Numerical taxonomy of some taxa of the genus - Springer Link

Hydrobiologia 260/261: 81-90, 1993. A. R. O. Chapman, M. T. Brown & M. Lahaye (eds), Fourteenth InternationalSeaweed Symposium. © 1993 Kluwer Academic Publishers. Printedin Belgium.

81

Numerical taxonomy of some taxa of the genus Fucus in the Iberian Peninsula Isabel PNrez-Ruzafa, Tomrs Gallardo & Rosario G6mez-Cancio Dept. Biologia Vegetal I. Fac. Biologia, Univ. Complutense, E-28040 Madrid, Spain

Key words: Fucus, numerical taxonomy, marine algae, Spain, Portugal

Abstract A study of morphological variation patterns in three Iberian Fucus species has been carried out. Data on 36 features from 113 specimens have been studied by numerical methods (PCA, discriminant analysis and ANOVA). The PCA ordination displayed a continuous trend of variation in the following Fucus species: F. ceranoides, F. vesiculosus and F. spiralis. However, no obvious morphological discontinuities have been observed. In addition, three varieties of F. spiralis and five of F. vesiculosus have been identified. At the varietal level discriminant functions could be used for identifying 93-100% of the individuals within F. vesiculosus and 72-91 o of F. spiralis. The most discriminating diagnostic character appeared to be the midrib size, as detected by ANOVA procedures. Some qualitative characters, such as presence of vesicles, dioecious-monoecious character and receptacle edge shape, frond and receptacle shape, have been also important for discriminating specific and infraspecific taxa. A nomenclatural discussion of varietal taxa is also included.

Introduction The genus Fucus is widely represented in Iberian Peninsula. It grows along the Atlantic coast and reaches Malaga inside the Mediterranean. Since this genus is very variable morphologically, a great number of specific and subspecific taxa has been described. Powell (1963) has assigned 100 such taxa to the six currently accepted species, i. e., F. distichus L., F. spiralis L., F. virsoides J. Agardh, F. vesiculosus L., F. ceranoides L., and F. serratus L. More recently, Rice & Chapman (1985) have assigned some subspecies ofF. distichus L. to two different species, namely, F. distichus L. and F. e-

vanescens C. Agardh. Wynne & Magne (1991) have proposed F. cottonii Wynne et Magne, as a new combination to include plants formerly named F. muscoides (Cotton) J. Feldm.; in their opinion, this species is taxonomically defensible on both ecological and morphological grounds. As infraspecific taxa, Powell (1963) has recognized the forms platycarpus (Thur.) Powell, spiralis, and nanus (Stackhouse) Boergesen for F. spiralis, and considered the latter form as a synonym of F. spiralis f. limitaneus (Montagne) Boergesen; Powell has suggested that the form dichotomus (= F. dichotomus Sauvageau) is intermediate between spiralis and nanus. F. vesiculosus also shows high morphological

82 Table 1. List of Fucus specimens used in this study giving their location (UTM coordinates) and autoecology in Iberian coasts. Taxa

Location

Autoecology

Fucus spiralis var. spiralis

Cabo Higuer, 30TWP90; Zarauz, 30TWP90; Castro Urdiales, 30TVP80; Punta Sonabia, 30TVP80; S. Pedro del Mar, 30TVP21; Comillas, 30TUP90; Playa de Pech6n, 30TUP80; Celorio, 30TUP51; Villaviciosa, 30TUP02; Puerto de Vega, 29TPJ92; Sada, 29TNH60; Viana do Castelo, 29TNG 11; Tarifa, 30STE68; Punta Carnero, 30STE89; Cala Burras 30SUF03.

Upper littoral, rocky substratum, semiexposed and sheltered, marine salinity.

Fucus spiralis var. platycarpus

Cabo Higuer, 30TWP90; Zarauz, 30TWP90; Castro Urdiales, 30TVP80; S. Pedro del Mar, 30TVP21; Ria de Suances, 30TVP11; Celorio, 30TUP51; Puerto de Vega, 29TPJ92; Sada, 29TNH69; Castelo do Queijo, 29TNF25.

Upper littoral, rocky substratum, semiexposed, marine salinity

Fucus spiralisvar. nana

Cabo Higuer, 30TWP90; Cabo Trafalgar, 29SQA60; Cabo de Plata, 30STE49; Bolonia, 30STE59; Tarifa, 30STE68.

Upper littoral, rocky substratum, exposed, marine salinity.

Fucus vesiculosus var. vesiculosus

Ria de Guernica, 30TWP20; Playa de Navia Sada, 29TNH69; Ramallosa, 29TPJ82; 29TNG16; Viana do Castelo, 29TNGl1; Figueira da Foz, 29TNE14; Torre de Belem, 29SMC88.

Middle littoral, rocky substratum, sheltered, marine salinity.

Fucus vesiculosus var. vadorum

Plencia, 30TVP00; S. Vicente de la Barquera, 30TUP80; Villaviciosa, 30TUP02.

Middle littoral, rocky substratum, quiet waters, marine salinity.

Fucus vesiculosus var. volubilis

Portimao, 29SNB40; Faro, 29SNA99.

Middle littoral, muddy substratum, quet waters, brackish water.

Fucus vesiculosus var. 'evesiculosus' El Abra, 30TVN99; Ria de Suances, 30TVP11; Puerto de Vega, 29TPJ92; Playa de Navia, 29TPJ82; Sada, 29TNH69; Puerto del Son, Canido, 29TMH92; Arcade, 29TNG38; 29TNG17; Rocamar, 29TNG05; Figueira da Foz, 29TNE14; Isla Cristina, 29SPB41.

Middle littoral, rocky substratum, semiexposed, marine salinity

Fucus vesiculosus var. linearis

Playa de Salinas, 30TTP63; Puerto de Vega, 29TPJ92; Playa de Navia, 29TPJ82; Burela, 29TPJ23; Punta Insua, 29TMH93; Puerto del Son, 29TMH92.

Middle littoral, rocky substratum, exposed, marine salinity.

Fucus ceranoides

Deba, 30TWN59; Santofta, 30TVP60; Ria de Tina Mayor, 30TUP70; Llanes, 30TUP50; Villaviciosa, 30TUP02; Playa de Navia, 29TPJ82; Rio Masma (Foz), 29TPJ42; Noya, 29TNH03; Cambados, 29TNH10; Ramallosa, 29TNG16; Figueira da Foz, 29TNE14.

Middle littoral, muddy substratum, quiet waters, low salinity.

fvariability; Powell (1963) has recognized several forms; he has distinguished, from lesser to higher exposure to wave-action, respectively, the forms 'vadorum', vesiculosus and linearis (Hudson) Pow-

ell. The latter includes F. chalonii Feldmann (Powell, 1963). Also two forms have been recognized that occur at the bottom of estuaries 'balticus (Kjelmann)' and volubilis (Turner). The lat-

83 ter includes F. lutarius (Chauvin) Kiltzing, although Wynne & Magne (1991) consider this as a separate species. In the Iberian Peninsula 18 Fucus taxa have been mentioned in the literature (Colmeiro, 1889; Sauvageau, 1907; Ardr6, 1970; Gallardo etal., 1984). They can be assigned to the following species: F. spiralisL., F. vesiculosus L., F. ceranoides L. and F. serratus L. Wynne & Magne (1991) suggest that F. cottonii could possibly occur in Spain. The plants identified by Fuentes & Niell (1985) as F. cottonii (= F. muscoides (Cotton) J. Feldm.) in the Ria de Vigo are in fact F. vesiculosus.

In this paper, we analyze the phenetic variation patterns within three Fucus species present in the Iberian Peninsula in order to verify their equivalence to the taxonomic groups previously established. Here we test numerical methods for solving taxonomical problems in this algal complex. Numerical taxonomy studies are not frequent in macroalgae (Garbary, 1979; Rice & Chapman, 1985); however, they are common in microalgae (Anton & Duthie, 1981; Marvan, 1982; Stoermer et al., 1986).

Materials and methods The study assesses the phenotypic variation of 113 plants collected around the Iberian coasts (Table 1). 36 morphological, anatomical and reproductive characters have been examined (Table 2). We have followed the methodology used by Rice & Chapman (1985). 21 parameters are either continuous or meristic variables, 4 are control variables and 11 are categorical or binary variables. Details on the character definition have been suggested by Rice & Chapman (1985). We have modified only one categorical variable, i.e., midrib shape, by transforming it to a continuous one: midrib height. The height of the midrib was measured in a thin section cut at a point midway between the youngest and next youngest dichotomy. We have assigned the individuals to each of the

Table 2. Features recorded for each Fucus plant. Number

Character

Type of character

Site Position on shore Date of collection Plant number Plant length Plant width Receptacle length Receptacle width Receptacle shape Receptacle shape at tip Holdfast shape Stipe width Midrib height Midrib width Midrib continuous to tip Number of lower dichotomies Number of upper dichotomies Angle of oldest dichotomy Angle of youngest dichotomy Sex Vesicles Number of conceptacles/section Number of oogonia/conceptacle Number of reproductive tips Number of vegetative tips Distance of oldest dichotomy Conceptacle length Conceptacle width Cross section receptacle Intermedullary distance Diameter of oogonium Mucus hole Conceptacle hairs Number cryptostomata/section Group Receptacle edge shape

Control Control Control Control Continuous Continuous Continuous Continuous Binary Binary Categorical Continuous Continuous Continuous Binary Meristic Meristic Meristic Meristic Categorical Binary Meristic Meristic Meristic Meristic Continuous Continuous Continuous Categorical Continuous Continuous Binary Binary Meristic Categorical Binary

groups present in the Iberian Peninsula, which are based on the taxonomic groups established byPowell (1963), by using the following criteria. Fucus spiralisf. spiralis:hermaphrodite conceptacle and sterile rim on receptacle. F. spiralis f. platycarpus: lateral branchlets bearing receptacles. F. spiralis f. nanus: fronds of fertile individuals less than 7 cm high and 1 cm wide. F. ceranoides: dioecious conceptacles, upper dichotomies very close, receptacle tip often pointed.

84 F. vesiculosus f. vesiculosus: dioecious conceptacles, frond with vesicles. F. vesiculosus f. vadorum: very heavily bladdered. F. vesiculosus f. volubilis: frond spirally twisted with axillary vesicles. F. vesiculosus f. linearis: frond without vesicles. Two multivariate numerical methods have been used in this study, namely Principal Components Analysis (PCA) and Discriminant Analysis (DA). PCA enabled us to examine the overall patterns of variation based on morphometric characters in plants of Fucus. PCA is an effective tool to study the interrelationships between measured variables and their grouping into complex gradients (Okland, 1990). DA, which maximizes the ratio of among- to within-group variance, has been used as a technique of classification evaluation and to examine morphological relationships among taxa. A univariate statistical procedure (ANOVA) has been used to test the equality of means among the species. Analysis of variance has been used both in cases where the assumptions of normality and homogeneity of variances are known, and in cases where the assumption of homogeneity of variances has been violated. In the latter cases a one-way ANOVA can be used if the number of samples is higher than 10, and any sample is not more than four times bigger than any other one (Harris, 1985; Bisquerra, 1989); every case met this condition. Analysis of variance has been performed for each of the 21 continous variables in the three species considered: Fucus spiralis, F. vesiculosus and F. ceranoides. F. serratus, has been excluded from the study because it can be distinctly recognized on our coasts. For all multivariate and univariate statistical methods the Statistical Package STATGRAPHICS (version 5.0) of Statistical Graphics Corporation has been used. Continuous variables have been subjected to transformation and standardization. This transformation has taken the form (Okland, 1990) z ' = log ((z - min)/(max - min) + 1), where z' is the range value, min is the lowest value

of variable z encountered over the n sample plots, and max is the highest value of the variable. After this transformation all of the analyses have been tun under the assumption of normality and homogeneity of variances. PCA and DA were performed on the transformed variables.

Results and discussion Plotting scores for the first and second axes (PCA) (Fig. 1) shows that there are no clear morphological discontinuities among the individuals which should allow for the recognition of taxa. The plot also shows that the arrangement of plant scores is elongated along the first component (this has been also noted by Rice & Chapman, 1985). The first axis summarizes 25.2% of the variability in the data set. The cumulative percentages of the second and third components are 42.5 % and 53.6%, respectively. The individuals in the plot have been identified to the species to which they have been assigned previously. A wide separation between individuals identified as F. spiralis and those identified as F. ceranoides is observed on the plot. The distribution of F. vesiculosus individuals in this plot shows a remarkable spread. They are placed close to the origin of the axes, suggesting some morphological similarity with both F. spiralis and F. ceranoides. F. spiralis can be defined in morphological terms by the highest scores of receptacle width, the width, length and number of conceptacles and the width and height of the midrib. F. ceranoides individuals are spread along the positive first axis and negative second axis. F. ceranoides can be defined by the highest scores of plant length, number of dichotomies, number of reproductive and vegetative tips and distance to the oldest dichotomy. The characters having higher correlations with the first component are those related to the length of the plant. Other authors (Sneath & Sokal, 1973; Rice & Chapman, 1985) have also noted that the first component represent a general size factor. The characters having higher correlations

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Fig. 1. Plot of the first two principal components scores of Spanish Fucus material. o F. spiralis, A F. vesiculosus, [ F. ceranoides.

with the second component are the width of the thallus and anatomical features of the vegetative and reproductive structures. The DA (Fig. 2) shows that there is a clear split for Fucus species (F. spiralis, F. vesiculosus and F. ceranoides). The functions can identify 94100% of the individuals of each species. We have additionaly examined the data set looking for evidence of sub-units within both the F. spiralis ('nana', 'spiralis' and 'platycarpus') and F. vesiculosus complexes ('vadorum', 'volubilis', 'vesiculosus' and 'linearis'). The plot of scores of the two first components (PCA, Fig. 3), whose points have been assigned to the infraspecific groups, shows the following. Firstly, the arrangement of group scores within F. spiralis is elongated along the second component. Secondly, groups included within F. vesiculosus show a morphometric ordination too; the arrangement of groups with vesicles that have

been identified as 'vadorum' or 'vesiculosus' are mainly spread along the positive zone of both axes; the arrangement of the group 'volubilis' is elongated along the second axis and the positive zone of the first axis. Thirdly, the group identified as 'linearis' is not homogeneus, some individuals are arranged along the negative zone of axis 1 and the positive of axis 2 but overall the arrangement is elongated in an opposite way. The existence of this split in the 'linearis'group has led us to re-examine the individuals of such a group. This group can be subdivided into two new groups including individuals that might be distinguished by their morphology and autoecology. The subgroup 'linearis' remains for individuals with narrow fronds, living on exposed shores. Individuals with wide fronds, living on sheltered shores have been assigned to a new subgroup, named 'evesiculosus'. The Discriminant Analysis performed for the

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Fig. 2. Plot of scores of functions 1 and 2 calculated by Discriminant Analysis among Spanish Fucus species. o F. spiralis, A F. vesiculosus, [] F. ceranoides. Letters indicate group centroids.

two species having infraspecific groups identified by us resulted in the following. For F. vesiculosus (Fig. 4), the discriminant functions can identify correctly 93-100% of the plants. For F. spiralis (Fig. 5), the discriminant functions allow for lesser values but they are, nevertheless, very high (72-91%); the groups 'platycarpus' and 'spiralis' overlap and so their prediction values are lower (72-84%), they are also the less characterized ones from an autoecological point of view. Table 3 shows the means, standard deviations and statistically significant difference levels on the basis of a one-way ANOVA for each of the quantitative characters used in F. spiralis, F. vesiculosus and F. ceranoides numerical taxonomy. The character averages differ significantly among taxa for nearly all the characters studied. A multiple range test showed that only four of the studied characters can separate the three taxa completely (p