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Seed morphology of Erica L. sect. Loxomeria Salisb. ex Benth., sect.Eremocallis Salisb. ex Benth. and sect. Brachycallis I. Hansen, and itssystematic implicationsJ. Fagúndez a; J. Izco a

a Department of Botany, University of Santiago de Compostela, Santiago de Compostela, Spain

First Published on: 17 August 2009

To cite this Article Fagúndez, J. and Izco, J.(2009)'Seed morphology of Erica L. sect. Loxomeria Salisb. ex Benth., sect. EremocallisSalisb. ex Benth. and sect. Brachycallis I. Hansen, and its systematic implications',Plant Biosystems - An International JournalDealing with all Aspects of Plant Biology,99999:1,

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Plant Biosystems

,

2009, 1–9, iFirst Article

ISSN 1126-3504 print/ISSN 1724-5575 online © 2009 Società Botanica ItalianaDOI: 10.1080/11263500902722626

Seed morphology of

Erica

L. sect.

Loxomeria

Salisb. ex Benth., sect.

Eremocallis

Salisb. ex Benth. and sect.

Brachycallis

I. Hansen, and its systematic implications

J. FAGÚNDEZ & J. IZCO

Department of Botany, University of Santiago de Compostela, Santiago de Compostela, Spain

Taylor and Francis

Abstract

Several quantitative and qualitative seed characters of the seven European species of

Erica

sect.

Loxomeria

,

Eremocallis

and

Brachycallis

were studied. Two main seed types are found based on size and shape: regular ellipsoid or oblong seeds of ca.0.4 mm for

E. ciliaris

and the

E. tetralix

group, and curved to kidney-shaped seeds of 0.6–0.9 mm for

E. cinerea

,

E.maderensis

and

E. terminalis

. The testa surface in

E. ciliaris

is reticulate, with indented outer periclinal walls.

Erica cinerea

has inflated outer anticlinal walls. This character is exclusive for this species within the European (and nearby areas) speciesof the genus. The seeds of

E. maderensis

are similar to those of

E. terminalis

. According to seed morphology, the classicalinfrageneric classification, by which

E. terminalis

would be grouped with the

E. tetralix

group in sect.

Eremocallis

and

E.maderensis

in sect.

Brachycallis

with

E. cinerea

, is artificial.

Keywords:

Ericaceae, Ericeae,

Erica

, taxonomy, SEM pictures, seed coat

Introduction

Many interesting and stable characters are found inthe seed morphology of the Ericaceae, as illustratedin some family treatments (Stevens 1971; Anderberg1993; Oliver 2000; Kron et al. 2002) as well as inspecific taxon studies within the family (Van derKloet 1983; Takahashi 1993). Seeds of

Erica

havebeen studied for fossil identification (Huckerby et al.1972; Wilson et al. 1973), ecological purposes (Vera1997) and descriptive studies (Bannister 1965,1966). Recently, we have highlighted the taxonomicimportance of seed morphology in this genus(Fagúndez & Izco 2003a, 2003b, 2004a, 2004b).

In the present study, we examined the Europeanspecies of sect.

Loxomeria

Salisb. ex Benth. (

E. ciliaris

L.), sect.

Eremocallis

Salisb. ex Benth. (

E. tetralix

L.,

E. mackayana

Bab.,

E. terminalis

Salisb.,

E. andeva-lensis

Cabezudo & Rivera) and sect.

Brachycallis

I.Hansen (

E. cinerea

L.,

E. maderensis

(Benth.)Bornm.).

Erica ciliaris

has lateral inflorescences, adistinctly curved, gibose corolla, and no antherappendages. This species resembles

E. tetralix

,

E.

mackayana

and

E. andevalensis

(here referred to asthe

E. tetralix

group) in many aspects such as indu-mentum and leaf shape. It also forms hybrids with

E.tetralix

(

E.

x

watsonii

Benth.) that might produceseeds (Rose et al. 1995).

Erica cinerea

has flowers inwhorls of one to three at the end of short secondarybranches. It has leaves in whorls of three, and youngstems have fascicles of leaves.

Erica maderensis

hasbeen considered a variety or subspecies of

E. cinerea

.McClintock (1981, 1989) stated that the speciesrank is the correct systematic level for this species. Italso has characters similar to those of

E. terminalis

(McClintock 1971, 1981).

Erica terminalis

has flow-ers in whorls at the end of long secondary branches,and leaves with half-rolled margins. The

E. tetralix

group is formed by

E. tetralix

,

E. mackayana

and

E.andevalensis

, a clearly differentiated group within thegenus but with taxonomic problems at the speciesrank for

E. mackayana

and

E. andevalensis

(McClin-tock 1989; Bayer 1993; Fagúndez & Izco 2004b).

The most widely used infrageneric classification ofthe European species of

Erica

is the one of Bentham(1839) with some modifications by Hansen (1950).

Correspondence: J. Fagúndez, Department of Botany, Faculty of Pharmacy, University of Santiago de Compostela, Santiago de Compostela 15782, ACoruña, Spain. Tel: 0034655611333. Email: jaime.fagundez@usc.es

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2

J. Fagúndez and J. Izco

Subgenus and sections were established based on afew characters considered as determinant such asanther exertion, inflorescence type and corollashape. This classification needs a profound revisionas some groups are clearly artificial (Oliver & Oliver2002).

In this work, seed morphology of the species ofthis complex was studied, and the taxonomy of thegroup is discussed. Seed characters can provideuseful information for the construction of a naturalsystematic classification within

Erica

.

Materials and methods

Seeds were either collected in the field or receivedfrom different seedbanks (Table I). In total 35 popu-lations were studied. Collected seeds were storedunder cold and dry conditions following the proce-dures of the University of Santiago de CompostelaSeedbank (Fagúndez 2001).

Seeds were measured using a video cameraconnected to a binocular microscope. Images weretreated by means of UTHSCSA Image Tool software(San Antonio, Texas, 1997). Area (a), perimeter (p),major axis length, minor axis length, elongation(main axis/minor axis) and sinuosity (4

π

a/p

2

) weremeasured for each seed; mean and standard deviationwere calculated for each population.

Nested ANOVAs – as described by Fagúndez andIzco (2004b) – were performed to check that specificdifferences are significant considering the intraspe-cific variability.

Seed weight was calculated for 100 seeds.A Munsell colour chart was used for colourdetermination.

For SEM pictures, 5–10 dry seeds from differentpopulations were mounted on metal stubs usingdouble-stick tape, and gold-coated. Pictures ofwhole seeds and details were taken of three seeds foreach population.

Table I. Populations studied for the seven species of

Erica

.

Population Species Collection place Collection date From

and79

E. andevalensis

Spain: Huelva, Tharsis 8-1999 J. Fagúndez, D. Reyesand100

E. andevalensis

Spain: Huelva, Valdelamusa 8-1999 J. Devesaand108

E. andevalensis

Spain: Huelva, El campillo 8-1994 R.J.B. Madridand126

E. andevalensis

Spain: Huelva J.B. Córdobaand283

E. andevalensis

Spain: Huelva, Zalamea la Real 1995 E.T.S.I.A. Madridcil18

E. ciliaris

Spain: A Coruña, Ferrol 8-1998 J. Fagúndezcil22

E. ciliaris

Spain: A Coruña, Ames 9-1998 J. Fagúndezcil24

E. ciliaris

Spain: A Coruña, A Capelada 9-1998 J. Fagúndezcil266

E. ciliaris

Spain: Cádiz, Alcornocales 9-2002 J. Fagúndez, D. Reyescil273

E. ciliaris

Portugal: Matas de Faia 9-2001 Unknowncin25

E. cinerea

Spain: A Coruña, A Capelada 9-1998 J. Fagúndezcin123

E. cinerea

Spain: A Coruña, Ames 11-1999 J. Fagúndez, A. Aguilarcin140

E. cinerea

Spain: Pontevedra, Burgueira 12-1999 J. Fagúndez, A. Aguilarcin194

E. cinerea

France: Gironde, Canéjean 10-1997 J.B. Bordeauxcin302

E. cinerea

Spain: Cuenca, Henarejos 9-2000 J. Fagúndez, B. Lunamac23

E. mackayana

Spain: A Coruña, Capelada 9-1998 J. Fagúndezmac148

E. mackayana

Spain: Lugo, Burela 9-1999 J. Fagúndezmac151

E. mackayana

Spain: A Coruña, Xistral 9-1999 J. Fagúndezmac250

E. mackayana

Spain: Oviedo, Llanes 8-2001 J. Fagúndez, A. Aguilarmac284

E. mackayana

Spain: Oviedo, Salas 1981 E.T.S.I.A. Madridmad192

E. maderensis

Portugal: Madeira, L. do Mouro 10-1998 J.B. da Madeiramad300

E. maderensis

Portugal: Madeira, Pico Areeiro 7-2003 J.C. Costamad339

E. maderensis

Portugal: Madeira, Pico Ruivo 9-2004 J. Fagúndezmad353

E. maderensis

Portugal: Madeira, Pico do Juncal 9-2004 J. Fagúndezmad354

E. maderensis

Portugal: Madeira, Pico Areeiro 9-2004 J. Fagúndezter92

E. terminalis

Spain: Valencia, Buñol 8-1999 J. Izcoter198

E. terminalis

Spain R.J.B. Madridter265

E. terminalis

Spain: Málaga, Ronda 9-2002 J. Fagúndez & D. Reyestet116

E. tetralix

Spain: A Coruña, Brandomil 11-1999 J. Fagúndez, R. Iglesiastet119

E. tetralix

Spain: A Coruña, Carnota 11-1999 J. Fagúndez, R. Iglesiastet130

E. tetralix

Spain: A Coruña, Toques 12-1999 J. Fagúndeztet211

E. tetralix

Spain: Ciudad Real, Cabañeros 10-2000 J. Fagúndez, A. Velascotet255

E. tetralix

Belgium: Namur 9-2001 B. Píastet285

E. tetralix

Spain 1998 J. B. Alcalátet286

E. tetralix

Sweden: Halland, Söndrum 11-1996 A. & A.-L. Anderberg

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Seed morphology of

Erica

sect.

3

Nomenclature used for description purposes isthat of Berggren (1981) and Barthlott (1981,1984).

Results

Seed size and shape

Two main seed sizes are found, with small seeds of0.35–0.45 mm for species of the

E. tetralix

groupand

E. ciliaris

, and seeds of (0.55) 0.6–0.9 mm for

E. cinerea

,

E. maderensis

and

E. terminalis

. Results(Table II) show large differences between popula-tions and wide intervals for most of the species,confirming the study by Fagúndez and Izco(2004b). Shape is variable: oval, ellipsoid or oblongfor the seeds of the

E. tetralix

group (Figure 1A, C,E), while

E. ciliaris

has oblong-ellipsoid seeds, withthe hilum region oblong and curved at the apex(Figure 1G). Seeds of

E. cinerea

,

E. maderensis

and

E. terminalis

are irregular, ellipsoid, round or mostlykidney-shaped with the hilum region displaced toone side (Figure 1I, K, M). This curved shape ismore accentuated in E. cinerea. These three species

have a trigonous section, with two flat and onecurved side, while the other species have a roundsection. Axis ratio is 4:3 for the E. tetralix groupwhile E. ciliaris has more elongate seeds with a 3:2axis ratio, as in E. cinerea and E. terminalis. E. made-rensis has a ca. 2:1 ratio, but the last three specieshave wide confidence ranges (Table II).Figure 1. SEM pictures of seeds of the seven different species: (A) E. andevalensis (and79) whole seed. (B) E. andevalensis (and126) detail of surface cells. (C) E. mackayana (mac23) whole seed. (D) E. mackayana (mac250) detail of surface cells. (E) E. tetralix (tet119) whole seed.(F) E. tetralix (tet211) detail of surface cells. (G) E. ciliaris (cil266) whole seed. (H) E. ciliaris (cil273) detail of surface cells. (I) E. cinerea (cin302) whole seed. (J) E. cinerea (cin25) detail of surface cells. (K) E. maderensis (mad192) whole seed. (L) E. maderensis (mad192) detail ofsurface cells. (M) E. terminalis (ter92) whole seed. (N) E. terminalis (ter265) detail of surface cells.

Primary ornamentation and testa cells

Ornamentation is reticulate for all the species.Testa cells are isodiametric or elongate with a ratioof up to 2:1, always longitudinal. Cell walls arecurved or convolute, sometimes strongly undulateas in E. tetralix (Figure 1E). Outer anticlinal wallsare continued by the outer periclinal walls, slightlydifferentiated except for E. cinerea with inflatedwalls (Figure 1J), as a result of the outer wallscollapsing over the thick inner anticlinal walls. Cellboundaries are either channelled as in the E. tetralixgroup, partially anastomosed as in E. terminalis, ortotally anastomosed as mostly observed in E.cinerea.

Table II. Seed characters (mean ± standard deviation).

Population N Area Perimeter Major axis length Minor axis length Elongation Sinuosity

and79 30 0.08 ± 0.009 1.12 ± 0.081 0.38 ± 0.021 0.26 ± 0.019 1.46 ± 0.076 0.77 ± 0.052and100 33 0.08 ± 0.007 1.12 ± 0.052 0.38 ± 0.018 0.26 ± 0.013 1.47 ± 0.085 0.79 ± 0.036and108 23 0.08 ± 0.007 1.20 ± 0.056 0.38 ± 0.021 0.28 ± 0.014 1.36 ± 0.089 0.73 ± 0.057and283 25 0.08 ± 0.008 1.39 ± 0.207 0.37 ± 0.027 0.27 ± 0.024 1.35 ± 0.138 0.51 ± 0.111cil18 25 0.08 ± 0.011 1.19 ± 0.086 0.40 ± 0.028 0.26 ± 0.017 1.58 ± 0.111 0.72 ± 0.065cil22 7 0.09 ± 0.008 1.72 ± 0.314 0.44 ± 0.037 0.26 ± 0.015 1.70 ± 0.168 0.40 ± 0.123cil24 25 0.07 ± 0.009 1.22 ± 0.142 0.35 ± 0.031 0.25 ± 0.020 1.39 ± 0.171 0.59 ± 0.118cil266 30 0.10 ± 0.007 1.73 ± 0.130 0.45 ± 0.026 0.28 ± 0.017 1.59 ± 0.127 0.42 ± 0.059cin25 50 0.80 ± 0.059 0.56 ± 0.050 1.43 ± 0.151cin123 33 0.29 ± 0.038 2.35 ± 0.194 0.74 ± 0.068 0.53 ± 0.044 1.42 ± 0.169 0.67 ± 0.055cin140 25 0.27 ± 0.029 2.35 ± 0.180 0.72 ± 0.050 0.49 ± 0.035 1.46 ± 0.120 0.62 ± 0.056cin194 30 0.35 ± 0.037 2.75 ± 0.155 0.85 ± 0.056 0.55 ± 0.036 1.53 ± 0.116 0.59 ± 0.027mac148 27 0.11 ± 0.008 1.41 ± 0.071 0.45 ± 0.031 0.31 ± 0.016 1.45 ± 0.141 0.68 ± 0.041mac151 18 0.10 ± 0.015 1.42 ± 0.158 0.41 ± 0.038 0.31 ± 0.029 1.32 ± 0.086 0.60 ± 0.067mac250 35 0.10 ± 0.009 1.40 ± 0.071 0.40 ± 0.027 0.33 ± 0.018 1.22 ± 0.113 0.65 ± 0.038mac284 25 0.10 ± 0.010 1.36 ± 0.088 0.40 ± 0.029 0.33 ± 0.020 1.22 ± 0.095 0.69 ± 0.054mad192 22 0.14 ± 0.019 1.79 ± 0.118 0.56 ± 0.043 0.33 ± 0.028 1.73 ± 0.190 0.55 ± 0.037mad300 29 0.14 ± 0.017 2.20 ± 0.309 0.59 ± 0.046 0.32 ± 0.033 1.88 ± 0.261 0.38 ± 0.069mad339 13 0.17 ± 0.014 1.76 ± 0.077 0.64 ± 0.038 0.35 ± 0.034 1.83 ± 0.166 0.70 ± 0.041mad353 14 0.24 ± 0.023 2.09 ± 0.115 0.77 ± 0.059 0.40 ± 0.036 1.95 ± 0.235 0.70 ± 0.049mad354 19 0.16 ± 0.023 1.73 ± 0.151 0.63 ± 0.065 0.33 ± 0.036 1.94 ± 0.312 0.67 ± 0.067ter92 25 0.20 ± 0.032 2.11 ± 0.150 0.62 ± 0.049 0.40 ± 0.038 1.56 ± 0.174 0.56 ± 0.072ter198 23 0.72 ± 0.049 0.55 ± 0.038 1.32 ± 0.120ter265 42 0.18 ± 0.017 2.29 ± 0.200 0.61 ± 0.032 0.39 ± 0.028 1.56 ± 0.124 0.44 ± 0.063tet116 19 0.10 ± 0.012 1.39 ± 0.108 0.41 ± 0.032 0.32 ± 0.020 1.30 ± 0.114 0.66 ± 0.056tet119 29 0.11 ± 0.011 1.41 ± 0.095 0.41 ± 0.027 0.33 ± 0.020 1.27 ± 0.113 0.66 ± 0.053tet130 32 0.10 ± 0.013 1.35 ± 0.108 0.40 ± 0.030 0.32 ± 0.025 1.29 ± 0.112 0.68 ± 0.050tet211 32 0.10 ± 0.012 1.43 ± 0.101 0.43 ± 0.037 0.31 ± 0.018 1.39 ± 0.106 0.63 ± 0.026tet255 31 0.08 ± 0.007 1.22 ± 0.050 0.36 ± 0.019 0.27 ± 0.016 1.35 ± 0.107 0.64 ± 0.025tet285 35 0.09 ± 0.008 1.18 ± 0.067 0.38 ± 0.024 0.29 ± 0.016 1.34 ± 0.100 0.77 ± 0.050

Note: All values for the seven species of Erica in mm except for area (mm2), elongation and sinuosity.

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4 J. Fagúndez and J. Izco

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Seed morphology of Erica sect. 5

Secondary ornamentation

Outer periclinal walls are smooth or with distinctornamentation, indented for E. ciliaris. Somevermiculate ornamentation (Figure 1B, D) might bedue to the drying effects of seed preparation forSEM (Brisson & Peterson 1976). Outer anticlinalwalls are smooth as in E. ciliaris (Figure 1H) orcoarsely vermiculate although this could be due tothe same drying effect.

Seed description

Erica ciliaris L. Seeds yellowish or reddish-brown.Weight around 0.01 mg. Seeds with a distinctoutline, oblong-elliptical, with hilum region oblongand elliptical at the distal end. Cross-section circu-lar. 0.35–0.45 mm long, 0.25–0.3 mm wide. Axisratio 3:2. Appendages absent. Hilum terminal,sometimes protruding. Seed surface reticulate, with8–10 cells in main axis. Ornamentation sometimesbranched, that might be confused with cell outline.Cells mostly quadrangular, elongated with a 2:1 axisratio, isodiametric near the polar ends, with undu-lated borders. Outer anticlinal walls thin, smooth,with almost no projection over the outer periclinalwalls which are indented. Cell boundariesanastomosing (see Table III).

Erica tetralix L. Seeds yellowish or reddish-brown.Weight around 0.01 mg. Seeds outline elliptical oroval. Cross-section circular. 0.35–0.45 mm long,0.28–0.32 mm wide. Axis ratio 4:3. Appendagesabsent. Hilum terminal. Seed surface reticulate, with10 cells in main axis. Cells irregular mostly with fourto six sides with a 1:1 axis ratio, with undulated orstrongly undulated borders. Outer anticlinal wallscontinued by outer periclinal walls, the latter smoothor with a vermiculated pattern. Cell boundarieschannelled.

Erica mackayana Bab. Seeds reddish or dark brown.Weight around 0.01 mg. Seeds outline oblong, ovalor elliptical. Cross-section circular. 0.4–0.45 mmlong, 0.3–0.35 mm wide. Axis ratio 5:4–4:3. Append-ages absent. Hilum terminal. Seed surface reticulatedwith 8–10 cells in main axis. Cells irregular mostlywith four to six sides with a 1:1 axis ratio, with curvedmargins. Outer anticlinal walls continued by outerpericlinal walls, which had a vermiculated pattern.Cell boundaries channelled.

Erica andevalensis Cabezudo & Rivera. Seedsyellowish or reddish-brown. Weight around 0.01 mg.Seeds outline oval, sometimes elliptical or oblong.Cross-section circular. 0.37–0.39 mm long, 0.26–0.3mm wide. Axis ratio 4:3–3:2. Appendages absent.Hilum terminal. Seed surface reticulated, with 8–10cells in main axis. Cells irregular mostly with four to

Figure 1. SEM pictures of seeds of the seven different species: (A) E. andevalensis (and79) whole seed. (B) E. andevalensis (and126) detailof surface cells. (C) E. mackayana (mac23) whole seed. (D) E. mackayana (mac250) detail of surface cells. (E) E. tetralix (tet119) wholeseed. (F) E. tetralix (tet211) detail of surface cells. (G) E. ciliaris (cil266) whole seed. (H) E. ciliaris (cil273) detail of surface cells. (I) E.cinerea (cin302) whole seed. (J) E. cinerea (cin25) detail of surface cells. (K) E. maderensis (mad192) whole seed. (L) E. maderensis(mad192) detail of surface cells. (M) E. terminalis (ter92) whole seed. (N) E. terminalis (ter265) detail of surface cells.

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6 J. Fagúndez and J. Izco

Tab

le I

II.

Mai

n se

ed c

hara

cter

isti

cs f

or t

he s

even

spe

cies

. S

ize

are

mea

n va

lues

cal

cula

ted

for

each

spe

cies

(se

e T

able

II

for

inte

rpop

ulat

ion

vari

atio

ns).

Dif

fere

nt l

ette

rs i

ndic

ate

sign

ifica

ntho

mog

eneo

us s

ub-g

roup

s ac

cord

ing

to S

tude

nt-N

ewm

an-K

euls

tes

t at

α =

0.0

1, a

fter

a o

ne-w

ay A

NO

VA

for

maj

or a

xis

leng

th.

E.

cilia

ris

E.

ande

vale

nsis

E.

mac

kaya

naE

. te

tral

ixE

. te

rmin

alis

E.

cine

rea

E.

mad

eren

sis

See

d si

ze0.

4 ×

0.26

ab0.

38 ×

0.2

7a0.

41 ×

0.3

2b0.

4 ×

0.3a

b0.

64 ×

0.4

4c0.

78 ×

0.5

4d0.

64 ×

0.3

5cS

eed

shap

eO

blon

g-el

lipso

idE

llips

oid

or o

void

Elli

psoi

d or

ovo

idE

llips

oid

or o

void

Cur

ved

Cur

ved,

kid

ney-

shap

eC

urve

dC

ross

-sec

tion

Rou

ndR

ound

Rou

ndR

ound

Tri

gono

usT

rigo

nous

Tri

gono

usT

esta

cel

ls o

utlin

eU

ndul

ate

Cur

ved

to u

ndul

ate

Cur

ved

to u

ndul

ate

Str

ongl

y un

dula

teS

trai

ght,

cur

ved

or

undu

late

Str

aigh

t to

cur

ved

Str

aigh

t, c

urve

d or

un

dula

teO

uter

per

iclin

al w

alls

Inde

nted

Sm

ooth

or

verm

icul

ate

Sm

ooth

or

verm

icul

ate

Mos

tly

smoo

thM

ostl

y sm

ooth

Sm

ooth

Mos

tly

smoo

thO

uter

ant

iclin

al w

alls

Thi

n an

d sm

ooth

Str

aigh

t, s

moo

th o

r ve

rmic

ulat

eS

trai

ght,

sm

ooth

or

verm

icul

ate

Str

aigh

t, s

moo

thS

trai

ght,

sm

ooth

Infl

ated

Str

aigh

t, s

moo

th

Cel

l bou

ndar

ies

Ana

stom

osin

gC

hann

elle

dC

hann

elle

dC

hann

elle

dC

hann

elle

d or

an

asto

mos

ing

Ana

stom

osin

gC

hann

elle

d or

an

asto

mos

ing

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Seed morphology of Erica sect. 7

six sides with a 1:1 axis ratio. Outer anticlinal wallscontinued by outer periclinal walls, which are smoothor had a vermiculated pattern. Cell boundarieschannelled.

Erica cinerea L. Seeds light or dark brown, imma-ture seeds blue, purple, whitish or green. Weightaround 0.1 mg. Seeds curve to kidney-shape, with acurved side and a straight side, apiculate and curvedat basal region, but also ellipsoid or other shapes.Cross-section irregular, mostly trigonous with twostraight sides and one curved. 0.7–0.9 mm long,0.5–0.56 mm wide. Axis ratio 3:2, variable. Append-ages absent. Hilum subterminal, displaced to oneside. Seed surface reticulate, with 15–20 cells inmain axis, variable. Cells with four to six sidesstraight or curved, isodiametric or slightly elongated.Outer anticlinal walls inflated, smooth, clearlydistinct from outer periclinal walls, the lattersmooth. Cell boundaries anastomosing.

Erica terminalis Salisb. Seeds yellowish or reddish-brown. Weight around 0.08 mg. Seeds curve tokidney-shape, with a curved side and a straight side,apiculated and curved at basal region, but alsoellipsoid or other shapes. Cross-section irregular,mostly trigonous with two straight sides and onecurved. 0.6–0.75 mm long, 0.38–0.5 mm wide. Axisratio 3:2, variable. Appendages absent. Hilum sub-terminal, displaced to one side. Seed surface reticu-late, with 10–15 cells in main axis, variable. Cells withfour to six sides straight, curved or undulate, isodia-metric or slightly elongated. Outer anticlinalwalls straight, smooth, distinct from outer periclinalwalls, which were smooth or slightly striated. Cellboundaries channelled or anastomosing.

Erica maderensis (Benth.) Bornm. Seeds yellowishor reddish-brown. Weight around 0.08 mg. Seedscurve to kidney-shape, with a curved side and astraight side, apiculated and curved at basal region,but also ellipsoid or other shapes. Cross-sectionirregular, mostly trigonous with two straight sidesand one curved. Variable in size, (0.55) 0.6–0.7(0.8) mm long, 0.3–0.4 mm wide. Axis ratio 2:1–5:3. Appendages absent. Hilum sub-terminal,displaced to one side. Seed surface reticulate, with8–12 cells in main axis, variable. Cells with four tosix sides with straight, curved or undulate margins,isodiametric or slightly elongated. Outer anticlinalwalls straight, smooth, distinct from outer periclinalwalls, which were smooth or slightly striated. Cellboundaries channelled or anastomosing.

Discussion

Seed characters provide a large amount of taxo-nomic information that should be used for thedelimitation of species and the elucidation of rela-tionships. Bentham (1839) proposed the first

infrageneric classification for Erica. The originallynamed subgenus Euerica is characterised bydorsifixed anthers (lateral) and urceolate to tubularcorollas. All the species treated here are part of thissubgenus. Within this, sect. Loxomeria has only onespecies, E. ciliaris, supported by its curved corollaand the absence of anther appendages. The seedtype of E. ciliaris is also clearly distinct from theseeds of other species of this group or any otherEuropean species of Erica. The oblong-ellipsoidshape with the sometimes protruding hilum (Figure1G), the reticulate ornamentation with thin outeranticlinal walls and the indented or pitted pattern ofsecondary ornamentation (Figure 1H) are onlyobserved in this species. The monospecific section isthus supported by seed morphology.

Erica ciliaris is related to the E. tetralix group(McClintock 1971; Chapman 1975). This is mainlybased on the leaf type, not totally rolled on itsmargins, indumentum with many long glandularhairs, and also ecological requirements for humidsoils (Webb & Rix 1972; Bayer 1993). Furthermore,natural hybridisation is found between E. tetralix andE. ciliaris. Seeds of E. ciliaris also show some similar-ities (seed size, basal position of hilum) with seedsfrom the E. tetralix group. Differences are found insecondary sculpture with indented outer periclinalwalls and the smooth, mostly anastomosed outeranticlinal walls, and the oblong-elliptical outline ofthe seeds of E. ciliaris.

Sect. Eremocallis has inflorescences in many-flowered whorls at the end of secondary branches,glabrous urceolate corollas and anther appendages.Bentham (1839) included in this section E. tetralix,E. mackayi (=E. mackayana), E. australis, E. stricta(=E. terminalis) and E. cinerea (including var.maderensis). Later Hansen (1950) proposed twomonospecific sections: sect. Tylospora for E. australisand sect. Brachycallis for E. cinerea (includingMadeira in its geographic distribution). Thisarrangement left E. terminalis and the E. tetralixgroup (including E. andevalensis discovered later on)in sect. Eremocallis (Bayer 1993). Seed morphologyshows a clearly different seed type for E. australis asstated in a previous paper (Fagúndez & Izco 2004a)mostly for the presence of a caruncle and striatedseed coat pattern, supporting the existence of sect.Tylospora. As for sect. Brachycallis, the main charac-ter used is the spike-like syninflorescence of E. cinereaversus umbel-like inflorescences in Eremocallis, andthe presence of fascicles of leaves in E. cinerea.However, in our opinion, these characters are over-weighed because the inflorescence of E. cinerea isformed by short secondary branches with only one tothree flowers at the top, giving the aspect of a spikewith terminal and lateral groups of flowers. The samehappens with the fascicles of leaves that are in fact

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8 J. Fagúndez and J. Izco

leaves placed on very short secondary branches. Thisis clear when we analyse E. maderensis, where axillarynon-flowering branches and secondary floweringbranches are not as short, somewhat intermediatebetween E. terminalis and E. cinerea.

Seed morphology groups together E. cinerea, E.terminalis and E. maderensis although the inflatedouter anticlinal walls of E. cinerea are a clearly distinctcharacter. E. maderensis and E. terminalis have thesame almost undistinguishable seed type. No cleardifferences were found for these two species, exceptfor the more elongated seeds of E. maderensis.

The E. tetralix group is formed by E. tetralix andtwo closely related species – that are E. mackayanaand E. andevalensis. The latter two have glabrousovaries and an indumentum with long glandular hairswhile E. tetralix has smooth, thin non-glandular hairs,and a hairy ovary. Differentiation of E. mackayanaand E. andevalensis is more difficult and this has ledto subordination of the latter species as E. mackayanasubsp. andevalensis (Cabezudo & Rivera) McClintock& Nelson (McClintock 1989). However, the two taxalive in distinct biogeographical regions: E. mackayanain Ireland and the Cantabric coast of the IberianPeninsula, and E. andevalensis in the Andévalo region(Huelva, Spain) and closer sites of Sevilla and Portu-gal. E. tetralix inhabits a much wider geographic area,including the gap area between the other two species.

In a previous work (Fagúndez & Izco 2004b) wefound that intraspecific and intrapopulation varia-tions for numerical seed characters in this groupwould explain most of the differences found betweenspecies. The character that would better adjust tospecific variation was sinuosity of surface cells. Itgrouped together E. andevalensis and E. mackayanaversus E. tetralix that has very sinuate surface cells.Size of seeds was very variable, but E. andevalensisand E. mackayana could be fairly well discriminatedwith seeds of 0.36–0.39 for E. andevalensis and 0.38–0.46 for E. mackayana (see Table II). Other charac-ters are not clear, such as outer anticlinal walls thatmight be thin and straight for E. tetralix (Figure 1F)or thicker with coarse vermiculated secondary sculp-ture for E. andevalensis and E. mackayana (SEM –Figure 1B, D). However, these types are not constantand different types can be found in any single species.Even if the seed types of E. andevalensis and E. mack-ayana are closer than that of E. tetralix, specific treat-ment should most likely be maintained.

Erica terminalis has umbel-like inflorescences likethose of the E. tetralix group, but it has no glandularhairs on them as E. cinerea. Seed morphology groupstogether E. terminalis and E. cinerea, clearly closer toeach other than to the E. tetralix group. However,the closest species to E. terminalis is E. maderensis,with seeds almost identical in ornamentation, sizeand shape (Figure 1K, M).

Erica maderensis was originally considered as avariety of E. cinerea (Bentham 1839; Hansen 1950;Bannister 1965) and is now a well-establishedspecies as stated by McClintock (1971, 1981). Thisauthor also found characters that would connect thisspecies to E. terminalis such as corolla shape.

Erica cinerea has some distinct seed characterssuch as size and the inflated outer anticlinal walls,but also the colour when immature or the mostlykidney-shaped form.

Erica terminalis has an exclusive character amongEuropean species of Erica, namely that its pollen isin monads instead of tetrads (McClintock 1981;Bayer 1993). Other characters are closer to E.tetralix, such as inflorescences in umbels and a hairyovary. Apart from comments made about the inflo-rescence type, both states for ovary hairiness arefound in closely related species such as those of theE. tetralix group, hairy in E. tetralix and glabrous inE. mackayana and E. andevalensis. Erica terminalisalso resembles E. maderensis in seed type, antherappendages and indumentum, while inflorescenceand foliar arrangement of E. maderensis is intermedi-ate between that of E. cinerea and E. terminalis. Thequestion has no easy solution, but E. terminalisshould neither remain in sect. Eremocallis nor beincluded in sect. Brachycallis.

Acknowledgements

We would like to thank the people and institutionsthat provided seeds for this study, and the reviewersfor their useful comments. Partial support for theproject was provided by CGL2006-06890, Ministe-rio de Educación y Ciencia, Spain.

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