCEPTED MAY 14, 2013
PALAIOS SPICULAR ANALYSIS 385