Universidad y Ciencia
ISSN: 0186-2979
[email protected]
Universidad Juárez Autónoma de Tabasco
México
López, N.; Rodríguez, D.; Candelaria Silva, C.
INTRASPECIFIC MORPHOLOGICAL VARIATION IN TURF-FORMING ALGAL SPECIES
Universidad y Ciencia, vol. Num. Esp., núm. I, 2004, pp. 7-15
Universidad Juárez Autónoma de Tabasco
Villahermosa, México
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Número Especial I: 7-15, 2004
INTRASPECIFIC MORPHOLOGICAL VARIATION IN TURF-FORMING ALGAL SPECIES
Variación morfológica intraespecífica en especies de algas cespitosas
N López
, D Rodríguez, C Candelaria-Silva
(NL) (DR) Laboratorio de Ficología Departamento de Biología Comparada
Facultad de Ciencias, Universidad Nacional Autónoma de México
A.P. 70-592. D.F.04510 México [email protected]
(CCS) Herbario-Sección de Algas (FCME) Facultad de Ciencias, UNAM
Artículo recibido: 26 de junio de 2004
Artículo aceptado: 25 de octubre de 2004
RESUMEN. Los ensambles de algas con forma de crecimiento de césped han sido ampliamente estudiados en arrecifes coralinos, sin
embargo, este tipo de comunidades son poco conocidas en el Pacífico tropical mexicano. Un total de 45 especies de algas cespitosas
fueron recolectadas en cinco localidades de esta costa para analizar sus variaciones morfológicas. Todas estas variaciones fueron
agrupadas en seis tipos cualitativos, los cuales pueden ser considerados como seis estrategias diferentes para ajustar los patrones de
crecimiento de las especies para formar céspedes. Estas respuestas fueron: el tipo 1 incluyó 21 especies con una reducción en la talla
del talo, pero dentro de la variación específica previamente registrada, como Halimeda discoidea, el tipo 2 agrupó 12 especies con
modificaciones en la talla del talo, pero fuera de la variación específica previamente observada, como Phyllodictyon anastomosans, el
tipo 3 incluyó cuatro especies con modificaciones en estructuras vegetativas, como Laurencia clarionensis, el tipo 4 formado por dos
especies con modificaciones de las estructuras reproductivas, como Ceramium mazatlanense, el tipo 5 agrupó cinco especies con
modificaciones de las estructuras vegetativas y de la talla del talo, como Grateloupia prolongata, y el tipo 6 integrado por una especie
con modificación de las estructuras reproductivas y de la talla del talo, como Acetabularia parvula. Los seis tipos de respuestas morfológicas
observadas pueden ser asociadas con diferentes estrategias de especies de algas para ajustar sus patrones de crecimiento para
formar céspedes.
Palabras clave: céspedes algales, variación intraespecífica, morfología algal, comunidades algales, Pacífico tropical mexicano.
ABSTRACT. Turf-forming algal assemblages have been studied on many coral reefs, but little is known about similar communities on
the Mexican tropical Pacific. A total of 45 turf-forming algal species were sampled from five locations on this coast to analyze their
morphological variations. All of those variations were grouped in six qualitative types, which could be considered as six different strategies
to adjust the growth patterns by the species to form turfs. These responses were: type 1 included 21 species with a reduction in overall
thallus size, but within the specific variation previously reported, for example Halimeda discoidea, type 2 grouped 12 species with
modifications in thallus size, but beyond the specific variation previously registered, as Phyllodictyon anastomosans, type 3 included
four species with modifications of vegetative structures, as Laurencia clarionensis, type 4 formed by two species with modifications of
reproductive structure, as Ceramium mazatlanense, type 5 grouped five species with modification of vegetative structures and thallus
size, as Grateloupia prolongata, and type 6 integrated by one species with modification of reproductive structures and thallus size, as
Acetabularia parvula. The six types of morphological observed responses could be regarded as different strategies of algal species to
adjust their growth patterns to form turfs.
Key words: algal turf, intraspecific variation, algal morphology, algal communities, Mexican tropical Pacific.
7
UNIVERSIDAD Y CIENCIA
Número Especial I
INTRODUCTION
Several algal turf growth forms have been described
(Dahl 1971; Hay 1981; Hackney et al. 1989). Most of the
observed variation in these growth forms is considered to
be a response of the algae to different environmental
conditions (Hay 1981; Lewis et al. 1987; Airoldi 2001). The
most general definition of “turfing algae” is that of an
assemblage of macroalgae that tend to form thick, dense
mats encompassing one to many epilithic and or epiphytic
algal species (Hackney et al. 1989). Hay (1981) noted that
turf-forming species have high morphological plasticity and
adjust their growth form in accordance with varying levels of
environmental disturbances such as different levels of
grazing and physical stresses such as desiccation. Thallus
morphology can change from arbustive, with loose and
sparse branching patterns, to thalli that are shorter, more
erect, and more highly branched and compacted.
In the Mexican tropical Pacific, turf-forming algal
assemblages have been recorded in the subtidal zone
(López et al. 2000). These multispecific assemblages
typically had tightly compacted thalli up to 2 cm in height
and a richness of 65 species, including fleshy species for
instance Grateloupia spp., filamentous species like
Ceramium spp., geniculate and non-geniculate coralline
species for example Amphiroa spp., and Lithophyllum sp.,
and a few bushy species such as Caulerpa sertularioides
and Padina spp. protruding from the turf. In addition, the turf
was covered with sediment, mainly sand, which was
constantly replaced, giving it a homogeneous appearance
(López et al. 2000).
Assessments regarding spatial and temporal
variation in community structure are in progress (López et
al. unpublished data), but morphological differences
appeared to be evident in many of the algal species, as
compared in contrast to available descriptions of the same
species in other locations of the Mexican Pacific coasts.
Given such preliminary observation, in this paper
quantitatively evaluate if the morphology of the species
present in our sampled sites differs from that reported, for
the same set of species, in previous studies in other Mexican
localities.
MATERIAL AND METHODS
Study site. Assemblages of turfing algae were
sampled at five sites on the tropical Pacific coasts of Mexico
(Table 1). The climate in the region is very warm and
subhumid with rain during the summer (García 1973).
Maximum temperatures occur from June to August and the
minimum from February to March. The average yearly
temperature is 23 °C and the annual precipitation is 1 102.1
mm. The substrate at Ensenada de los Presos is composed
8
of rocks, cobbles and sand; the slope is 10 ° and the
maximum depth is 6 m. Fuerte San Diego is a 100 m long
dock supported by piles. Below the dock, the substrate is
composed of cement blocks, rocks, cobbles and sand; the
slope is 45 ° and the maximum water depth is 8 m. The
substrate in La Ropa and Las Gatas consists of sand and
rocky outcrops of various sizes; in both, the slope is 15 °
and the maximum water depth is 4 m and 5 m, respectively.
The bottom at El Yunque is rocky with a steep slope (45 °)
and a maximum depth of 12 m. In all localities, water
movement caused a constant replacement of sediment
resulting in a strong abrasion and light depletion.
Table 1. Sampling localities of turf-forming algal species on the coasts of
Guerrero State.
Tabla 1. Localidades de muestreo de las especies que forman céspedes
en las costas de Guerrero.
Study sites
Ubication
Ensenada de los Presos, Acapulco
15°49’43” N - 99°53’48” W
Muelle del Puerto, Acapulco
16°50’33” N - 99°54’19” W
Playa La Ropa, Zihuatanejo
17°39’21” N - 101°32’50” W
Playa Las Gatas, Zihuatanejo
17°37’17” N - 101°33’18” W
El Yunque, Zihuatanejo
17°36’35” N - 101°33’41” W
Sampling design. Within each location samples
were scraped from rocky surfaces and samples were
obtained from twelve 10 x 10 cm quadrants positioned at 2
m intervals along a single 25 m line transect. This sampling
was repeated in spring, summer, autumn and winter in 1992,
1993 and 1994. The samples were preserved in 4 % glycerin
formalin/sea water, and deposited in the Algal Section of the
Herbario de la Facultad de Ciencias (FCME), Universidad
Nacional Autónoma de México (UNAM). The corresponding
references are: PTM 4651-4663, 4670-4695, 4696-4708,
4709-4737, 4837-4848, 4849-4862, 4863-4919, 4920-4969,
4972-4986, 4987-5000, 5038-5087, 5088-5101, and 51025113.
Taxonomic identification and data analysis.
Specimens were identified and the morphological characters
to specific separation in each genera, established by different
authors, were used to determine the turf species (Setchell &
Gardner 1920; 1937; Dawson 1944; 1953; 1954; 1961; 1962;
1963a; 1963b; Taylor 1945; 1960; Hillis 1958; Earle 1969;
Abbott & Hollenberg 1976; León 1986; Rodríguez 1989;
Sentíes et al. 1990; León-Alvarez & González-González
1995; Sentíes 1995; Pedroche & Silva 1996. Only those
species without changes in the diagnostic characteristics
were considered. By this criterion, 20 species were
eliminated suggesting taxonomic problems or maybe the
presence of new species.
Overall characteristics previously utilized in specific
descriptions and taxonomic keys available for the American
López, Rodríguez, Candelaria-Silva t Intraspecific morphological variation in turf-forming algal species
Pacific algal species were used for the taxonomic
identification and to describe their variation, and to carry out
morphometric analyses of the specimens.
The morphometric variation of each character of
every species was analyzed by Statistica software in order
to obtain mean, and both standard deviation and error, and
to correlate it with character values of previous descriptions,
and the variation of each species was established, so that
45 species descriptions were elaborated. These specific
descriptions were compared with the authors descriptions
cited in Table 2. A comparative character analysis was
realized to determine the variation type and magnitude, and
then groups were formed.
RESULTS
All 45 identified algal species had previously been
reported in the intertidal or subtidal zones of the Mexican
tropical Pacific coast. One additional species of the genus
Lithophyllum was recognized. However, determination of its
species was not possible because reproductive structures
were absent; this species provided the substrate upon which
many other species grew.
Only five species were higher than 2 cm,
Grateloupia prolongata reached 4 cm in El Corsario, Padina
crispata and P. durvillaei measured 7-8 cm in La Ropa,
Caulerpa sertularioides with 7 cm, was the smallest height
reported in other sampling sites, and Halimeda discoidea of
11 cm height was collected in El Yunque.
The most frequent morphological variation was the
height reduction (Figure 1). The height measurements tended to fall in the lower end of the before reported height
range. Variation in more than one character was also
notorious, sometimes was the height and width or the height
and thickness like Grateloupia versicolor (Figure 2). Another
set of species showed size reduction and other morphological
differences too. Reduction in cortical cell rows, utricular
dimensions, and cortical cell diameter, absence of prostrate
thalli, prostrate branches, lenticular thickness, and rhizoids,
changes in distance between branchlets, and in length and
width of nodes and internodes like Ceramium paniculatum
(Figure 3) were observed on sporophyte vegetative
structures. Shifts in reproductive structures such as reduction
of cystocarps diameter, increment of spores diameter,
tetrasporangia length, or absence of involucre were observed
too.
Phyilodictyon anastomosans
Padina durvillaai
Grateloupia versicolor
Gelidum mgnabbiana
Dictyopteris delicatula
Champia parvula
Ceramium paniculalum
Causlerpa sertularioides
Bryopsis perrata
Acetabularia parbula
Figure 2. Height (mm) and thickness (µm) of Grateloupia versicolor from
the coasts of Guerrero in this study (1) and from the literature (2).
Figura 2. Altura (mm) y grosor (µm) de Grateloupia versicolor de las
costas de Guerrero de este trabajo (1) y de la literatura (2).
Figure 1. Mean (± SD, SE) of height thalli (cm) of the species from the
coasts of Guerrero studied in this study (1) and mean values for the species
obtained from the literature (2).
Figura 1. Promedio (± SD, SE) de la altura de los talos (cm) de las especies de las costas de Guerrero en este trabajo (1) y los valores promedios de las especies obtenidos de la literatura (2).
Figure 3. Height (mm), nodes diameter (µm) and nodes longitude (µm)
of Ceramium paniculatum from the coasts of Guerrero in this study (1)
and from the literature (2).
Figura 3. Altura (mm), diámetro de los nodos (µm) y longitud de los nodos
(µm) de Ceramium paniculatum de las costas de Guerrero de este trabajo (1) y de la literatura (2).
9
UNIVERSIDAD Y CIENCIA
Número Especial I
Table 2. Morphological variations of the subtidal algal species in the coasts of Guerrero (* species without both, size reduction and other morphological
shifts).
Tabla 2. Variaciones morfológicas de las especies algales submareales en las costas de Guerrero (* especies sin reducción de la talla y sin otros cambios
morfológicos).
Species
Size reduction
Other morphological shifts
References
Thalli 0.5-1.0 cm high, which are
2.6-4.0 cm smaller than previously
reported. Axis diameter 36-210 µm
which is 10-334 µm smaller than
previously reported
Distance between branchlets 33-403 µm,
which extends the lower limit
previously recorded as 3 mm
Setchell & Gardner 1920, Taylor
1945, Abbott & Hollenberg 1976
Caulerpa sertularioides
(S. Gmelin) Howe
Thalli 2.0-7.0 cm high, which are
8.0-11.0 cm smaller than previously
registered
The pinnules had a small basal
constriction, which has not been
reported before
Taylor 1960
Codium picturatum
Pedroche et Silva
Without size reduction
Utricular length is (188.5) 210-465
(517) µm, which extends the lower
limit previously reported as (270)
400-900 (1 200) µm.
Utricular diameter is 19.31-48.84 µm,
which extends the lower interval observed
as (38) 55-85 (125) µm
Pedroche & Silva 1996
Chlorophyta
Bryopsis pennata Lamouroux
*Halimeda discoidea Decaisne
Hillis 1958, Taylor 1960
Phyllodictyon anastomosans
(Harvey) Piccone et Grunow ex
Piccone
Thalli 0.5-1.5 cm high, which is
2.5-4.5 cm smaller than previously
recorded
Without other morphological shifts
Acetabularia parvula
(Solms-Laubach) Schnetter
et Bula Meyer
Thalli 1.0-2.0 cm high, which is cm
5.0-6.0 mm smaller than previously
reported
Spores 79-131.5 µm diameter, which extend Taylor 1945, León 1986
the lower and upper limits previously
registered as 104-117 µm
Thalli 0.5-1.5 cm high, which are
1.5-7.5 cm smaller than previously
registered
Without other morphological shifts
Earle 1969
Thalli are always prostrate and have
moniliform rhizoids only
Taylor 1945
Phaeophyta
Dictyopteris delicatula
Lamouroux
Lobophora variegata (Lamouroux) Without size reduction
Womersley ex Oliveira
*Padina crispata Thivy
Padina durvillaei Harvey
Taylor 1945
Thalli 7-8 cm high, which are 32-33
cm smaller than previously reported
Without other morphological shifts
*Padina mexicana Dawson
Ralfsia hancockii Dawson
Taylor 1960
Taylor 1945
Dawson 1944
*Ralfsia pacifica Hollenberg
León-Alvarez & GonzálezGonzález 1995
Hollenberg 1969
*Sphacelaria rigidula Kützing
Abbott & Hollenberg 1976
Rhodophyta
*Asparagopsis taxiformis (Delile)
Trevisan(phase Falkenbergia)
Abbott & Hollenberg 1976
*Amphiroa beauvoisii Lamouroux
Norris 1981
*Amphiroa misakiensis Yendo
Norris 1981
10
Without size reduction
Rhizoids are absent
López, Rodríguez, Candelaria-Silva t Intraspecific morphological variation in turf-forming algal species
Table 2.
Species
Size reduction
Other morphological shifts
References
*Amphiroa rigida Lamouroux
Norris 1981
*Amphiroa valonioides Yendo
Norris 1981
*Callithamnion paschale Börgesen
Dawson 1962, Taylor 1945
*Ceramium flaccidum (Kützing)
Ardissone
Dawson 1962
*Ceramium hamatispinum Dawson
Dawson 1962
Ceramium mazatlanense Dawson Without size reduction
Tetrasporangia 42.5-50 µm diameter,
which extends the upper limit previously
reported as 30 µm. Tetrasporangi
lack involucres
Dawson 1962
Ceramium paniculatum Okamura
Thalli 5.0 mm high, which are
3.0-7.0 mm smaller than
previously reported
Node diameter 75-88 µm, which extends
the lower limit previously reported as
150 µm
Upper internodes 2 µm in length, which
extend the lower limit previously recorded
as 15-20 µm long
Dawson 1962
Ceramium sinicola Setchell et
Gardner
Thalli 3.0-5.0 mm high which
are 7.0-27.0 mm smaller than
previously registered
Without other morphological shifts
Dawson 1962
Ceramium vagans Silva
Thalli to 2.0 mm high, which
are 2.0-3.0 mm smaller than
previsouly reported.
Erect axes 62.5-125 µm diameter,
which extend the lower limit
previously reported as 120-140 µm
Without other morphological shifts
Dawson 1962
Champia parvula (C. Agardh)
Harvey
Thalli 0.3-0.8 cm high, which are
0.7-1.7 (5.7) cm smaller than
previously reported
Without other morphological shifts
Dawson 1963
Chondria decipiens Kylin
Thalli 0.5-1.3 cm high, which are
7.5-15.5 cm smaller than
previously recorded
Without other morphological shifts
Dawson 1963
*Gelidiopsis tenuis Setchell et
Gardner
Gelidium mcnabbiana (Dawson )
Santelices
Dawson 1944
Thalli 2.0 cm high, which are 5.0 cm
smaller than previously reported
Without other morphological shifts
*Gelidium sclerophyllum Taylor
Rodríguez 1989
Rodríguez 1989
Grateloupia prolongata J. Agardh
Thalli 4.0 cm high, which are 4.016.0 cm smaller than previously
reported.
Thickness 460-513 µm, which
extends the upper limit previously
registered as 250-400 µm
There are 2 rows of cortical cells,
which are 3 times smaller than
previously reported. Cortical cells 5 7.5 µm diameter, which increase the
upper limit previously reported as 1.5 µm
Dawson 1954
Grateloupia versicolor J. Agardh
(J. Agardh)
Thalli 170-150 µm thick, which
extend the lower limit previously
recorded as 300-500 µm
Without other morphological shifts
Dawson 1954
*Hypnea pannosa J. Agardh
Dawson 1961
11
UNIVERSIDAD Y CIENCIA
Número Especial I
Table 2.
Species
Size reduction
Other morphological shifts
References
*Hypnea spinella (C. Agardh)
Kützing
Dawson 1961
*Jania tenella (Kützing) Grunow
Dawson 1953
Laurencia clarionensis Setchell
et Gardner
Without size reduction
The lenticular thickness are absent
*Peyssonnelia rubra (Greville)
J. Agardh
Dawson 1963
Abbott & Hollenberg 1976,
Denizot 1968
Pterocladiella caloglossoides
Thalli 55-145 µm thick, which
(Howe) Santelices et Hommersand extend the lower limit previously
reported as 300-500 µm
Without other morphological shifts
Dawson 1953
Polysiphonia confusa
Erect branches 123-172 µm
diameter, which is 30-60 µm wider
than previously registered
Without other morphological shifts
Sentíes 1995
Polysiphonia mollis J. Hooker
et Harvey
Thalli 0.5-2.0 cm, which are 0.5 cm
smaller than previously recorded
Prostrate branches absent
Sentíes 1995
*Polysiphonia sertularioides
(Grateloup) J. Agardh
Sentíes 1995
*Polysiphonia simplex Hollenberg
Sentíes 1995
Polysiphonia sphaerocarpa
Börgesen
Without size reduction
Cystocarps 100-133 µm diameter, which
is 100-246 µm smaller than previously
registered
Sentíes 1995
Polysiphonia subtilissima
Montagne
Thalli to 0.5 cm high, which are
0.5-1.5 cm smaller than previously
reported
Without other morphological shifts
Sentíes 1995
Figure 4. Frequency of the types of morphological responses of Turfforming algal in the coasts of Guerrero (Type 1: species with a reduction
in overall thallus size, but within of the specific variation previously reported.
Type 2: species with modifications in thallus size, but beyond the specific
variation previously recorded. Type 3: species with modification of
vegetative structures. Type 4: species with modification of reproductive
structures. Type 5: species with modification of both, vegetative structures
and thallus size. Type 6: species with modification of both, reproductive
structures and thallus size).
Figura 4. Frecuencia de los tipos de respuestas morfológicas de algas
cespitosas en las costas de Guerrero (Tipo 1: especies con una reducción en la talla del talo, pero dentro de la variación registrada previamente para especie. Tipo 2: especies con modificaciones en la talla del talo
que sobrepasan la variación previamente observada para la especie.
Tipo 3: especies con modificaciones de las estructuras vegetativas. Tipo
4: especies con modificaciones en las estructuras reproductivas. Tipo 5:
especies con modificaciones de las estructuras vegetativas y la talla del
talo. Tipo 6: especies con modificaciones de las estructuras reproductivas
y la talla del talo).
12
Six types of morphological responses were
recognized in the base of the morphological variation of turf
forming species. The percentage of frequency for each type
of morphological response suggests that type 1 response
was predominant, and both type 2 and type 5 were frequent
(Figure 4).
These six types were: Type 1, a reduction in overall
thallus size, but within the specific variation previously
reported, and with no other apparent morphological
differences, included 21 species. Type 2, modifications in
thallus size, but beyond the specific variation previously
recorded, and without other apparent morphological
differences, formed by 12 species. Type 3, modification of
vegetative structures, grouped 4 species. Type 4,
modification of reproductive structures, with two species.
Type 5, included five species with modification of vegetative
structures and thallus size. Type 6, with one species only,
showed modification of reproductive structures and thallus
size.
DISCUSSION
Morphological shifts have been shown for several
intertidal and subtidal algal species for long time ago (Norton
López, Rodríguez, Candelaria-Silva t Intraspecific morphological variation in turf-forming algal species
et al. 1981). Thalli size has been suggested as an important
trait in determining survival of algae on intertidal habitats
(Carrington 1990; Gaylord et al. 1994). Results from this
study showed a marked reduction of size in the most species
suggesting it as a response to particular environmental
disturbance such as light depletion, sedimentation, abrasion
and grazing. The size reduction has been considered as a
collective and similar response of the turf growth form.
Recently, shifts on the thallus cortication,
calcification and thickness and complexity of branching have
been reported for turf forming algal species (Airoldi 2001).
The data of this study are in concordance with
morphological shifts observed from other regions. The six
types of morphological responses could be considered as
different strategies of algal species to adjust their growth
patterns to form turfs. For example, the reduction of utricle
size without modifying the overall size of Codium picturatum
(type 3) result in looser thalli that require less energy for
development. Differences in spore size which can lead to
variations in thallus height; in Acetabularia parvula (type 6)
for example increased the variation interval of these
structures.
Currently, it is accepted that the turf phenomenon
is a strategy to increase survival under changing
environmental conditions (Lewis 1985; 1986; Hackney et al.
1989). The results of this research strengthen this proposal,
as well as suggest that algal turfs are the consequence of
expression of a set of dissimilar morphological specific
responses which give a collective homogeneous appearance
of the turf. Additionally, each species can modified its
morphology in different habitats, for example the turf thalli
are shorter, more erect, and more highly branched and
compacted (Hay 1981), and the same species under different
environmental conditions are more sparsely or as discrete
thalli (Airoldi 2001).
The algal assemblage, described in this study, is
very similar to the turf growth form described by Hay (1981)
for areas that are subject to physical stress or moderate
grazing pressure. It has been also shown that associated to
such morphologies, turf-forming algae have mechanisms of
physiological adjustment, which possibly reduce survival
costs (Hay 1981). In this sense, this study provides an
important observational basis for assess the simultaneous
impact of the different environmental factors (abrasion,
deposition, grazing, light depletion) on phenotypic plasticity
of the turf forming species at Mexican tropical Pacific.
Finally, specific morphological differences observed
imply a sharp knowledge on that phenotypic plasticity for
each species which get important taxonomic meaning
because allows a better delimitation of species.
ACKNOWLEDGEMENTS
This work was funded by grant (DGAPA IN-214098)
of UNAM. The authors are grateful to Cheryl Patten for her
assistance with the last English version, to Ligia Collado and
Rodolfo Dirzo for the critical comments to drafts. We thank
Juan Manuel Barnard, Juan Carlos Huitrón and Héctor Ramos for their valuable field assistance.
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