Epibiosis of Calpensia nobilis (Esper) (Bryozoa: Cheilostomida) on

Posidonia oceanica (L.) Delile rhizomes: Effects on borer colonization and

morpho-chronological features of the plant

Mariamichela Cigliano a,*, Silvia Cocito b, Maria Cristina Gambi a

a Laboratorio di Ecologia del Benthos, Stazione Zoologica ‘‘A. Dohrn’’ di Napoli, P.ta S. Pietro, 80077 Ischia-Napoli, Italyb ENEA Marine Environment Research Centre, P.O. Box 224, 19100 La Spezia, Italy

Received 14 May 2005; received in revised form 9 July 2006; accepted 11 August 2006

Abstract

Shoots of the Mediterranean seagrass Posidonia oceanica (L.) Delile can be overgrown with a thick encrustation of the bryozoan Calpensia

nobilis (Esper) (Chelostomida) particularly under high hydrodynamic conditions. We compared shoots with and without this encrustation and

assessed whether it affected shoot morphology and production, and incidence of polychaete borers. The borers collected were represented by three

species of polychaete Eunicidae (Lysidice ninetta, Lysidice collaris and Nematonereis unicornis). Shoots affected by overgrowth of C. nobilis

showed a significantly lower borer frequency (17% versus 49%), lower values of both yearly biomass of the rhizome (mean 6.3 mg/year in shoot

with C. nobilis versus 8.3 mg/year in shoot without) and biomass/elongation (B/E) ratio, and lower mean sheath thickness (0.25 mm versus

0.30 mm), while the mean width of the leaves was slightly higher (1.0 mm versus 0.7 mm). Significant Spearman coefficient’s values were

estimated between carbonate mass of C. nobilis and rhizome length, muff length and rhizome length, and maximum thickness of the muff and

rhizome length. Plant and bryozoan morphometrics allowed to estimate between 5 and 10 years the colonization age of C. nobilis on the living

shoots studied.

# 2006 Elsevier B.V. All rights reserved.

Keywords: Posidonia oceanica; Bryozoan; Calpensia nobilis; Polychaete; Borer; Lepidochronology; Mediterranean sea

www.elsevier.com/locate/aquabot

Aquatic Botany 86 (2007) 30–36

1. Introduction

In seagrasses, borers represent mesofaunal organisms

burrowing into seagrass tissue (Gambi et al., 2003a). In

Posidonia oceanica meadows of the Mediterranean, a single

species of borer isopod and four species of borer polychaete

Eunicidae (Guidetti et al., 1997; Gambi, 2002), represent a

unique group of detritus consumers since they specifically

colonize and feed on P. oceanica sheaths (remains of the leaf

bases which persist along the rhizome). Their burrowing

activities enhance scale fragmentation, and microbial activity,

thus they may play a role in accelerating sheath decay and their

recycling (Gambi et al., 2000). The distribution of borers has

been studied in several Posidonia beds mainly along the Italian

coasts, from analysis at regional scale (Di Maida et al., 2003;

Gambi et al., 2005a,b) to depth gradients along a single

* Corresponding author.

E-mail address: cigliano@szn.it (M. Cigliano).

0304-3770/$ – see front matter # 2006 Elsevier B.V. All rights reserved.

doi:10.1016/j.aquabot.2006.08.006

meadow (Gambi, 2002) and temporal distribution (Gambi and

Cafiero, 2001). Overall these organisms occur in a wide range

of environmental conditions and showed a high spatial

variability in abundance and frequency. Among local factors,

silting and epiphytism on P. oceanica shoots could affect sheath

features, e.g. oxygen concentration, that may prevent coloniza-

tion by these organisms. Among the epiphytes of P. oceanica

shoots, particularly in meadows subject to strong currents, the

bryozoan Calpensia nobilis forms thick calcareous muff-like

structures circum-encrusting rhizomes (Occhipinti Ambrogi,

1986; Poluzzi and Coppa, 1991; Romero Colmenero and

Sanchez Lizaso, 1999). This species is commonly recorded as

epiphyte on a large variety of marine plants and hard substrates

(Gautier, 1962). In a previous study of the coast of Spain,

Romero Colmenero and Sanchez Lizaso (1999) evaluated the

effects of C. nobilis on a set of phenological variables of P.

oceanica. The overgrowth of this bryozoan produced important

changes in P. oceanica rhizomes: a significant increase in

rhizome growth rate and a decrease in its weight/length ratio;

there were no significant differences in rhizome production;

M. Cigliano et al. / Aquatic Botany 86 (2007) 30–36 31

size of C. nobilis colonies was positively correlated with rhizome

growth rate and negatively correlated with its weight/length ratio.

On the whole, the bryozoan effects on the seagrass were similar to

those due to hyper-sedimentation. Presence of this dense

overgrowth may thus affect P. oceanica performance, but could

also interfere with colonization by borers. The aim of this paper is

to compare P. oceanica shoots heavily colonized by C. nobilis

and shoots without the bryozoan, with the null hypothesis that no

differences could be detected in biological characteristics of the

plant and borer occurrence between the two types of shoots.

2. Study site, materials and methods

A strong colonization of the bryozoan C. nobilis was

observed around P. oceanica shoots (Plate 1a) in a meadow

Plate 1. (a) In situ picture showing some Posidonia oceanica shoots colonized by C

colonized by C. nobilis, note that a single muff on the left is enveloping two rhizo

located at 15–17 m depth in the Ischia Strait (between the

islands of Ischia and Procida, Gulf of Naples, Italy) (latitude:

40844.7060N and longitude: 13858.7600E). This site experi-

ences strong flow estimated up to 7500 m3/s and current speed

reaching 40 cm/s. The dominant current has a NNW direction

in autumn and winter, while reverses to SSE in summer (Duing,

1965; De Maio et al., 1983). For morpho-chronological and

borers’ analyses orthotropic (vertical) living rhizomes heavily

colonized by C. nobilis and rhizomes not colonized by the

bryozoan were randomly collected by SCUBA diving in August

2002. In addition, several living rhizomes with different

degrees of bryozoan colonization, and dead rhizomes covered

by the bryozoan, but still in a vertical position, were collected to

study the relationships between bryozoan colony and plant

features. The dead rhizomes collected do not represent shoots

alpensia nobilis colonies at the studied site, (b) some dead shoots of Posidonia

mes and (c) a dead rhizome with the apical growing rims completely merged.

M. Cigliano et al. / Aquatic Botany 86 (2007) 30–3632

Fig. 1. Mean density values (number of shoots/m2) estimated at the margin and

at the inner part of the studied Posidonia oceanica meadow. Rhizomes with and

without Calpensia nobilis, and dead rhizomes covered by C. nobilis were

estimated (bars represent standard deviations).

that were necessarily killed by the bryozoan, since they could

have also been colonized after the death of the shoot by other

natural causes. All rhizomes collected were fixed in 4%

neutralised formalin.

Shoot density (number of shoots per m2) was determined by

counts within quadrates (40 cm � 40 cm; Buia et al., 2004). In

the counts, we distinguished the rhizomes colonized and not

colonized by C. nobilis. In order to estimate the entity of

bryozoan colonization also dead rhizomes covered by C.

nobilis were counted. Shoot density was evaluated in two

different locations, on the margin of the meadows (13

replicates) and a few meters inside the meadow (12

replicates). In the laboratory, borer occurrence was checked,

as well as the presence of traces of previous colonization, and

two indices have been measured: index of borers (IB = per-

centage of rhizomes hosting borers over the total rhizome

analysed) and index of traces (IT = percentage of rhizomes

with only empty traces of borers) (Gambi, 2002; Buia et al.,

2004). In order to date rhizome segments and estimate annual

growth of the plants, analyses were performed according to the

current protocol for ageing reconstruction known as lepido-

chronology (Crouzet et al., 1983). This technique, widely used

in P. oceanica (Pergent and Pergent-Martini, 1991; Pergent-

Martini and Pergent, 1994; Guidetti et al., 2000; Buia et al.,

2004), consists of the measurement of sheath thickness which

presents a cyclical annual variation; two minima in sheath

thickness define a single ‘‘lepidochronological year’’.

Rhizome biomass production (mg/year), elongation (mm/

year), and number of leaves per year were also measured

(Pergent et al., 1989). In addition, thickness of sheaths,

number of intact sheaths and sheath production per year (mass

mg/year) were evaluated. Morphological parameters, such as

number, age (‘adult’ = with a well defined sheath, ‘inter-

mediate’ = without a well defined sheath, and ‘juveniles’ = -

below 5 cm length, according to Giraud, 1977), length and

width of leaves, were examined on shoots colonized by C.

nobilis and shoots free from the bryozoan. To evaluate the

difference of each of the measured variables between the

rhizomes colonized by C. nobilis and those without the

bryozoan, one-way ANOVA was applied. To maintain

independency of data for each variable different rhizomes

were analysed. For some of the morpho-chronological

variables the analyses were made on the last four lepido-

chronological years in order to test independent and

comparable numbers of rhizomes. Homogeneity of variance

for each variable was tested with the Cochran C-test.

Morphology of C. nobilis constructions at different stages of

development on both living and dead rhizomes was analysed to

understand the bryozoan colonization pattern. For each muff,

length, thickness, and weight (dry weight) were measured. The

Table 1a

Some morphometric features of Calpensia nobilis constructions overgrowing livin

Carbonate mass (g d.w.) Length (mm

Living rhizomes (n = 28) 8.3 � 11.9 90.9 � 43.

Dead rhizomes (n = 41) 35.6 � 25.2 127.9 � 40.

number, and the external and internal structure of circum-

encrusting layers forming each muff was counted and analysed

at the microscope. To assess the relationship among morpho-

metric features of the bryozoan a regression analysis was

applied. Correlation between plant morpho-chronological

variables, borer occurrence, and C. nobilis morphometrics

were tested with the Spearman analysis.

3. Results

The total mean shoot density values (number of shoots/m2)

estimated in the inner part of the meadow were slightly lower

than on the margin (229 � 75 and 264 � 85, respectively)

(Fig. 1). The rhizomes colonized by C. nobilis were

significantly more abundant in the marginal part of the

meadow (152 � 88) than in the inner part of the meadow

(36 � 32) (F = 18.69; p = 0.001) (Fig. 1). Also the number of

dead rhizomes covered by the bryozoan was significantly

higher in the marginal meadow (32 � 21) than inside (13 � 19)

(F = 5.59; p = 0.02).

Morphology and growth patterns of the bryozoan were

analysed on colonies occurring both on living and dead

rhizomes (Table 1a). C. nobilis produced superimposed layers

via self-overgrowth, involving vertical growth and thickening

of the resulting three-dimensional architecture, which

enwrapped the rhizome of P. oceanica like a muff. Complete

fusion between different parts of the same colony of the

bryozoan was observed as well as a couple of active margins

acting as potential generators of a new layer.

g and dead rhizomes of Posidonia oceanica

) Maximum thickness (mm) Maximum number of layers

7 3.17 �1.42 –

5 8.34 � 4.68 12.5 � 5.5

M. Cigliano et al. / Aquatic Botany 86 (2007) 30–36 33

Table 1b

Mean values and standard deviations (in parentheses) of the plant morpho-chronological variables measured, and of borer occurrence in rhizomes with Calpensia and

without Calpensia

Number of shoots

examined

Shoots with

Calpensia

Shoots without

Calpensia

F-values p

Rhizome biomass (mg/year) 40 83.7 (32.7) 95.3 (37.3) 6.40 0.05 Rh with C < Rh without C

Rhizome elongation (mm/year) 40 12.9 (6.0) 11.3 (4.5) 1.30 n.s.

B/E (biomass/elongation) 40 6.3 (1.5) 8.3 (1.4) 14.93 0.001 Rh with C < Rh without C

Number of sheaths/year 40 7.0 (0.6) 7.2 (0.6) 0.02 n.s.

Mean sheath thickness (mm) 40 0.25 (0.07) 0.3 (0.04) 63.76 0.001 Rh with C < Rh without C

Number of intact sheaths 40 4.7 (1.2) 2.2 (2.0) 45.29 0.001 Rh with C > Rh without C

Sheath production (mg/year) 40 255.9 (10.2) 212.6 (61.3) 11.17 0.01 Rh with C > Rh without C

Number of leaf/year 20 4.8 (1.3) 5.4 (1.7) 1.92 n.s.

Mean leaf length 20 40.8 (28.3) 44.5 (30.8) 0.19 n.s.

Mean leaf width 20 1.0 (0.1) 0.7 (0.4) 14.59 0.001 Rh with C > Rh without C

Number of borers/shoot 50 0.3 (0.6) 0.8 (0.7) 16.11 0.001 Rh with C < Rh without C

F and p values of the one-way ANOVA analyses (n.s. = not significant), Rh = rhizome, C = Calpensia.

Fig. 2. (a) Trend of biomass and elongation ratio (B/E) in the time interval analysed (lepidochronological years) for rhizomes with and without C. nobilis overgrowth,

(b) trend of mean scale thickness (mm) measured for various lepidochronological years in rhizomes with and without the colonization of C. nobilis (bars represent

standard deviations), (c) trend of the mean number of intact scales in the various lepidochronological years for rhizomes with and without the colonization of C.

nobilis (bars represent standard deviations) and (d) trend of the mean scale production (mg/year) in the last four lepidochronological years for rhizomes with and

without the colonization of C. nobilis (bars represent standard deviations).

M. Cigliano et al. / Aquatic Botany 86 (2007) 30–3634

The external and internal structure of the circum-

encrusting layers revealed that the common zooid growth

direction was parallel to the direction of rhizome develop-

ment. Sometimes, a single muff was found to envelope two

rhizomes (Plate 1b).

The apical part of the muff, surrounding Posidonia leaves,

sometimes displayed an enlarged margin with the rim

oriented towards the internal part, probably as an adaptation

to the movement of the leaves. In contrast, the bryozoan

continued to produce superposed encrusting layers on dead

rhizomes, and the apical rims partially or completely merged.

Commonly, the number of layers forming the apical part of

the muff was lower than those produced at the base of the

rhizome.

The analysis of borers revealed the occurrence of three

species of polychaete Eunicidae Lysidice collaris (Grube) (27

specimens) and Lysidice ninetta (Audouin and Milne Edwards)

(21 specimens), and Nematonereis unicornis Schmarda (three

specimens).

Borer colonization was significantly higher (Table 1b) in the

rhizomes without C. nobilis (whole IB value = 49%, total of 38

specimens) than in those with the bryozoan (IB = 17%, total of

13 specimens). On the contrary, the index of the traces (IT) was

higher in rhizomes covered by C. nobilis (IT = 65%) than in

rhizomes free from the bryozoan (IT = 44%).

Rhizome production (mg/year) was significantly lower in

rhizomes with C. nobilis than in those not affected by the

bryozoan (Table 1b), while rhizome elongation (mm/year) did

not show significant differences among the two kind of shoots

(Table 1b). The B/E (biomass/elongation ratio) was therefore

lower in colonized rhizomes (Table 1b), and differences were

strongly evident, from the lepidochronological year 0 (2002) to

the year �10 (1992), with always lower ratios in colonized

rhizomes (Fig. 2a). In accordance, sheath thickness in the

rhizomes with the bryozoan was significantly lower (Fig. 2b)

than in those not covered. The mean values start to differ

sensibly in the lepidochronological year �4 (1998).

Both the number of intact sheaths and sheath production

(mg/year) were significantly higher (Tables 1a and 1b) in

rhizomes affected by C. nobilis than in unepiphytized rhizomes

(Fig. 2c and d). In particular, intact sheaths were present in

rhizomes overgrown by C. nobilis up to the lepidochronological

year �4, while these could be found in rhizomes without up to

year �2 (Fig. 2c). Sheath production also showed differences

due to bryozoan colonization, especially evident for the years

1998 (�4) and 1999 (�3) (Fig. 2d). Among the morphological

variables measured (number, age, length and width), only the

mean leaf width showed significant higher values in shoots

colonized by C. nobilis (1.0 � 0.1 mm) than in shoots free from

the bryozoan (0.7 � 0.4) (Table 1b).

For the living colonized rhizomes significant Spearman

coefficient’s values were observed between carbonate mass of

C. nobilis colonies and rhizome length (0.67; p = 0.001),

bryozoan length and rhizome length (0.63; p = 0.001), and

bryozoan length and B/E ratio (�0.31; p = 0.04), maximum

thickness of the muff and rhizome length (0.48; p = 0.01), as

well as B/E ratio (�0.43; p = 0.004).

4. Discussion

Although the eurytopic C. nobilis is commonly recorded

from a large variety of marine plants and hard substrates, it

occurs preferentially in high flow conditions such as those

recorded in the studied Posidonia meadow. In our site,

epiphytic colonies occupy all space available on rhizomes of

P. oceanica developing a multilayered, three-dimensional

architecture. Our data show an unusual, conspicuous coloniza-

tion of C. nobilis, in terms of muff length and biomass, not

recorded previously (Poluzzi and Coppa, 1991). This may be

related to the intense hydrodynamics that characterize the

studied area. The difference in frequency of the bryozoan

between the margin and the inner bed suggests more favourable

conditions at the margins. Here the current is probably stronger

than inside the meadow, where the leaf canopy reduces flow

speed and bottom friction (Gacia et al., 1999).

This massive epiphytism by C. nobilis on the rhizomes of P.

oceanica affects borer colonization, thus limiting borer

occurrence. The muff encrusting the rhizome represents a

physical barrier for these boring organisms, since the calcareous

exoskeleton of the bryozoan is hard to penetrate by the jaw

apparatus of the worms. In addition, bryozoan cover can reduce

oxygen penetration into the sheaths, thus exerting an eco-

physiological constraint for borers. These organisms are

therefore concentrated in the rhizomes free from C. nobilis,

with IB and IT indices higher than those recorded in other beds at

comparable depth and time (Gambi, 2002; Gambi et al., 2003b).

Values of rhizome production (as biomass and elongation),

both in shoots affected and not affected by the bryozoan

colonization, were higher than those recorded in other sites off

the Island of Ischia at comparable depth and environmental

conditions (Sferratore, 1997; Flagella et al., 2006). This can

again be an effect of the peculiar hydrodynamics experienced

by shoots at the studied meadow. The influence of C. nobilis

growth is evident in almost all the morpho-chronological

variables examined, especially for rhizome biomass, E/B ratio

and scale thickness, as well as for leaf width. Low values of

weight/length ratio in colonized shoots suggest that the plant

invests more energy in rhizome elongation than in biomass

production. Although the sheaths are thinner in colonized

shoots, the high sheath production (mg/year) is due to both the

high number of intact sheaths, protected by the muff, and to

their higher length. Leaf width, known to respond to local

environmental conditions, including stress and pollution

(Wittmann, 1984; Abbate et al., 2000), was higher in colonized

shoots than in free ones. Consequently, photosynthetic

performance may be enhanced to compensate for the lowered

rhizome production due to bryozoan load.

Our data are in agreement with findings by Romero

Colmenero and Sanchez Lizaso (1999), and the effect is similar

to that of enhanced sedimentation as illustrated by Di Carlo

et al. (2004), Gambi et al. (2005b), and Flagella et al. (2006).

No data are available on C. nobilis reproduction and growth

rate, so it is difficult to define the dynamic of the colonization

process. While we can hypothesize the larval dispersion as

responsible of medium and large scale colonization within the

M. Cigliano et al. / Aquatic Botany 86 (2007) 30–36 35

bed, as it is known for many cheilostomate bryozoans

(Hayward and Ryland, 1998), clonal growth of individual

colonies seems the main mechanism for contiguous shoot

colonization. In fact, two or more shoots were often embedded

in apparently the same muff. The age of the colonies settled on

the shoots, can be estimated indirectly from differences

between colonized and uncolonized rhizomes: these are

evident for the past 10 years, although more evident with

the B/E ratio for the past 4–5 years. This pattern suggests that

the colonization by the bryozoan is older than 5 years and lies

possibly between 5 and 10 years.

Finally we observed that all the morphometric variables of

bryozoan colonies sampled on dead rhizomes, but still in place

on the bottom, are higher than those measured on living ones,

indicating that bryozoan colonies may either grow directly on

dead rhizome, or may contribute to the death of the shoots and

continue to grow thereafter. We hypothesize that during the first

stage of construction muff thickening protects rhizomes from

being heavily scoured or buried by sediment. Subsequently, the

weight of the muff could cause rhizome death or detachment by

breakage enhanced by water movement, particularly for those

rhizomes made weaker by long-lasting periods of colonization.

On the other hand, the occurrence of many dead rhizomes of

different ages, lead to hypothesize that the bryozoan can also

settle on shoots already dead for other natural causes.

Our study illustrates an extreme case of epiphytism on

Posidonia, and shows that Posidonia shoots can react to heavy

colonization of Calpensia by changing its growth rate.

Although conspicuous epiphytes on Posidonia are numerous,

we are not aware of other species exerting a similar effect on the

rhizomes and on borer colonization, although this aspect has

still received little attention.

Acknowledgments

We wish to thank B. Iacono for support in SCUBA diving for

shoot sampling and shoot density measurements. M.C. Buia

and S. Flagella gave useful advice for shoot morpho-

chronological analysis and I. Guala for statistical analysis of

data. Carla Chimenz Gusso and Luisa Nicoletti kindly

confirmed the taxonomy of C. nobilis. An anonymous referee

and the Editor made constructive criticism.

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