Biodata of Domenico D’Alelio, Maria Teresa Cante, Giovanni Fulvio Russo, Cecilia
Totti, and Mario De Stefano, authors of “Epizoic Diatoms on Gastropod Shells:
When Substrate Complexity Selects for Microcommunity Complexity”
Dr. Domenico D’Alelio is currently a post-doc researcher at the IASMA Research
and Innovation Centre, Fondazione Edmund Mach, S. Michele all’Adige, Trento,
Italy, in the Environment and Natural Resources Area and in the frame of the
programme of Biocomplexity and Ecosystem Dynamics. He was a Research
Associate at the Department of Environmental Science of the Second University
of Naples, Italy, from April 2008 to April 2009. He obtained his Ph.D. from the
Stazione Zoologica “A. Dohrn” of Naples and Messina University, Italy, in 2008.
Domenico D’Alelio’s scientific interests include mainly ecology and evolution of
diatoms and cyanobacteria in marine and freshwater environments.
E-mail: domenico.dalelio@iasma.it
Ms. Maria Teresa Cante is currently a Ph.D. student at the Department of
Environmental Science of the Second University of Naples, Italy. She obtained her
Master Degree from the Parthenope University of Naples, Italy, in 2007. Maria
Teresa Cante’s scientific interests include taxonomy, ecology, and biogeography of
tropical and Mediterranean diatom communities.
E-mail: cantemariateresa@yahoo.it
Maria Teresa Cante
Domenico D’Alelio
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J. Seckbach and Z. Dubinsky (eds.), All Flesh Is Grass,
Cellular Origin, Life in Extreme Habitats and Astrobiology 16, 345–364
DOI 10.1007/978-90-481-9316-5_16, © Springer Science+Business Media B.V. 2011
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Prof. Giovanni Fulvio Russo is currently a Full-time Professor in Ecology at the
Faculty of Sciences and Technologies of the University of Naples “Parthenope,”
where he also teaches Benthic Ecology, Biological Oceanography, and Conservation
of Nature. He obtained his degree in Biological Sciences with full marks at the
University of Naples “Federico II” in 1979. In 1981, he was a post-doctoral fellow
of the National Research Council at the Institute of Zoology of the University of
Vienna. From 1982 to 1998, he was a researcher at the Stazione Zoologica “Anton
Dohrn” of Naples. From 1992 to 1998, he was a professor under contract of Marine
Biology at the University of Naples “Federico II”. From 1998 to 2001, he was an
associated Professor of Marine Ecology at the University of Catania. From 2002 till
date, he is a member of the panel of supervisors of the Ph.D. theses in Environmental
Sciences: Marine Environment and Resources of the University of Messina.
E-mail: giovanni.russo@uniparthenope.it
Dr. Cecilia Totti is currently a Senior Researcher at the Department of Marine
Sciences, Polytechnical University of the Marche (Italy). She obtained her Ph.D.
in 1999 from the Polytechnical University of the Marche. Cecilia Totti research
activity is focused on ecology and taxonomy of marine microalgae: phytoplankton
long time series, mucilage aggregates, harmful microalgae, and microphytobenthic
communities (epipelic, epilithic, epiphytic, and epizoic), particularly deepening
the relationships occurring between microalgae and marine invertebrates.
E-mail: c.totti@unicpm
Giovanni Fulvio Russo
Cecilia Totti
EPIZOIC DIATOMS ON GASTROPOD SHELLS
347
Prof. Mario De Stefano is currently a Researcher at the Department of
Environmental Science of the Second University of Naples, Italy. He obtained his
Ph.D. from the Stazione Zoologica “A. Dohrn” of Naples and Messina University,
Italy, in 2002, and continued his studies and researches at Stazione Zoologica until
2004 and from 2005, at the Second University of Naples. Mario De Stefano is
involved in basic researches focused on the life history of Mediterranean and tropical diatom communities, on extremophile organisms and in applied researches on
the potential use of diatom for nanotechnological application in the field of optoelectronics, nanomechanics, and biosensoring. These research activities involve
several collaborations with national and international scientific institute, university, and private companies.
E-mail: mario.destefano@unina2.it
EPIZOIC DIATOMS ON GASTROPOD SHELLS
When Substrate Complexity Selects for Microcommunity Complexity
DOMENICO D’ALELIO1,4, MARIA TERESA CANTE1,
GIOVANNI FULVIO RUSSO2, CECILIA TOTTI3,
AND MARIO DE STEFANO1
1
Department of Environmental Sciences, 2nd University of Naples,
81100 Caserta, Italy
2
Department of Environmental Sciences, University of Naples
Parthenope, 80133, Napoli, Italy
3
Department of Marine Sciences, Polytechnical University
of the Marche, Via Brecce Bianche Ancona, Italy
4
Iasma Research and Innovation Centre, Fondazione Edmund Mach,
San Michele all’Adige, Italy
1. Introduction
Complexity pervades biological systems at any scale: from microbes to higher
organisms, from individuals to populations, from communities to ecosystems. The
degree of organization of plant and animal populations, their trophic relationships, and ecological associations is currently explored in ecology. Biodiversity
and community structure are strongly influenced by the complexity of those relationships, in addition to the interplaying between multiple environmental conditions. On the other hand, complexity in microcommunities has not been solved
yet. For instance, the role of substrates in shaping the diversity and structure of
biofouling communities is virtually unexplored.
Benthic microalgae living in shallow coastal regions give a reliable contribution to
the dynamics of the aquatic ecosystems, in terms of primary production, oxygenic
activity, and trophic processes (Mac Intyre et al., 1996). Attached communities of
microalgae can develop in different benthic microenvironments: from detritus (epipelon
and endopelon), rocks (epilithon and endolithon), and sediment sands (epipsammon),
to microalgal and seagrasses turfs (epiphyton) and animals (epizoon) (Round, 1971).
The peculiar microenvironments provided by marine animals – i.e., growing in size,
metabolite-rich, and potentially grazers-free – are successfully exploited by an important lineage of benthic microalgae, the diatoms (Round, 1981).
1.1. THE DIATOMS
Diatoms (Bacillariophyta) constitute a successful lineage of unicellular Heterokonts
(Falkowski et al., 2004), both planktonic and benthic, which is responsible for the
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20% of the global primary production (Smetacek, 1999). Diatoms represent the
most intensively studied marine microalgae. To date, more than 10,000 diatom
species have been described (Mann, 1999), but the evaluation of the total number
of existing species is still on debate due to both cryptic diversity within and the
capability of this algae to spread around the world in every aquatic environment.
Another unique feature of diatoms is the capability to take silicon from water and
convert it into a highly ornamented siliceous cell wall, the frustule, in which the
protoplast is enclosed. The frustule is constructed like a pill-box, consisting of
two valves, with the ventral (hypovalve) slightly smaller than the dorsal (epivalve),
joined together by a series of silica bands (copulae) that form the lateral walls
of the box (girdle or cingulum) (Round et al., 1990; van den Hoek et al., 1996)
(Fig. 1a). Cell division occurs with the formation of a new valve inside each of
the two mother valves, so that one daughter-cell has the same size as the mother,
whereas the other is smaller. This modality of division is called “size reduction” as
it leads to a progressive diminishing of the size of the population. The size reduction ends with a meiotic process, which produces two gametes. Gametes fuse and
form a diploid cell (auxospore), which lacks the silica frustule at the first stages
of development, and it is thus able to re-establish the original maximum cell size
(Round et al., 1990).
Diatoms possess a number of chloroplasts that vary from one to many per
cell, depending on the species (Fig. 1). Chlorophyll a, c1, c3, and c2 are the most
important photosynthetic pigments. Carotenoids and xanthophylls, mainly
fucoxanthin, are the most abundant accessory pigments. Diatoms have an enormous ecological significance; they are ubiquitous in the plankton and benthos of
marine and freshwater environments, from the tropics to the Polar Regions, as
well as in temporarily humid surroundings, such as damp moss or rocks (Round,
1981; Mann, 1999). Diatoms are crucially involved in the ocean biological pump,
and frustules form a consistent part of organogenic sediments in marine bottoms
(Smetacek, 1999).
Traditionally, two main orders have been considered within diatoms,
Centrales and Pennales, showing radial and bilateral symmetry of the valves,
respectively (Hustedt, 1959). However, we must point out that this classification
is often arbitrary. Some centric diatoms do not possess radial symmetry and some
pennates are not bilaterally symmetric. Round et al. (1990) proposed a different
classification based on three classes: Coscinodiscophyceae (corresponding to
centric diatoms, Fig. 1b), Fragilariophyceae (araphid pennate species, Fig. 1c),
and Bacillariophyceae (raphid pennate species, Fig. 1d), with a total of 44 orders
and 91 families.
Species ascribed to Bacillariophyceae have a pennate symmetry and are
characterized by a peculiar structure, the raphe, which is a deep slit running
across the valve from pole to pole, and from which mucous is emitted. Raphid
diatoms (mono- or biraphid, whether the raphe is borne in only one or both the
valves) use this structure for locomotion, i.e., they slide above the mucous trails
released by the raphe itself (Fig. 1e, f). Species ascribed to Fragilariophyceae have
EPIZOIC DIATOMS ON GASTROPOD SHELLS
351
Figure 1. (a) The diatom frustule; (b) a centric diatom showing several chloroplasts; (c) a pennate
araphid diatom showing two chloroplasts; (d) a pennate raphid diatom showing two chloroplasts;
(e–f) a schematic view and a light microscopy image (LM) of the raphe in a pennate diatom, respectively.
(a) and (e) modified from Round et al., 1990.
a pennate symmetry too, but lack the raphe, and are generally attached to the
substrate by means of mucous pillows or stalks/peduncles extruded by specific
structures located at the valve apices (apical pore fields).
1.2. EPIZOIC DIATOMS: GLASS CELLS LIVING ON WET FLESH
Among those characterized by a benthic life mode, many diatoms are reported to
colonize sponges (Cerrano et al., 2004a, b), hydrozoans (Bavestrello et al., 2008;
Romagnoli et al., 2006), bryozoans (Wuchter et al., 2003), crustaceans (Ikeda,
1977), bivalves (Round, 1981), and vertebrates (Round, 1981; Round et al., 1990),
with a high degree of specificity for some hosts. This is possible because of the
presence of different and sometimes ad hoc strategies used by these microalgae
to keep in connection with, as well as to gain “hospitality” by, their substrate.
The main strategy accounts for the development of differentiated growth forms
(Fig. 2a–f), such as:
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Figure 2. (a) and (b) Adnate diatom cells adhering horizontally to a substrate (Scanning Electron
Microscope, SEM, scale bars = 10 and 5 µm, respectively); (c) and (d) erect diatom cells adhering
vertically to a substrate (SEM, scale bar = 10 and 10 µm, respectively) – a peduncle connecting the
colony to the host surface is visible in C; (e) and (f) motile diatom cells (SEM, scale bars = 5 and 2 µm,
respectively).
1. Adnate cells (both biraphids and monoraphids diatoms), strongly adhering
horizontally to the substrate by means of the raphidic valve (Fig. 2a, b)
2. Erect cells (araphid, biraphid, and monoraphid diatoms), adhering vertically to
the substrate by means of mucous pillows or stalks/peduncles (Fig. 2c, d)
3. Motile cells (mostly biraphid, some monoraphid diatoms), having high
movement capability enabling them to glide and spread above the substrate
(Fig. 2e, f)
EPIZOIC DIATOMS ON GASTROPOD SHELLS
353
The succession of benthic diatom communities is well explained by the
dynamics of colonization of a new substrate by the above-mentioned growth
forms. Populations of adnate forms, strongly attaching to the substrate, represent
the first encrusting and more stable component in the diatom assemblage.
Populations of erect forms, by adhering to a smaller surface, are less stable and
colonize the substrate after the adnates. Eventually, populations of motile forms,
only partially adhering, spread more effectively above the substrate than the other
forms, but are less stable and can be easily removed by water movements. Thus,
while a young community is mainly dominated by adnates, an older and wellstructured community should include the three growth forms, all equally important in quantitative terms (Round et al., 1990).
Despite the general ecological succession explained earlier, epizoic diatom
communities have a complex dynamics strongly depending on the nature and
dynamics of their substrate, e.g., the animal’s growth, position in the water column, swimming behavior, exposition to streams, and so on.
The interaction between diatoms and Porifera has been recently well documented. Many Antarctic sponges can host rich communities of these microalgae
due to the capability of pinacoderms cells to incorporate them for a certain time
before their digestion (Cerrano et al., 2004a, b; Totti et al., 2005). Monospecific
assemblages of the diatom Porannulus contentus Hamilton, H. Klöser, and M. Poulin
have been observed in some species of Antarctic sponges. A dense mat of P. contentus was detected on the outer surface of the sponge Mycale acerata Kirkpatrick;
this mat is incorporated within the animal tissues, thus suggesting that the sponge
itself can feed on this diatom (Cerrano et al., 2004a). A much more complex diatom
community is associated with the sponge Sphaerotylus antarcticus Kirkpatrick, a
species externally covered by a dense layer of spicules. This envelop represents a
three-dimensional habitat richly colonized by a diversified community of benthic
diatoms – e.g., the centric diatom Hyalodiscus sp., the pennate Diploneis crabro
Ehrenberg, Entomoneis paludosa (W. Smith) Reimer, Trachyneis aspera (Karsten)
Hustedt, Pleurosigma intermedium Smith – and a high density of planktonic species,
such as Fragilariopsis curta (Van Heurck) Hustedt (Totti et al., 2005).
A number of examples of epizoic associations are known for marine
hydroids, as their episarc represents a very suitable habitat for diatom growth and
it often looks brown for the presence of adnate and pedunculate diatoms. A dense
assemblage of the pennate Cocconeis notata Petit was reported on the hydroid
Campanularia integra MacGillivray, which is in turn an epibiontic of the brown
seaweed Macrocystis pyrifera (Linnaeus) C. Agardh (Siqueiros-Beltrones et al.,
2001). Round et al. (1961) documented different kinds of diatom assemblages
lying on hydroids ascribed to Sertularia operculata Linnaeus and exposed at different hydrodynamic conditions. Recently, Di Camillo et al. (2005) reported several examples of host specificity for epibiontic diatoms and hydroids. A clear
spatial distribution of epibiontic diatoms has been reported for the marine
hydroid Eudendrium racemosum Gmelin (Romagnoli et al., 2006): adnate diatoms
were distributed mainly in the basal and central part of the hydroid colonies,
while erect forms were in the apical part only.
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Interesting epizoic associations are also known for planktonic crustaceans,
both in freshwater and marine environments, which carry epibiontic diatoms or
cyanobacteria on their exoskeleton and appendages (Ikeda, 1977; Round, 1981;
Hiromi et al., 1985; Gaiser and Bachmann, 1994). For example, diatoms belonging
to the genus Pseudohimantidium can produce monospecific and stable assemblages
on the marine copepod, Coryacaeus (Gibson, 1978).
2. Diatom–Gastropod Interactions
The hard shells of mollusks are reported to provide a substrate for the settling of
microphytobenthos, and sometimes a high degree of specificity has been found
between epizoic diatoms and their animal hosts. For instance, a rich community
including several benthic diatom genera (e.g., Licmophora, Achnanthes, Cocconeis)
was reported on the bivalve Pinna nobilis Linnaeus, with a species composition
differing from that seen in co-occurring thalli of the brown algae Cystoseira
(Round, 1971 and references therein). A dense assemblage of Cocconeis placentula Ehrenberg has been reported on the shells of Hydrobia ulvae Pennant, with
no relation between the size of the shell and the density of the diatomaceous layer
(Gillan and Cadée, 2000).
In a recent study, gastropod species were sampled from a coastal site in the
Bay of Naples during summer 2006 (Cante et al., 2008). The sampled specimens
were highly representative for inshore Mediterranean waters and differed in
dimension, gross-, and fine-scale morphology of the shell. By means of a
multi-approached research, based on Scanning Electron Microscopy and computer-based image analysis, we revealed that the degree of complexity of epizoic diatom mats (in terms of species composition and biodiversity indexes) is mainly
influenced by the complexity of the host shell, despite its overall dimension. The
following sections open a detailed window about the above-mentioned study.
2.1. GASTROPOD SHELLS AS SELECTIVE MICROENVIRONMENTS
FOR DIATOM COMMUNITIES
In order to decrypt reliable microselective constraints in the building process of
diatom communities on the shell surface, the following gastropod species were
extensively investigated:
1. Columbella rustica Linnaeus (Gasteropoda, Prosobranchia, Caenogastropoda,
Neogastropoda, Columbellidae)
2. Alvania lineata Risso (Gasteropoda, Prosobranchia, Caenogastropoda, Mesogastropoda, Rissoidae)
3. Nassarius incrassatus Stroem (Gasteropoda, Prosobranchia, Caenogastropoda,
Neogastropoda, Nassariidea)
EPIZOIC DIATOMS ON GASTROPOD SHELLS
355
4. Bittium reticulatum Da Costa (Gasteropoda, Prosobranchia, Caenogasteropoda,
Mesogasteropoda, Cerithiidae)
5. Clanculus cruciatus Linnaeus (Gasteropoda, Prosobranchia, Archaeogastropoda, Vetigasteropoda, Trochidea)
6. Gibbula adansoni Payraudeau (Gasteropoda, Prosobranchia, Archaeogastropoda, Vetogastropoda, Trochidea)
7. Jujubinus striatus Linnaeus (Gasteropoda, Prosobranchia, Archaeogastropoda,
Vetogastropoda, Trochidea)
The above-mentioned gastropods, shown in detail in Figs. 3 and 4, were ordered
according to their shell fractal dimension (D) – i.e., the theoretical dimension
measuring the degree of irregularity and interruption of an object (Mandelbrot,
1977). D is commonly used to quantify the degree of discontinuity of landscapes.
Basically, the higher the D, the more chaotic and discontinuous is the surface.
In turn, more organized (i.e., regular) landscapes show a relatively lower value
of D. D value ranges 1.460–1.635 for the above-mentioned gastropods species.
However, the one-dimensional shell size is more variable, ranging 4–20 mm
(Table 1).
The first three species, A. lineata, Co. rustica, N. incrassatus, showing the
highest values of D and a low degree of fine-scale ornamentation, represent
highly irregular microscopic landscapes (Fig. 3a–i). The following two species,
B. reticulatum and C. cruciatus, with a value of D approaching 1.56 and a moderate
degree of ornamentations, represent a better organized and more regular landscape (Fig. 4a–f). Gibbula adansoni’s landscape was comparable with those made
by the previous two species in terms of regularity, though this species was weakly
ornamented on one side, and relatively smooth on the other side of the shell
(Fig. 4g–i). Finally, J. striatus, characterized by the lowest fractal dimension and
the highest density of radial swirls, represented the more regular and organized
landscape among those under examination (Fig. 4j–l).
The substrate provided by gastropod shells is characterized by different
kinds of structures lying on a spatial scale comparable to the cell size (20–100 µm).
The simplest substrates, with a chaotic arrangement, are generally deprived of
stable structures; the more organized ones show a regular succession of “mountain-like” swirls, deep “canyons,” and smooth and protected “valleys”. Such a
“microscopic landscape” can be differentially exploited by encrusting organisms.
Different diatom species (and different growth forms, see Section 1.2) can
buildup different communities, depending on the actual microenvironments they
develop on.
Adnate forms took advantage from the different shell morphologies, because
they effectively exploited the microhabitats provided by shells with a more
organized landscape. For instance, the genera Amphora and Cocconeis adhered
preferentially to surfaces with protuberances and reticulations (e.g., Bittium
reticulatum), and small Cocconeis species (e.g., C. neothumensis Krammer) managed to adhere to surfaces with many microhabitats (e.g., Clanculus cruciatus).
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Figure 3. (a) Alvania lineata (optical image, OI, scale bar = 1 mm); (b) A. lineata (SEM, scale bar =
300 µm); (c) A. lineata, shell surface with few ornamentations (SEM, scale bar = 150 µm); (d) Columbella
rustica (OM, scale bar = 6 mm); (e) C. rustica (SEM, scale bar = 400 µm); (f) C. rustica, surface with
calcareous incrustations (scale bar = 50 µm); (g) Nassarius incrassatus (OI, scale bar = 5 mm); (h)
N. incrassatus (SEM, scale bar = 500 µm); (i) N. incrassatus, shell surface with spiral bands and canyons
(scale bar = 250 µm).
Some adnate taxa, colonizing shells with complex morphological structures, slid
into the canyons and formed endolithic structures, which eventually became
integrated into the shell surface. This peculiar behavior might represent a strategy
to avoid grazers as well as competition for space with other diatom species. Erect
diatoms, in turn, could only hardly cope with water movements (e.g., by means of
elastic fluctuations of their peduncle), because their adhesion to the shell was
partial. Finally, the almost absolute absence of motile species in nearly all the
shells under analysis should be due to the scarce capability of this substrate to
keep them safe from water turbulence and mechanical stress provoked by streams
and animal motion.
EPIZOIC DIATOMS ON GASTROPOD SHELLS
357
Figure 4. (a) Bittium reticulatum (OI, scale bar = 4 mm); (b) B. Reticulatum (SEM, scale bar = 300 µm);
(c) B. reticulatum, shell surface with many ornamentation and a complex reticulation (SEM, scale bar
= 150 µm); (d) Clanculus cruciatus (OM, scale bar = 5 mm); (e) C. cruciatus (SEM, scale bar = 600 µm);
(f) C. cruciatus, shell surface with small canyons among granulated swirls (scale bar = 250 µm);
(g) Gibbula adansoni (OI, scale bar = 6 mm); (h) G. adansoni (SEM, scale bar = 700 µm); (i) G. adansoni,
shell surface with coarse spiral bands and few canyons (scale bar = 100 µm); (J) Jujubinus striatus (OI,
scale bar = 5 mm); (k) J. striatus (SEM, scale bar = 1 mm); (l) J. striatus, shell surface with narrows
swirls (scale bar = 100 µm).
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Table 1. Combined characteristics of gastropods and relating epibionthic diatom communities.
Gastropods having different gross shell morphology, dimension, and ornamentation are ranked
according to their fractal dimension (D), from the highest to the lowest value. The diatom communities
are characterized by the overall cell abundance (A, cells per square millimeter), the species richness
(S), and community evenness (P).
Gross shell
morphology
Gastropods
Shell
dimension
(mm)
1.653
1.650
829
531
13
17
0.32
0.60
1.563
1,467
9
0.61
1.557
684
25
0.80
1.551
1,323
25
0.72
1.460
350
16
0.70
Many spiral rounds
Elongated
13
C. cruciatus
Spinning
top-shaped
Spinning
top-shaped
Spinning
top-shaped
10
Co
0.30
10
B. reticulatum
A
7
11
17
15
J. striatus
448
Spiral rounds with
radial swellings
None
Radial protuberances
and spiral bands
Radial swellings and
bands
Spiral rounds and
granulated bands
Few rounds, smooth
Co. rustica
N. incrassatus
G. adansoni
(S)
1.653
(D)
Globular/
tower-like
Globular
Globular
A. lineata
(A)
(c·mm−2)
Ornamentation
4
N
B
C
G
(J)
J
Adnate
Erect
Motile
Figure 5. Distribution of the main diatom growth forms (adnate, erect, and motile) above each
gastropod shell (indicated by the bold capital letter above each pie: A = Alvania lineata, Co = Columbella
rustica, N = Nassarius incrassatus, B = Bittium reticulatum, C = Clanculus cruciatus, G = Gibbula adansoni,
J = Jujubinus striatus).
The adnate genus Amphora (biraphid) and Cocconeis (monoraphid) were
the primary component of shell-diatom communities. Another component more
differentiated in terms of genera, which may be defined as secondary, included
erect genera, mainly Tabularia, Grammatophora, Rhabdonema, and Licmophora.
A fraction of motile diatoms, rarely becoming numerically important, was represented by the genera Navicula, Diploneis, and Nitzschia. Moreover, the presence
of conspicuous bacterial and fungal mats competed against diatoms for space.
Thus, the peculiar substrate provided by gastropods could have fostered the
dominance of adnate against erect and motile species (Fig. 5).
EPIZOIC DIATOMS ON GASTROPOD SHELLS
359
Alvania lineata, Columbella rustica, and Nassarius incrassatus showed a
globular and heavy shell with few ornamentations (Fig. 3a–i), such as coarse spiral
bands (Fig. 3b, c, h, i) and calcareous incrustations (Fig. 3f), and they all hosted a
community prevalently made by adnate species (Fig. 6). Those shells were also
differentially colonized. While the apical portion of A. lineata was poorly colonized, the central and inferior sides showed a uniform distribution of Amphora
cf. helenensis (Fig. 6a–c). The central portion of Co. rustica showed scales and
rich assemblages of adnate (dominated by Amphora cf. helenensis) and some
erect taxa accumulated among adjacent scales (Fig. 6d–f). Finally, Amphora
cf. helenensis dominated in the apex, while Cocconeis spp. formed the central portion
of N. incrassatus (Fig. 6h, i).
Figure 6. SEM pictures of Alvania lineata (a–c), Columbella rustica (d–f), and Nassarius incrassatus
(g–i) at different magnifications. (a) shell surface with few ornamentation (scale bar = 150 µm);
(b) microcommunity of adnate dominated by Amphora cf. helenensis (scale bar = 20 µm); (c) two cells
of Amphora cf. helenensis (scale bar = 10 µm); (d) shell surface with scales (scale bar = 150 µm);
(e) a rich assemblage of adnate and some erect taxa among adjacent scales (scale bar = 50 µm);
(f) cells of Amphora cf. helenensis (scale bar = 25 µm); (g) shell surface with small canyon (scale
bar = 30 µm); (h) microcommunity of adnates (scale bar = 10 µm); (I) cells of Amphora cf. helenensis
(scale bar = 10 µm).
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Bittium reticulatum and Clanculus cruciatus showed many ornamentations in
their shells, which created microhabitats that favored the adhesion of several
adnate species, some erects, and the movement of motile taxa (Fig. 4a–f). Amphora
cf. helenensis and Cocconeis scutellum effectively colonized B. reticulatum, while
other Cocconeis spp. grew inside the shells forming a rich endolithic community
(Fig. 7a–c). A copious diatom community, made up of adnate (dominant), erects,
and motile, developed on C. cruciatus where many small cells (e.g., C. neothumensis)
slid into small canyons among granulated swirls (Fig. 7e, f). Moreover, many motile
species found protection within little and narrow valleys where they could keep
moving in and reproduce.
Gibbula adansoni showed a highly organized shell which was, however, rather
smooth at the spatial scale of the cells (Fig. 4g–i). Only a small number of ornamentations and coarse spiral bands with few canyons were present and the central
portion of the shell showed some grooves hosting rich assemblages of Cocconeis
spp. (Fig. 7g–i). However, the remnant portion of the shell showed a scattered
colonization, with single cells or small groups of two or three specimens (e.g.,
Amphora cf. helenensis).
Jujubinus striatus shell showed dense, homogenously distributed, and narrow swirls. However, though describing a regular and highly organized landscape,
it lacked a complex reticulation at the scale of the cells (Fig. 4j–l). The diatom
community, dominated by adnate species, was not copious and cells were single
or in small groups of two or three (Fig. 7j, k). Among adnate, Cocconeis peltoides
Hustedt and Cocconeis distans (Gregory) Grunow (which are also epipsammic
species) were dominant (Fig. 7l).
2.1.1. How Substrate Complexity Influences Community Structure
One would expect that gastropod shells should select for diatom communities
based on their size, with smaller shells hosting extremely simple communities, both
in terms of absolute abundance and species composition, and large shells hosting more structured communities. In fact, in our research, Bittium reticulatum,
Gibbula adansoni, Columbella rustica, and Clanculus cruciatus hosted a high quantity of epizoic diatoms, while the smallest shells, Jujubinus striatus, Alvania lineate,
and Nassarius incrassatus, hosted a lower quantity. However, shells with a similar
size, such as B. reticulatum and J. striatus, hosted far different diatom communities: B. reticulatum showed the highest abundance with a low diversity, whereas
J. striatus showed the lowest abundance, but high species richness. Moreover,
Gibbula adansoni, Clanculus cruciatus, and Jujubinus striatus hosted the highest
specific diversity, even though they had different dimension and ornamentations
(Table 1). In addition, while the specific composition did not vary significantly in
different shells, the absolute and relative abundances of diatom community were
more variable (Table 1). The Pielou index of evenness (J, a number ranging 0,
for a community dominated by only one species, and 1, for a richer community
where all species are equally represented; Pielou, 1966) varied significantly among
the investigated shells (Table 1). From the comparison of J and D in different
EPIZOIC DIATOMS ON GASTROPOD SHELLS
361
Figure 7. SEM pictures of Bittium reticulatum (a)–(d), Clanculus cruciatus (e) and (f), Gibbula adansoni
(g)–(i), and Jujubinus striatus at different magnifications (j)–(l). (A) Shell surface with deep canyons
(scale bar = 150 µm); (b) assemblage of Amphora cf. helenensis (scale bar = 60 µm); (c) endolithic
communities of Cocconeis scutellum (scale bar = 30 µm); (D) small canyons among granulated swirls
(scale bar = 120 µm); (e) diatom communities dominated by adnate (scale bar = 40 µm); (f) few cells of
Cocconeis spp. (scale bar = 30 µm); (g) shell surface with a small number of ornamentation (scale bar
= 60 µm); (h) endolithic community of Cocconeis spp. (scale bar = 40 µm); (i) small group of Amphora
cf. helenensis and a couple of endolithic cells in the background (scale bar: 10 µm); (j) shell surface with
few ornamentation (scale bar = 90 µm); (k) small group of two or three cells (scale bar = 30 µm); (L)
two cells of Cocconeis spp. (scale bar = 15 µm).
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DOMENICO D’ALELIO ET AL.
1.0
C
0.8
G
J
N
J
0.6
B
0.4
0.2
0.0
1.65
Co
R2 = 0.8
A
1.60
1.55
1.50
1.45
D
Figure 8. A comparison between the evenness (J) of diatom communities on gastropods shells (capital
letters, as in Fig. 5) and shell fractal dimension (D). The dimension of each ball represents the individual shell size. The scale of the y-axis is inverted for graphical reasons.
shells, an interesting pattern emerged: the diatom community structure in different
shells seems to be influenced by the complexity of the substrate. The more organized is the gastropod shell (i.e., the lower the D), the more complex (in terms of
species richness and biodiversity indexes) is the diatom community. For instance,
the Pielou index well correlates with the shell fractal dimension, with the more
irregular shells having a low evenness, and the latter parameter increasing with the
increasing substrate complexity (Fig. 8).
The diatom community encrusting the irregular and discontinuous substrate
provided by A. lineata was composed by only seven species (S = 7, Table 1), four
of which were adnate, two motile, and only one erect; in such shells, adnate cells
occurred in large majority (90% of the total cells, Fig. 5) and J for this community
was close to 0 (Table 1). An analogous community (J = 0.32) – made by 13 species,
among which 6 were adnate, 3 erect, and 4 motile-colonized Co. rustica, which also
showed a chaotic shell arrangement. As an exception, Nassarius incrassatus and
B. reticulatum showed similar evenness (J approaching 0.60), though having far
different shell-fractal dimensions (1.65 vs. 1.56, respectively); also, both the shells’
diatom communities were dominated by adnate taxa (11 out of 17 in N. incrassatus
and 7 out of 9 in B. reticulatum). On the contrary, well-structured diatom communities colonized the more organized shells of C. cruciatus, G. adansoni, and
J. striatus. These three shells showed the higher specific diversity (S = 25, 25, and 19,
respectively) and evenness (J = 0.80, 0.72, and 0.70, respectively). Adnate taxa were
dominant in all the three (57%, 65%, and 68% of the total species, respectively),
but erect and motile together accounted for 43% of the total species in C. cruciatus,
35% in G. adansoni, and 22% in J. striatus. Moreover, C. cruciatus hosted a large
amount of motile cells (Fig. 5), which might successfully exploit the fine-arranged
microenvironment provided by this shell and spread into it.
EPIZOIC DIATOMS ON GASTROPOD SHELLS
363
In comparison with other animal-derived microenvironments, and based on
the scarce literature available, diatom communities colonizing vagile mollusks, such
as gastropods, seem to be different from those developing on sponges, hydrozoans,
and crustaceans. In particular, gastropod shells and hydroid colonies, for which a
comparable amount of data has been collected, host different diatom communities.
The global dominance of adnate taxa in any microenvironment available on gastropod shells contrasts with the reliable spatial segregation of adnate and erect taxa
detected in hydroids, with the first dominant on the basal and central side of the
host, and the second, on the apical side, probably due to a combined effect of differential grazing and hydrodynamic conditions (Romagnoli et al., 2006).
The data included in this section, though preliminary, clearly suggest that,
besides the overall dimension, the gastropod shell morphology represents a
stronger constraint in the developing and structuring of epizoic diatom communities. Adnate taxa are largely dominant in those substrates, while erect and
motile forms occur generally with low abundances, probably due to the effect of
particular hydrodynamic conditions (such as microturbulence) that may limit the
colonization of the taxa having reduced adhesion surface (erect) or being partially
detached from the substrate (motile). Adnate taxa, in turn, can strongly adhere
to the substrate – and sometimes “inside” the substrate in a sort of endolithic
behavior – and grow in number within shell ravines.
3. Chapter’s Conclusions
In general terms, community complexity emerges from a combination of differential environmental conditions on substrates and the capability of organisms to
adapt to them: the more complex the substrate, the more complex the dynamics
of colonization. As a cascade effect, the more diverse the way organisms stabilize
into an environment, the higher the biodiversity and the evenness of colonizing
communities.
The chapter shed light upon animal–plants interaction at the microscale.
Our final conclusion is that microscopic “plants” like diatoms can successfully
exploit animal-derived microenvironments to grow and build different kinds of
communities whose organization is strongly selected by the organization of the
substrate itself.
4. References
Bavestrello, G., Cerrano, C., Di Camillo, C., Puce, S., Romagnoli, T., Tazioli, S. and Totti, C. (2008)
The ecology of protists epibiontic on marine hydroids. J. Mar. Biol. Ass UK 88(8): 1611–1617.
Cante, M.T., De Stefano, M., Giudice, F., Totti, C. and Russo, G.F. (2008) Marine gastropod shells
as selective microenvironment for diatom communities. 20th International Diatom Symposium
2008 7–13 September 2008, Dubrovnik, Croatia.
364
DOMENICO D’ALELIO ET AL.
Cerrano, C., Calcinai, B., Cucchiari, E., Di Camillo, C., Nigro, M., Regoli, F., Sarà, A., Schiapparelli,
S., Totti, C. and Bavestrello, G. (2004a) Are diatoms a food source for Antartic sponges? Chem.
Ecol. 20(1): 57–64.
Cerrano, C., Calcinai, B., Cucchiari, E., Di Camillo, C., Totti, C. and Bavestrello, G. (2004b). The
diversity of relationships between Antartic sponges and diatoms: the case of Mycale acerata
Kirkpatrick, 1907. Polar Biol. 27: 231–337.
Di Camillo, C., Puce, S., Romagnoli, T., Tazioli, S. and Bavestrello, G. (2005) Relationships between
benthic diatoms and hydrozoan (Cnidaria). J. Mar. Biol. Ass UK 85: 1373–1380.
Falkowski, P., Katz, M.E., Knoll, A.H., Quigg, A., Raven, J.A., Schofield, O. and Taylor, F.J.R. (2004)
The evolution of modern eukaryotic phytoplankton. Science 305: 354–360.
Gaiser, E. and Bachmann, R. (1994) Seasonality, substrate preference and attachment sites of epizoic
diatoms on cladoceran zooplankton. J. Plank. Res. 16(1): 53–68.
Gibson, R.A. (1978) Pseudohimantidium pacificum, an epizoic diatom new to the Florida Current.
J. Phycol. 14: 371–373.
Gillan, D. and Cadée, G.C. (2000) Iron-encrusted diatom and bacteria epibiotic on Hydrobia ulvae.
J. Sea Res. 43: 83–91.
Hiromi, J., Kadota, S. and Takano, H. (1985) Infestation of Marine Copepods (Review). Bull. Tokai
Reg-Fish Res. Lah, pp. 117.
Hustedt, F. (1959) Die Diatomeenflora der Unterwesser von der Lesummündung bis Bremerhaven mit
Berücksichtigung des Unterlaufs der Hunte and Geeste. Ver, ff. Inst. Meeresforsch. Bremerhaven
6: 13–176.
Ikeda, T. (1977) A pelagic marine copepod associated with diatoms. Bull. Plankton Soc. Jap. (Japan)
24(2): 115–118.
Mac Intyre, H.L., Geider, R.J. and Miller, D.C. (1996) Microphytobenthos: the ecological role of the
secret garden of unvegetated, shallow-water marine habitas. I. Distribution, abundance and primary
production. Estuaries 12(2a): 186–201.
Mandelbrot, B.B. (1977) The Fractal Geometry of Nature. W.H. Freeman & Co., San Francisco,
pp. 460.
Mann, D.G. (1999) The species concept in diatoms. Phycologia 38: 437–495.
Pielou, E.C. (1966) The measurement of diversity in different types of biological collections. J. Theor.
Biol. 13: 131–144.
Romagnoli, T., Bavestrello, G., Cucchiari, E., De Stefano, M., Camillo, C., Pennesi, C., Puce, S. and
Totti, C. (2006) Microalgal communities epibiontic on the marine hydroid Eudendrium racemosum
in the Ligurian Sea during an annual cycle. Mar. Biol. 151(2): 537–552.
Round F.E. (1971) Benthic marine diatoms. Ocean. Mar. Biol. Ann. Rev. 9: 83–139.
Round F.E. (1981) The Ecology of Algae. Cambridge University Press, Cambridge, pp. 653.
Round, F.E., Sloane, J.F., Ebling, F.J. and Kitching, J.A. (1961) The ecology of Lough Ine X. The
hydroid Sertularia operculata (L.) and its associated flora and fauna: effects of transference to
sheltered water. J. Ecol. 49: 617–629.
Round, F.E., Crawford, R.M. and Mann, D.G. (1990) The diatoms. Biology, Morphology of the Genera.
Cambridge University Press, Cambridge, pp. 747.
Siqueiros Beltrones, D.A., Serviere-Zaragoza, E. and Argumedo Hernandez, U. (2001) First record
of the diatom Cocconeis notata Petit living inside the hydrotheca of a hydrozoan epiphyte of
Macrocystis pyrifera (L.). C. Ag. Oceànides 16(2): 135–138.
Smetacek, V. (1999) Diatoms and the ocean carbon cycle. Protist 150: 25–32.
Totti, C., Calcinai, B., Cerrano, C., Di Camillo, C., Romagnoli, T. and Bavestrello, G. (2005) Diatom
selection by the Antartic sponge Sphaerotylus antarticus, 1908. J. Mar. Biol. Ass. UK 85: 795–800.
van den Hoek, C., Mann, D.G. and Jahns, H.M. (1996) Algae: An Introduction to Phycology. Cambridge
University Press, Cambridge, pp. 637.
Wuchter, C., Marquardt, J. and Krumbein, W.E. (2003) The epizoic diatom community on four bryozoan
species from Helgoland (German Bight, North Sea). Helgol. Mar. Res. 57: 13–19.