Aquatic Botany 86 (2007) 30–36 www.elsevier.com/locate/aquabot
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, Italy b 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
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:
[email protected] (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 colonization 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 Sa`nchez 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 Sa`nchez 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;
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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
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located at 15–17 m depth in the Ischia Strait (between the islands of Ischia and Procida, Gulf of Naples, Italy) (latitude: 40844.7060 N and longitude: 13858.7600 E). This site experiences 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
Plate 1. (a) In situ picture showing some Posidonia oceanica shoots colonized by Calpensia nobilis colonies at the studied site, (b) some dead shoots of Posidonia colonized by C. nobilis, note that a single muff on the left is enveloping two rhizomes and (c) a dead rhizome with the apical growing rims completely merged.
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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 = percentage 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 lepidochronology (Crouzet et al., 1983). This technique, widely used in P. oceanica (Pergent and Pergent-Martini, 1991; PergentMartini 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, ‘intermediate’ = 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 lepidochronological 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
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).
number, and the external and internal structure of circumencrusting layers forming each muff was counted and analysed at the microscope. To assess the relationship among morphometric 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.
Table 1a Some morphometric features of Calpensia nobilis constructions overgrowing living and dead rhizomes of Posidonia oceanica
Living rhizomes (n = 28) Dead rhizomes (n = 41)
Carbonate mass (g d.w.)
Length (mm)
Maximum thickness (mm)
Maximum number of layers
8.3 11.9 35.6 25.2
90.9 43.7 127.9 40.5
3.17 1.42 8.34 4.68
– 12.5 5.5
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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
Rhizome biomass (mg/year) Rhizome elongation (mm/year) B/E (biomass/elongation) Number of sheaths/year Mean sheath thickness (mm) Number of intact sheaths Sheath production (mg/year) Number of leaf/year Mean leaf length Mean leaf width Number of borers/shoot
Number of shoots examined
Shoots with Calpensia
Shoots without Calpensia
F-values
p
40 40 40 40 40 40 40 20 20 20 50
83.7 (32.7) 12.9 (6.0) 6.3 (1.5) 7.0 (0.6) 0.25 (0.07) 4.7 (1.2) 255.9 (10.2) 4.8 (1.3) 40.8 (28.3) 1.0 (0.1) 0.3 (0.6)
95.3 11.3 8.3 7.2 0.3 2.2 212.6 5.4 44.5 0.7 0.8
6.40 1.30 14.93 0.02 63.76 45.29 11.17 1.92 0.19 14.59 16.11
0.05 n.s. 0.001 n.s. 0.001 0.001 0.01 n.s. n.s. 0.001 0.001
(37.3) (4.5) (1.4) (0.6) (0.04) (2.0) (61.3) (1.7) (30.8) (0.4) (0.7)
Rh with C < Rh without C Rh with C < Rh without C Rh with C < Rh without C Rh with C > Rh without C Rh with C > Rh without C
Rh with C > Rh without C 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).
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The external and internal structure of the circumencrusting layers revealed that the common zooid growth direction was parallel to the direction of rhizome development. 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 colonization 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 ecophysiological 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 Sa`nchez 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
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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 morphochronological 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. References Abbate, M., Peirano, N., Ugolini, U., 2000. Structural changes in Posidonia oceanica leaves along the coast of Liguria (Italy): responses to environmental stress. In: Pergent, G., Pergent-Martini, C., Buia, M.C., Gambi, M.C. (Eds.), Proceedings of the 4th International Seagrass Biology Workshop, Corsica, September 2000, Biol. Mar. Medit. 7 (2), 320–323. Buia, M.C., Gambi, M.C., Dappiano, M., 2004. Seagrass ecosystems. In: Gambi, M.C., Dappiano, M., (Eds.), Mediterranean Marine Benthos: A Manual for its Sampling and Study. Biol. Mar. Medit. 11 (Suppl. 1), 133–183. Crouzet, A., Boudouresque, C.F., Meinesz, A., Pergent, G., 1983. Evidence of the annual character of cyclic changes of Posidonia oceanica scale thickness (erect rhizomes). Rapp. Comm. Int. Mer. Medit. 28, 113–114. De Maio, A., Moretti, M., Sansone, E., Spezie, G., Vultaggio, M., 1983. Dinamica delle acque del Golfo di Napoli e adiacenze. Risultati ottenuti
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