Sizefrequency Distributions of Joania Cordata and Argyrotheca Cuneata

Marine Ecology. ISSN 0173-9565

ORIGINAL ARTICLE Size-frequency distributions of Joania cordata and Argyrotheca cuneata (Brachiopoda: Megathyrididae) from the Central Tyrrhenian Sea Francesca Evangelisti, Paolo G. Albano & Bruno Sabelli

Department of Biological, Geological and Environmental Sciences, University of Bologna, Bologna, Italy

Keywords Abstract Argyrotheca cuneata; Brachiopoda; Joania cordata; Recent brachiopods; Secche di Tor Size-frequency distributions can support reliable inferences concerning popula- Paterno; size-frequency distributions. tion dynamics of brachiopods, but only a few data are available so far. In this study, length and width frequency distributions of dead specimens of the Correspondence Recent brachiopods Joania cordata and Argyrotheca cuneata from the Marine Francesca Evangelisti, Department of Protected Area ‘Secche di Tor Paterno’, Central Tyrrhenian Sea, Italy Biological, Geological and Environmental (41°35′ N, 12°20′ E), are reported in order to add new data about size- Sciences, University of Bologna, Via Selmi 3, frequency distributions of brachiopods. The studied specimens came from 40126, Bologna, Italy. E-mail: [email protected] death assemblages in the coralligenous substrate, in the Posidonia oceanica meadows, and in the sand channels. The observed patterns vary from left- Accepted: 11 July 2013 skewed (J. cordata) to right-skewed (A. cuneata), indicating respectively a low and high mortality of smaller individuals. Signiﬁcant differences between the doi: 10.1111/maec.12096 coralligenous substrate and the P. oceanica meadow were observed for both species, revealing a variation among different habitats. All length and width distributions are clearly polymodal, but the biological meaning of the peaks is difﬁcult to interpret, as the two species seem to have a 2-year life span. A biometric analysis of shell sizes revealed that length and width are the most variable parameters during the growth of the animal.

Bambach 1975; Cadee 1982) and taphonomic processes Introduction (Emig 1990; Simoes~ et al. 2005; Tomasovych & Rothfus Size-frequency distributions (SFDs) have been largely 2005). Also, predation can inﬂuence SFDs of brachiopods used as a tool in the study of population dynamics of as predators often choose their prey by size, and preda- both fossil (e.g. Cadee 1982; Alvarez 1986, 1990; Bitner & tion pressure on both recent and fossil brachiopods can Pisera 2000; Bitner 2002; Tomasovych 2004) and present- be appreciable (e.g. Evangelisti et al. 2011; Harper 2011). day brachiopods (e.g. Thayer 1975, 1977; Noble & Logan However, growth and mortality rates are the main prob- 1981; Curry 1982; Taddei Ruggiero 1987; Brey et al. lems because their assessment depends on age determina- 1995). Published works showed that distributions patterns tion and there is no convenient way to estimate the age are mainly bi- or polymodal and that the most common of brachiopods. A direct relationship between size and type of population size-structure is a right-skewed one age cannot be the rule because individuals of the same (e.g. Taddei Ruggiero 1987; Bitner 2002), with only a few age may reach different sizes (Thayer 1977), and there cases of left-skewed SFDs (Thayer 1975; Brey et al. 1995). may also be size variations be due to different local envi- Nevertheless, inferences about population dynamics of ronmental conditions, geographic locations or habitats brachiopods by SFDs may provide ambiguous interpre- (e.g. Thayer 1977; Aldridge 1981). Variations in the size tations as size-frequency graphs can be biased by several of living brachiopods have been recently observed factors, such as inadequate sampling (Richards & with latitude and depth (Peck & Harper 2010). Another

Marine Ecology 35 (2014) 377–386 ª 2013 Blackwell Verlag GmbH 377 Size-frequency distributions of J. cordata and A. cuneata Evangelisti, Albano & Sabelli possibility is the estimation of age estimation from bands located 12 km off the coast of Lazio, Italy (41°35′ N, on the shell surface. In a study about population dynam- 12°20′ E), and it covers a total surface of 27 hectares. ics of a dense assemblage of Magellania fragilis from the The top of the reef is at –18 m, and the reef lies on the shelf of the Lazarev sea, Antarctica (Brey et al. 1995), the surrounding mud bottom at a depth of ~70 m. The area bands on the shell surface were interpreted as annual is characterized by two primary habitats typical of the growth marks and treated as size-at-age data. Following Mediterranean Sea: the coralligenous substrate composed this method, other authors published works on living of the accumulation of encrusting algae, and small brachiopods (Peck et al. 1997; Park et al. 2000). Never- meadows formed by the endemic Mediterranean seagrass theless, there is no tangible proof that the bands visible Posidonia oceanica. on the shell surface have been formed seasonally and, Several samples were collected at depths of 20–28 m by moreover, extra, non-annual growth lines can be pro- SCUBA divers through airlift suction samplers, which duced, at least in some species, as reported for Terebratal- were used on the coralligenous substrate, on the rhizome ia transversa (Paine 1969). The best way to define age layer of P. oceanica and in the sand channels, providing would be by recurring observations of the same popula- specimens from the three different death assemblages. tions in their life environment over a period of several The samples were sieved with meshes down to 1 mm, years, used in the techniques of staining and radiography and all retrieved brachiopods were identified, counted in corals, but difficulties in sampling the same site, as and measured using an ocular micrometer. All three well as potential modifications due to human intrusions, dimensions of the shell were recorded as defined by have to be taken into account as possible limitations Williams & Brunton (1997), so that length and width (Tunnicliffe & Wilson 1988; Asgaard & Bromley 1990; were those of the ventral valve, which is usually the Taddei Ruggiero 2001). In some cases, analyses were per- largest one. formed on populations kept alive in the laboratory (e.g. A biometric analysis was carried out on the two species Thayer 1975; Curry 1982; Collins 1991) but the results to investigate their variability, and all three dimensions of can be inaccurate, as reproducing natural life conditions the shell were taken into account. Data were put in artificially is difficult or often impossible. length-width and thickness-width scatter diagrams, which In this study we have investigated the SFDs of two were performed on each kind of sample separately. Recent brachiopods, Joania cordata and Argyrotheca cune- Spearman rank correlations and linear regressions were ata, in order to add new data about SFDs of brachiopods. computed for each scatter diagram to determine the rela- The two species are micromorphic brachiopods living in tionship among the variables. For each species, an analy- shallow waters, attached to cave walls and roofs, boulders sis of covariance (ANCOVA) was also performed to and coralligenous substrate (Logan 1979; Logan et al. highlight possible differences in length-width and thick- 2004; Alvarez et al. 2005, 2008). Their morphology is ness-width relationship among the three analysed sam- illustrated in these publications. The analysis was carried ples. All statistical analyses were performed using the out on samples from the Marine Protected Area ‘Secche program R (R Development Core Team 2008). di Tor Paterno’, Central Tyrrhenian Sea, as part of the Length and width frequency distributions were also biodiversity study of the area (Albano & Sabelli 2011; performed to analyse their variation within and between Evangelisti et al. 2011, 2012). The distributions were the two species. Thickness was not considered because no examined for the two species separately and, within each significant variation among specimens was observed for species, for the three different death assemblages which either species. Histograms were performed for both spe- the specimens came from: within the coralligenous sub- cies, for each kind of sample separately. For each distri- strate, within a Posidonia oceanica meadow, and from bution, a Shapiro–Wilks test and Skewness index were sand channels containing specimens originated from the computed to investigate shape. For each species, length nearby coralligenous substrate and Posidonia meadows. and width frequency distributions of the three samples The outcome was then compared with data from the lit- were compared in their shape and mean values using erature. This is the first study on size-frequency distribu- respectively the Kolmogorov–Smirnov (D) and Mann– tions on Recent specimens of J. cordata and A. cuneata. Whitney (U) tests, to highlight possible differences among the death assemblages of the coralligenous substrate, the P. oceanica meadow and the death assemblages Material and Methods in the sand channels. Both tests were computed with the Samples of empty shells of Joania cordata and Argyrotheca program PAST (Hammer et al. 2001). A level of 5% was cuneata were collected from the Marine Protected Area considered significant for all statistical analyses. The stud- ‘Secche di Tor Paterno’, Central Tyrrhenian Sea, from ied material is kept in the Zoological Museum of the May to June 2007. The area is a completely off-shore reef University of Bologna, Italy.

378 Marine Ecology 35 (2014) 377–386 ª 2013 Blackwell Verlag GmbH Evangelisti, Albano & Sabelli Size-frequency distributions of J. cordata and A. cuneata

the coralligenous substrate offered a reasonable number of Results specimens but the number was much lower than the sand The analysis was carried out on 1071 complete dead speci- channels (103 J. cordata and 90 A. cuneata). mens, 631 Joania cordata and 440 Argyrotheca cuneata. Length, width and thickness values of the smallest and Most specimens came from the samples collected in the largest specimens of both species are given in Table 1. sand channels (455 J. cordata and 330 A. cuneata); the Pos- For both species, no individuals less than 1.0 mm in size idonia oceanica meadow gave only a small amount of mate- were observed because material was passed through a 1.0- rial (73 J. cordata and 20 A. cuneata). Samples collected in mm sieve. Biometric analysis revealed identical results for both species and, within each species, for all three analysed Table 1. Minimum and maximum size values for dead Joania cordata and Argyrotheca cuneata. samples. There was a signiﬁcant positive correlation between length and width and between thickness and Joania cordata Argyrotheca cuneata width (Fig. 1: J. cordata, and Fig. 2: A. cuneata), with rs Size Min (mm) Max (mm) Min (mm) Max (mm) values ranging from 0.75 to 0.95 for J. cordata and from 0.78 to 0.92 for A. cuneata (Table 2). In all cases the Length 1.0 3.5 1.0 3.7 greatest length and thickness percent variance was in Width 1.0 3.5 1.3 3.8 width, with r² values ranging from 0.29 to 0.91 for J. cor- Thickness 0.3 0.5 0.5 1.9 data and from 0.57 to 0.86 for A. cuneata (Table 2). Min, minimum value; Max, maximum value. Length-width and thickness-width scatter diagrams of

Fig. 1. Length-width and thickness-width scattergrams for dead Joania cordata in the coralligenous substrate, n = 103 (A,B), Posidonia oceanica meadows, n = 73 (C,D) and the sand channels, n = 455 (E,F).

Marine Ecology 35 (2014) 377–386 ª 2013 Blackwell Verlag GmbH 379 Size-frequency distributions of J. cordata and A. cuneata Evangelisti, Albano & Sabelli

Fig. 2. Length-width and thickness-width scattergrams for dead Argyrotheca cuneata in the coralligenous substrate, n = 90 (A,B), the Posidonia oceanica meadows, n = 20 (C,D), and the sand channels, n = 330 (E,F).

Table 2. Correlation and linear regression data for length-width and thickness-width scattergrams for dead Joania cordata and Argyrotheca cuneata in the coralligenous substrate, the Posidonia oceanica meadows and the sand channels.

2 Species Samples Variables Regression lines rs nP r FdfP

Joania cordata Coralligenous substrate Length-width y = 0.9798x + 0.0934 0.95 103 <0.0001 0.91 1066.00 1,102 <0.0001 Thickness-width y = 0.3649x + 0.0381 0.88 103 <0.0001 0.78 370.30 1,102 <0.0001 Posidonia oceanica Length-width y = 0.8739x + 0.3744 0.86 73 <0.0001 0.70 187.30 1,72 <0.0001 meadows Thickness-width y = 0.2618x + 0.3187 0.75 73 <0.0001 0.29 31.96 1,72 <0.0001 Sand channels Length-width y = 0.9417x + 0.1839 0.89 455 <0.0001 0.81 2477.00 1,454 <0.0001 Thickness-width y = 0.3573x + 0.0849 0.75 455 <0.0001 0.59 824.60 1,454 <0.0001 Argyrotheca Coralligenous substrate Length-width y = 0.8205x + 0.1339 0.81 90 <0.0001 0.66 183.40 1,89 <0.0001 cuneata Thickness-width y = 0.5075x À 0.1502 0.89 90 <0.0001 0.76 297.70 1,89 <0.0001 Posidonia oceanica Length-width y = 0.8791x + 0.1108 0.86 20 <0.0001 0.78 65.51 1,19 <0.0001 meadows Thickness-width y = 0.7838x À 0.735 0.92 20 <0.0001 0.86 118.20 1,19 <0.0001 Sand channels Length-width y = 0.6625x + 0.5095 0.78 330 <0.0001 0.57 489.40 1,366 <0.0001 Thickness-width y = 0.5709x À 0.2625 0.84 330 <0.0001 0.64 664.00 1,366 <0.0001 rs, Spearman rank correlation coefﬁcient; n, sample size; r², coefﬁcient of determination; F, Fisher’s F-test; df, degrees of freedom; P, P-values.

J. cordata showed a different linear trend, the two lines low slope values (Fig. 1). Length-width and thickness- having different slope values. The length-width lines had width scatter diagrams of A. cuneata were very similar to high slope values, whereas the thickness-width lines had the ones of J. cordata, the slope of length-width lines

380 Marine Ecology 35 (2014) 377–386 ª 2013 Blackwell Verlag GmbH Evangelisti, Albano & Sabelli Size-frequency distributions of J. cordata and A. cuneata

Table 3. ANCOVA results for length-width and thickness-width data for dead Joania cordata and Argyrotheca cuneata, obtained from comparisons among the coralligenous substrate, the Posidonia oceanica meadows and the sand channels.

Species Variables Differences F df P

Joania cordata Length-width Slope differences 2.80 2,732 0.3920 Y mean value differences 2.80 2,734 0.4531 Thickness-width Slope differences 1.30 2,732 0.4431 Y mean value differences 3.00 2,734 0.5433 Argyrotheca cuneata Length-width Slope differences 1.42 2,475 0.1291 Y mean value differences 2.50 2,477 0.2440 Thickness-width Slope differences 0.37 2,574 0.3851 Y mean value differences 1.10 2,477 0.3660

F, Fisher’s F-test; df, degrees of freedom; P, P-value.

Fig. 3. Length and width frequency distributions for dead Joania cordata in the coralligenous substrate, n =103 (A,B), the Posidonia oceanica meadows, n = 73 (C,D), and the sand channels, n = 455 (E,F).

Marine Ecology 35 (2014) 377–386 ª 2013 Blackwell Verlag GmbH 381 Size-frequency distributions of J. cordata and A. cuneata Evangelisti, Albano & Sabelli being higher than the slope of thickness-width lines peak at 3.0 mm suggests a unimodal pattern, but poly- (Fig. 2). Nevertheless, the slope values of length-width modality cannot be totally excluded. The width histo- lines for A. cuneata were lower than those of J. cordata, gram presented a very high peak at 2.7 mm. Other whereas the slope values of thickness-width lines were peaks were evident but they were definitely lower. The higher. For both species, there were no significant differ- great difference in frequency values between these peaks ences among length-width and thickness-width regression and the highest peak was more evident than the one lines of the three analysed samples (ANCOVA, Table 3), reported for the length histogram. Therefore the width- indicating that there were no significant differences in frequency distribution may be considered unimodal. In growth shell among them. the assemblage from the sand samples, the length and Analysis of SFDs revealed that the two species showed width frequency distributions displayed clearly the pres- opposite skews. Length and width frequency distributions ence of two distinct significant peaks at 2.5 mm (the of J. cordata from the coralligenous substrate, the P. ocea- highest peak) and 2.0 mm, but other well defined high- nica meadow and the sand channels, were skewed to the frequency-length classes were distinguishable. This sug- left, indicating that larger individuals were dominant in gests a bimodal or, more likely, a polymodal pattern. all the three samples (Fig. 3, Table 4). Conversely, length Pairwise comparisons among the coralligenous substrate, and width frequency distributions of A. cuneata from the the P. oceanica meadows and the sand channels, demon- coralligenous substrate, the P. oceanica meadow and the strated significant differences between length-frequency sand channels were skewed to the right, indicating that and width-frequency distributions, both in shape and smaller individuals were dominant in all the three distinct mean values (Table 5). samples (Fig. 4, Table 4). This suggests a low mortality of The length-frequency histogram of A. cuneata from the smaller individuals for J. cordata, which enables the bra- coralligenous sample (Fig. 4) showed clearly the presence chiopods to reach a larger size, and a high mortality of of two distinct significant peaks, the first at 1.7 mm (the smaller individuals for A. cuneata, which prevents the highest peak) and the second, less consistent, at 2.3 mm. brachiopods from reaching a larger size. This indicates clearly a bimodal pattern. The width histo- Length and width frequency histograms of J. cordata gram had four distinct significant peaks, the first at from the coralligenous substrate (Fig. 3) showed clearly 2.0 mm (the highest peak), the second, weaker, at the presence of two distinct major peaks, respectively at 2.3 mm, and the third and fourth, weaker and with the 2.2 and 2.5 mm, and at 2.5 and 2.7 mm, but other same frequency values, respectively at 2.6 and 2.7 mm. weaker peaks were also evident. This represents a bimo- This may indicate a trimodal pattern. In the assemblage dal pattern, with a possible polymodality. The assem- from the P. oceanica meadows, the length histogram blage from the P. oceanica meadows was characterized showed clearly four peaks, at 1.8, 2.1, 2.3 and 2.7 mm, by a length-frequency distribution with a clear higher and the width histogram showed three (2.0, 2.3 and peak at 3.0 mm, but other, though less evident, peaks 2.6 mm) or six peaks (the additional peaks were at 1.8, were distinguishable. The high frequency value of the 2.2 and 3.0 mm). This indicates a polymodal pattern.

Table 4. Statistical data for length and width frequency distributions for dead Joania cordata and Argyrotheca cuneata in the coralligenous substrate, the Posidonia oceanica meadows and the sand channels.

Min Max Species Size Sample n (mm) (mm) Χ Æ SD W P SKEW P

Joania cordata Length Coralligenous substrate 104 1.0 3.4 2.24 Æ 0.54 0.97 0.0076 À0.29 0.0049 Posidonia oceanica meadows 80 1.3 3.5 2.53 Æ 0.46 0.97 0.038 À0.41 0.015 Sand channels 554 1.0 3.5 2.40 Æ 0.42 0.98 0.0002 À0.29 0.0315 Width Coralligenous substrate 104 1.0 3.2 2.19 Æ 0.53 0.94 0.0004 À0.47 0.0421 Posidonia oceanica meadows 80 1.1 3.5 2.47 Æ 0.44 0.95 0.0082 À0.76 0.0349 Sand channels 554 1.2 3.4 2.35 Æ 0.40 0.98 0.0005 À0.39 0.0112 Argyrotheca cuneata Length Coralligenous substrate 93 1.2 3.1 1.92 Æ 0.40 0.93 0.0002 0.75 0.0283 Posidonia oceanica meadows 20 1.6 3.3 2.22 Æ 0.42 0.94 0.0341 0.71 0.0157 Sand channels 368 1.0 3.7 2.12 Æ 0.36 0.98 <0.0001 0.360 0.0327 Width Coralligenous substrate 93 1.3 3.2 2.18 Æ 0.40 0.97 0.0493 0.14 0.0342 Posidonia oceanica meadows 20 1.8 3.4 2.40 Æ 0.42 0.95 0.0421 0.56 0.0208 Sand channels 368 1.3 3.8 2.43 Æ 0.41 0.98 0.0005 0.20 0.0148 n, sample size; Min, minimum value; Max, maximum value; Χ, mean; SD, standard deviation; W, Shapiro–Wilks; SKEW, skewness; P, P-values.

382 Marine Ecology 35 (2014) 377–386 ª 2013 Blackwell Verlag GmbH Evangelisti, Albano & Sabelli Size-frequency distributions of J. cordata and A. cuneata

Fig. 4. Length and width frequency distributions for dead Argyrotheca cuneata in the coralligenous substrate, n = 90 (A,B), the Posidonia oceanica meadows, n = 20 (C,D), and the sand channels, n = 330 (E,F).

Table 5. Kolmogorov–Smirnov and Mann–Whitney values for length and width frequencies distributions for dead Joania cordata and Argyrotheca cuneata, obtained from the comparisons among the coralligenous substrate, the Posidonia oceanica meadows and the sand channels.

Species Size Samples KS (D) P MW (U)n1 n2 P

Joania cordata Length C-PM 0.22 0.0130 2869.00 103 73 0.0002 C-S 0.21 0.0004 2.42 103 455 0.0099 PM-S 0.17 0.0220 1.81 73 455 0.0081 Width C-PM 0.23 0.0098 2932.00 103 73 0.0007 C-S 0.20 0.0011 2.49 103 455 0.0246 PM-S 0.18 0.0120 1.79 73 455 0.0063 Argyrotheca cuneata Length C-PM 0.37 0.0130 552.50 90 20 0.0033 C-S 0.38 <0.0001 1.153 90 330 <0.0001 PM-S 0.18 0.5010 3250 20 330 0.3821 Width C-PM 0.23 0.2009 673.00 90 20 0.0504 C-S 0.29 <0.0001 1.15 90 330 <0.0001 PM-S 0.20 0.3792 3447.00 20 330 0.6476

C, coralligenous substrate; PM, Posidonia oceanica meadows; S, sand channels; KS, Kolmogorov–Smirnov value; MW, Mann-Whitney value; N, sample size; P, P-values.

Marine Ecology 35 (2014) 377–386 ª 2013 Blackwell Verlag GmbH 383 Size-frequency distributions of J. cordata and A. cuneata Evangelisti, Albano & Sabelli

The assemblage from the sand channels showed a length- with respect to the longer ones is more pronounced in frequency distribution with an evident high peak at A. cuneata than in J. cordata, so that in A. cuneata, width 2.0 mm; however, other peaks, possibly four, were distin- is more variable. No significant differences in thickness guishable; this indicates a unimodal or polymodal pat- were evident between the smallest and the largest individ- tern. The width-frequency distribution displayed clearly uals of J. cordata, indicating that thickness remains sub- the presence of four distinct significant peaks at 2.0, 2.3, stantially constant during its growth. In contrast, in 2.4 and 2.7 mm. However, other well-defined high- A. cuneata, the predominance of wider individuals with frequency-length classes were distinguishable. This sug- respect to the thickest ones is less evident, suggesting gests a polymodal pattern with at least four modes. that thickness is more variable than this species than in Pairwise comparisons among the coralligenous substrate, J. cordata. For both species, the lack of any significant the P. oceanica meadows and the sand channels, demon- difference between the coralligenous substrate and the strated significant shape and mean value differences of P. oceanica meadows indicates that no particular environ- the length-frequency distributions between the coralligen- mental factors or substrate characteristics influencing the ous substrate and the P. oceanica meadows, and between growth of the shell, occur in these habitats. the coralligenous substrate and the sand channels, but no The low mortality of smaller individuals observed for significant different shapes and mean values were J. cordata may be related to its environment. Both the observed between the P. oceanica meadows and the sand coralligenous substrate and the P. oceanica meadows offer channels (Table 5). Width-frequency distributions were cryptic and protected habitats where small brachiopods significantly different in shape and mean value between can easily find suitable attachment surfaces. In addition, the coralligenous and the sand samples, whereas no sig- small brachiopods in these microhabitats are less vulnera- nificant differences were present between the coralligen- ble to burial by organic detritus or suspended particles, ous substrate and the P. oceanica meadows, or between avoiding clogging effects on the lophophore. However, the sand channels and the P. oceanica meadows. predation events may be another possible cause of the low mortality of smaller individuals of J. cordata.Ina recent study on predatory holes found in some of the Discussion specimens of J. cordata and A. cuneata analysed here For Joania cordata a relatively high percentage of larger (Evangelisti et al. 2012), a size preference of predators for individuals were found in both the coralligenous substrate individuals having length values >1.9 mm was found for and the Posidonia oceanica meadows, which indicates J. cordata. This means that larger individuals were preyed these may both be suitable environments for the growth upon more frequently, whereas smaller individuals were of this species. This may be due to the richness of cryptic less affected by predation. habitats present in the rhizome layer of P. oceanica,as The high mortality of smaller individuals found for well as in the coralligenous substrate. Conversely, Argyrot- A. cuneata is difficult to interpret as A. cuneata has the heca cuneata was poorly represented in the P. oceanica same life environment of J. cordata. Besides, it is known meadows, which may imply that the species has greater that SFDs with a high mortality of smaller individuals difficulty surviving in the rhizome environment. Indeed, represent species which normally inhabit muddy bottoms, the rhizomes and the coralline algae and other epiphytes where hard substrates for attachment are often scarce, living on them provide a hard, dark substrate rich in and where the frequently agitated layer of particles and cryptic micro-habitats, potentially hosting these species. organic detritus suspended in the water constantly threa- However, it is important to highlight that, for both spe- ten small brachiopods by clogging their lophophores. cies, data from samples on the coralligenous substrate However, again, predation events can provide a possible may be considered the closest match to the living popula- answer. Contrary to J. cordata, 1.5–2.5-mm specimens of tion, because the substrate represents the typical habitat A. cuneata were preyed on more often (Evangelisti et al. of these brachiopods in the Mediterranean Sea (Logan 2012). 1979; Logan et al. 2004). The polymodality observed for J. cordata and A. cune- The biometric analysis performed on the two species ata is consistent with the observations reported by other highlights that the parameters which most determine the authors, who suggested that the frequency distributions growth of the shell during the growth of the animal are of brachiopods are mainly bi- or polymodal (e.g. Thayer width and length, with the former reaching greater values, 1975, 1977; Curry 1982; Taddei Ruggiero 1985, 1987; whereas the thickness increasing very little. This means Bitner 2002). It is difficult to determine the biological that the largest individuals are the ones with major width meaning of the multiple peaks, as the most likely hypoth- and length values, with an evident predominance of the esis – that this represents different age classes, correlated widest specimens. The predominance of wider individuals to seasons or years of life – is not supported by the

384 Marine Ecology 35 (2014) 377–386 ª 2013 Blackwell Verlag GmbH Evangelisti, Albano & Sabelli Size-frequency distributions of J. cordata and A. cuneata conclusions of Asgaard & Bromley (1990), who assessed References J. cordata and A. cuneata as having a 2-year life span. For J. cordata, the significant differences in shape and Albano P.G., Sabelli B. (2011) Comparison between death and mean values among the pairwise length- and width- living mollusks assemblages in a Mediterranean infralittoral frequency distributions of the coralligenous substrate and off-shore reef. Palaeogeography Palaeoclimatology 310 – the P. oceanica meadows, indicate variation in different Palaeoecology, , 206 215. habitats, confirming that the population structure of bra- Aldridge A.E. (1981) Intraspecific variation of shape and size chiopods can be distinct in different life environments in subtidal populations of two Recent New Zealand 8 (e.g. Bitner 2002). articulate brachiopods. New Zealand Journal of Zoology, , 169–174. The data reported here were compared with similar Alvarez F. (1986) Population structure of three species of data on J. cordata and A. cuneata from fossil assemblages, the genus Plicathyris (Brachiopoda: Athyridacea) from the as no studies about SFDs on Recent communities of the Devonian of the Cantabrian Zone (NW Spain) and two species have been made so far. Bitner (2002) analysed their significance. Biostratigraphie du Paleozoique, 4, Miocene brachiopod assemblages in reef environments 167–177. and gave data on J. cordata and A. cuneata. Bitner’s data Alvarez F. (1990) Devonian athyrid brachiopods from the are compared here with samples from the sand channels Cantabrian Zone (NW Spain). Biostratigraphie du only, as they are considered the most similar to a fossil Paleozoique, 11, 311. assemblage. In addition, only the length-frequency distri- Alvarez F., Martinez A., Nunez~ L., Nunez~ J. (2005) Sobre la butions were compared, as they were the only ones per- presencia en Canarias de varias especies de braquiopodos formed by Bitner. For J. cordata and A. cuneata, Bitner (Brachiopoda: Rhynchonellata) en cuevas y cornisas reported length-frequency distributions varying from submarinas. Vieraea, 33, 261–279. right-skewed to bell-shaped with several intermediates; no Alvarez F., Brunton C.H.C., Long S.L. (2008) Loop left-skewed distributions were observed. Thus, the skew- ultrastructure and development in Recent Megathirioidea, ness to the right of A. cuneata is consistent with Bitner’s with description of a new genus, Joania (type species results, but not the skewness to left of J. cordata. This Terebratula cordata Risso, 1826). Earth and Environmental confirms that, although some brachiopods have right- Sciences Transactions of the Royal Society of Edinburgh, 98, skewed size-frequency distributions, others do not, as 391–403. 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Department of Evolutionary Experimental Biology, Uni- Curry G.B. (1982) Ecology and population structure of the versity of Bologna, who kindly provided useful sugges- recent brachiopod Terebratulina from Scotland. tions for all statistical analyses. Michela Kuan, Maria Palaeontology, 25, 227–246. Teresa Greco, Linda Tragni and Francesca Orru helped Emig C.C. (1990) Examples of post-mortality alteration in with the sample sorting. None of the authors have any recent brachiopod shells and (palaeo) ecological 104 – potential conflicts of interest. consequences. Marine Biology, , 233 238.

Marine Ecology 35 (2014) 377–386 ª 2013 Blackwell Verlag GmbH 385 Size-frequency distributions of J. cordata and A. cuneata Evangelisti, Albano & Sabelli

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