Seagrass epiphyte blooms potentially have important economic and ecological consequences in Tampa Bay, one of the Gulf of Mexico’s largest estuaries. As part of a Tampa Bay pilot study to monitor the impact of environmental stresses,precise characterization of epiphyte diversity is required for efficient management of affected resources. Thus, epiphyte diversity may be used as a rational basis for assessment of ecosystem health. In May 2001, epiphytic species encompassing green, brown and red macroalgae were manually collected from dense and sparse seagrass beds of
Thalassia testudinum
and
Syringodium filiforme
. A total of 20 macroalgal epiphytes, 2 Chlorophyta, 2 Phaeophyta, and 16 Rhodophyta,were found on
T. testudinum
and
S. filiforme
seagrass at the four sampling sites (Bishop Harbor, Cockroach Bay, Feather Sound, and Mariposa Key). The Rhodophyta, represented by 16 species, dominated the numbers of species. Among them, the thin-crusted
Hydrolithon farinosum
was the most commonly found epiphyte on seagrass leaves. Species number, as well as species frequency of epiphytes, is higher at dense seagrass sites than sparse seagrass sites. Four attachment patterns of epiphytes can be classified according to cortex and rhizoid development: 1) creeping, 2) erect,3) creeping & erect, and 4) erect & holding. The creeping type is characterized by an encrusting thallus without a rhizoid or holdfast base. Characteristics of the erect type include a filamentous thallus with or without a cortex, and a rhizoid or holdfast base. The creeping and erect type is characterized by a filamentous thallus with a cortex and rhizoid. A filamentous thallus with a cortex, holdfast base, and host holding branch is characteristics of the erect and holdfast attachment type. This study characterized each species found on the seagrass for epiphyte identification.
INTRODUCTION
Seagrass meadows are very productive ecosystems of which a large proportion is often attributed to epiphytes(Heijs 1984, Leliaert et al. 2001). Seven seagrass species occur in Florida:
Syringodium filiforme, Halodule beaudettei, Halophila johnsonii, Thalassia testudinum, Halophila decipiens, Halophila engelmannii
and
Ruppia maritima
(Virnstein and Cairns 1986, Dawes et al. 1995). Seagrass affects sedimentation by baffling currents with long leaves and providing substrates suitable for diverse epiphytic biota (Land 1970, Almasi et al. 1987, Koch 1999,Hemminga and Duarte 2000). Among these,
T. testudinum
(Banks ex König) and
S. filiforme
(Kützing) dominate in the Caribbean Sea and Gulf of Mexico (Eiseman 1980).
Seagrass epiphytes are very important components of the meadows. At least 113 epiphytes and up to 120 macroalgal species have been identified from Florida seagrass blades and communities, respectively (Dawes 1987). Although lists and ecological studies about epiphytes on
T. testudinum
and
S. filiforme
have been conducted, studies have not reported detailed characterization of macroalgal epiphytes on these grasses.
This paper characterizes macroalgal epiphytes and determines attachment patterns on seagrass blades of
T. testudinum
and
S. filiforme
. This study also compares macroalgal species composition between sites of sparse and dense seagrass beds.
MATERIALS AND METHODS
During the spring of 2002, seagrass shoots of
T. testudinum
and
S. filiforme
with epiphytes were collected from different subtidal biotopes at four sites around Tampa Bay, Florida, USA: Bishop Harbor, Cockroach Bay, Feather Sound, and Mariposa Key. To compare dense and sparse sites, seagrass beds were sampled by 50 cm × 50 cm quadrates. All samples were labeled and preserved in a 4% formaldehyde seawater solution for morphological observation. A detailed study of the epiphytes was carried out in the laboratory. Under a stereomicroscope, all epiphytes were separated from the seagrass leaves by gentle scraping. Epiphytes were stained with 1% aqueous aniline blue for anatomical study, characterization of macro-algal epiphytes, and species identification. Twenty-five seagrass leaves were selected and collected from each sparse and dense site. The number of all epiphytes on each blade was counted to compare species
Comparison of epiphyte attachment patterns on Syringodium filiforme and Thalassia testudinum
Comparison of epiphyte attachment patterns on Syringodium filiforme and Thalassia testudinum
abundance of epiphytes between sparse and dense sites.
RESULTS AND DISCUSSION
- Epiphytic species composition, species abundance,and attachment pattern
As shown in
Table 1
, a total of 20 macroalgal epiphytes (2 Chlorophyta, 2 Phaeophyta, and 16 Rhodophyta) are found in
T. testudinum
and
S. filiforme
seagrass beds at the four sampling sites. Of them, four taxa,
Acrochaetium, Griffithsia, Gayliella,
and
Ceramium
, are not identified to species level because only single or small sized plants were found. Thus, sample size is insufficient for identification.This is relatively restricted when compared to other similar studies in Florida. Humm (1964) observed 113 species on
T. testudinum
in South Florida, and Ballantine and Humm (1975) mentioned 66 epiphytes on the 4 seagrass species in Florida. In this study, the number of epiphytes is less than in previous studies because previous research studies were conducted over several seasons.
Rhodophyta exceeds 80% at the total species number. Of them, the thin-crusted
Hydrolithon farinosum
is the most commonly found epiphyte on seagrass leaves. It is similar to other results that indicate crustose Corallinaceae are the dominant epiphytic species on seagrasses (Heijs 1984, Leliaert et al. 2001). Although the epiphyte species of the genus
Spyridia
and
Hypnea
have been reported as drift macroalgae in seagrass systems (Dawes et al. 1985), they are also typical epiphytes on the seagrass in this study.
The total species number of epiphytes on each narrow
S. filiforme
and wide
T. testudinum
is similar. However, epiphytic composition differs strongly between
T. testudinum
and
S. filiforme
even though they were collected from the same locality.
Enteromorpha flexuosa, Sphacelaria rigidula, Griffithsia
sp., and
Ceramium
sp. are found only on
S. filiforme
seagrass beds, while
Cladophora prolifera,Hydrolithon farinosum, Hypnea valentiae
, and
Heterosiphonia crispella
are found only on
T. testudinum
seagrass beds.
Species number, as well as species frequency, of epiphytes is higher at dense seagrass sites than sparse seagrass sites. Fourteen epiphytes were identified from dense sites of
S. filiforme
seagrass beds, while 11 were identified from sparse sites. Five species,
E. flexuosa, S. rigidula, Gayliella sp, Ceramium
sp.
Herposiphonia tenella
, were collected only from dense sites, while two others,
Acrochaetium
sp.,
Griffithsia
sp., were only collected from sparse sites. Fifteen epiphytes were identified from dense sites of
T. testudinum
seagrass beds, while 12 were identified from sparse sites. Four species,
C. prolifera, Hypnea musciformis, H. valentiae, H. tenella,
were collected from dense sites, while Heterosiphonia crispella was only collected from sparse sites. Since density of seagrass blades causes modifications of physical factors such as water movements, and it increases the possibil-
Abundance of epiphytic macroalgae expressed as the total number of individuals found on 25 Thalassia testudinum from each dense and sparse site.
ity of attachment of macroalgal epiphytes to seagrass blades, a larger number of epiphytes may occur in dense sites. Species frequency of epiphytes on each blade of
T. testudinum
is also larger in dense sites (
Fig. 1
)
As summarized in
Table 1
, four attachment patterns of epiphytes can be classified according to development of cortex and rhizoid: 1) creeping, 2) erect, 3) creeping & erect, and 4) erect & holding. The creeping type is characterized by an encrusting thallus without a rhizoid or holdfast base. This type is found in
Hydrolithon farinosum
. The erect type is characterized by a filamentous thallus with or without a cortex, and a rhizoid or holdfast base. This type is found in
E. flexuosa, C. prolifera, Hincksia mitchelliae, S. rigidula, Stylonema alsidii, Hypnea spinella, H. valentiae, Champia parvula, Polysiphonia flaccidissima, H. crispella, Chondria collinsiana, Acrochaetium
sp., and
Griffithsia
sp. The creeping and erect type is characterized by a filamentous thallus with a cortex and rhizoid. This type is found in
Centroceras gasparrinii,H. tenella, Gayliella
sp., and
Ceramium
sp. The erect and holdfast type is characterized by a filamentous thallus with a cortex, holdfast base, and host holding branch. This type is found in
H. musciformis
and
Spyr-
idia filamentosa.
Epiphytes with erect attachment patterns are common at dense sites, while epiphytes with creeping and erect attachment patterns are common at sparse sites.
- List and characterization of epiphytes
Although most of these epiphytic species have previously been reported from Florida (Dawes 1987, Littler and Littler 2000), we characterize each species with detailed morphology.
- Chlorophyta
Enteromorpha flexuosa
(Wulfen) J. Agardh 1883 (
Fig. 2
& 3)Basionym:
Ulva flexuosa
Wulfen 1803.
Vegetative thallus. Figs 2 & 3. Enteromorpha flexuosa
Cross section view. Scale bars represent: Fig. 2 1 mm; Fig. 3 100 ㎛
Vegetative thallus Figs 4-7. Cladophora prolifera
Upper part of thallus Figs 4-7. Cladophora prolifera
Dichotomous branching Figs 4-7. Cladophora prolifera
Trichotomous branching. Scale bars represent: Fig. 4 l mm; Fig. 5 100 μm; Fig. 6 40 μm; Fig. 7 40 μm Figs 4-7. Cladophora prolifera
Vegetative thallus with tapering apices (arrows). Figs 8-10. Hincksia mitchelliae
Reproductive thallus Figs 8-10. Hincksia mitchelliae
Branch with plurilocular sporangia (S). Scale bars represent: Fig. 8 0.5 mm; Fig. 9 100 μm; Fig. 10 40 μm. Figs 8-10. Hincksia mitchelliae
Vegetative thallus Figs 11 & 12. Sphacelaria rigidula
Slender biradiate propagula (P). Scale bars represent: Fig. 11 0.5 mm; Fig. 12 100 μm. Figs 11 & 12. Sphacelaria rigidula
The thallus is slender, erect, and about 1 cm high. Blades taper toward base and are cylindrical and hollow. Rhizoids form a tightly knit basal pad.
Cladophora prolifera
(Roth) Kützing 1843 (
Figs 4
-
7
) Basionym:
Conferva prolifera
Roth 1797; 182.
The thallus is filamentous, pseudo-dichotomous or pseudo-trichotomous, branching, erect, and about 1 cm high. Filaments are straight to slightly curved. Rhizoids are formed from basal cells.
- Phaeophyta
Hincksia mitchelliae (Harvey) P. C. Silva in Silva et al. 1987 (
Figs 8
-
10
)
Basionym:
Ectocarpus mitchelliae
Harvey 1852; 142.
The thallus is filamentous tufts or mats, erect, and 0.5 cm high. Filaments are irregularly branched, and taper toward apices. Plurilocular sporangia are cylindrical, rarely stalked, and lateral on filaments.
Sphacelaria rigidula
Kützing 1843 (
Fig. 11
&
12
)
The thallus is filamentous, erect, and 0.3 cm high. Filaments are straight and cylindrical. Propagules have 2-3 cylindrical arms.
- Rhodophyta
Stylonema alsidii
(Zanardini) Drew 1956 (
Fig. 13
&
14
) Basionym:
Bangia alsidii
Zanardini 1839; 136.
The thallus is erect, pseudodichotomously branched, and 0.2-0.3 cm high. Cells are discoid to ellipsoid.
Acrochaetium
sp. (
Fig. 15
-
17
)
The thallus is filamentous, erect, and 0.3-0.5 cm high. Cells are cylindrical or rod-shaped. Monosporangia are basal in lateral clusters and develop adaxially at the upper part of the cell.
Hydrolithon farinosum
(J. V. Lamouroux) Penrose & Y. M. Chamberlain 1993 (
Fig. 18
-
24
) Basionym:
Melobesia farinose
J. V. Lamouroux 1816; 315.
The thallus is prostrate, thin, crusts, develops from an initial four-celled structure, and measures 0.3-0.5 cm diam. Tetrasporangial conceptacles are hemispherical and tetrasporangia are zonately divided.
Hypnea musciformis
(Wulfen) J. V. Lamouroux 1813 (
Figs 25
-
29
) Basionym:
Fucus musciformis
Wulfen in Jacquin 1791; 154.
The thallus is tangled, wiry, erect, then coiled, and about 10-15 cm high. Apices are slightly upcurved, flattened hooks. Holdfast is disc-like, becoming more tangled by the coiled apex.
H. spinella
(C. Agardh) Kutzing 1847 (
Fig. 30
-
33
) Basionym:
Sphaerococcus spinellus
C. Agardh 1822; 323.
The thallus is wiry, erect, and 5-6 cm. Apices are tapering and pointed, but not upcurved. Branchlets are spine-like and numerous. Holdfast is disc-like.
H. valentiae
(Turner) Montagne1841 (
Fig. 34
-
36
) Basionym:
Fucus valentiae
Turner 1808-1809; 17.
The thallus is tough, wiry, erect, and 7-8 cm high. Apices are tapering and pointed, but not upcurved. Branchlets are spine-like and star-shaped with up to six points. Holdfast is disc-like.
Champia parvula
(C. Agardh) Harvey 1853 (
Fig. 37
-
50
)Basionym:
Chondria parvula
C. Agardh 1824; 207.
The thallus is gelatinous, alternately branching, erect, and about 3-5 cm high. Branches are cylindrical to slightly flattened. Apices are bluntly pointed. Segments are swollen or barrel-shaped. The inner wall is lined with faint longitudinal filaments with sparsely scattered and oval gland cells. Spermatangia are in swollen spermatangial sori and produced from cortical cells. Cystocarps are protuberant with wide ostioles. Tetrasporangia are spherical, tetrahedrally divided, and produced on the inner side of cortical cell.
Griffithsia
sp. (
Fig. 51
)
The thallus is monosiphonous, dichotomous, erect, and 1 cm high. Sterile filaments are whorled at upper ends of segments and trichotomously branched.
Centroceras gasparrinii
(Meneghini) Kützing 1849 (
Figs 52
-
58
)
The thallus is filamentous, dichotomous, creeping and erect, and 2-4 cm high. Apices are incurved. The cortex is complete and has whorled spines. Spermatangia are in the terminal clusters of the node. Tetrasporangia are spherical, produced from periaxial cells, and protected by involucral branchlets. Recently, Won et al. (2009) resurrected this species based on morphological and molecular evidence.
Gayliella
sp. (
Figs 59
&
60
)
The thallus consists of prostrate axes giving rise to erect axes, and is 0.2-0.3 cm high. The axis has four periaxial cells. Three cortical initials are produced per periaxial cell. Of them, basipetal cortical cells are produced horizontally and grow basipetally. This species is similar to
Gayliella transversalis
(Collins and Hervey) T. O. Cho and Fredericq reported from Key West, Florida by Cho et al. (2008), in that it may be distinguished by branching pattern.
Ceramium
sp. (
Figs 61
&
62
)
The thallus is simple, filamentous, pseudo-dichotomous, creeping and erect, and 0.5 cm high. Cortication is incomplete. Two cortical cells are acropetally produced from a peraxial cell.
Herposiphonia tenella
(C. Agardh) Ambronn 1880 (
Fig. 63
)Basionym:
Hutchinsia tenella
C. Agardh 1828; 105.
Vegetative thallus. Fig. 13 & 14. Stylonema alsidii
Upper part of thallus with branch initials (arrow). Scale bars represent: Fig.13 40 μm; Fig. 14 40 μm. Fig. 13 & 14. Stylonema alsidii
Vegetative thallus Fig. 15-17. Acrochaetium sp
Upper part of thallus with monosporangia (arrows). Fig. 15-17. Acrochaetium sp
Lower part of thallus with holdfast. Scale bars represent: Fig. 15 100 μm; Fig. 16 40 μm; Fig. 17 40 μm Fig. 15-17. Acrochaetium sp
Vegetative thallus. Fig. 18-24. Hydrolithon farinosum
Four celled initials Fig. 18-24. Hydrolithon farinosum
Cross section view of thallus on seagrass Fig. 18-24. Hydrolithon farinosum
Female conceptacle Fig. 18-24. Hydrolithon farinosum
Cross section view of female conceptacle Fig. 18-24. Hydrolithon farinosum
Tetrasporangial conceptacle Fig. 18-24. Hydrolithon farinosum
Cross section view of tetrasporangial conceptacle having tetrasporangia (T). Scale bars represent: Fig. 18 100 μm; Fig. 19 10 μm; Fig. 20 40 μm; Fig. 21 20 μm; Fig. 22 40 μm; Fig. 23 20 μm; Fig. 24 40 μm.
Vegetative thallus Fig. 25-29. Hypnea musciformis
Curved apex Fig. 25-29. Hypnea musciformis
Coiled apex. Fig. 25-29. Hypnea musciformis
Tangled branches (arrow). Fig. 25-29. Hypnea musciformis
Cross section view of thallus. Scale bars represent: Fig. 25 1 mm; Fig. 26 0.5 mm; Fig. 27 0.5 mm; Fig. 28 1 mm; Fig. 29 50 μm. Fig. 25-29. Hypnea musciformis
Vegetative thallus Figs 30-33.
Upper part of thallus Figs 30-33.
Spine-like branchlets (arrows) on middle part of thallus Figs 30-33.
Cross section view of thallus. Scale bars represent: Fig. 30 1 mm; Fig. 31 1 mm; Fig. 32 0.5 mm; Fig. 33 50 μm. Figs 30-33.
Vegetative thallus Figs 34-36. Hypnea valentiae
Stellate branchlets (arrows) on middle part of thallus Figs 34-36. Hypnea valentiae
Cross section view of thallus. Scale bars represent: Fig. 34 1 mm; Fig. 35 0.5 mm; Fig. 36 50 μm. Figs 34-36. Hypnea valentiae
Vegetative thallus Figs 37-50. Champia parvula
Surface showing the scattered small cells Figs 37-50. Champia parvula
Cross section view through node. Figs 37-50. Champia parvula
Cross section view through internode Figs 37-50. Champia parvula
Longitudinal section view of upper thallus Figs 37-50. Champia parvula
Longitudinal section view of nodal part. Figs 37-50. Champia parvula
Longitudinal section view showing gland cell (arrow head) and longitudinal filaments (arrow). Figs 37-50. Champia parvula
Male branch with spermatangial sori. Figs 37-50. Champia parvula
Surface of spermatangial sori Figs 37-50. Champia parvula
Cross section of male branch with spermatangia (S). Figs 37-50. Champia parvula
Female thallus with cystocarp (C). Figs 37-50. Champia parvula
Longitudinal section of cystocarp with carpospores Figs 37-50. Champia parvula
Surface of tetrasporic thallus with tetrasporangia (T). Figs 37-50. Champia parvula
Cross section of tetrasporic thallus showing tetrasporangium developed from cortical cell. Scale bars represent: Fig. 37 1 mm; Fig. 38 40 μm; Fig. 39 50 μm; Fig. 40 50 μm; Fig. 41 100 μm; Fig. 42 50 μm; Fig. 43 20 μm; Fig. 44 0.5 mm; Fig. 45 40 μm; Fig. 46 40 μm; Fig. 47 100 μm; Fig. 48 100 μm; Fig. 49 100 μm; Fig. 50 20 μm. Figs 37-50. Champia parvula
Griffithsia sp. Fig. 51. Vegetative thallus. Scale bar represents: 0.5 mm.
Vegetative thallus. Figs 52-58. Centroceras gasparrinii
Cross section view through cortical node Figs 52-58. Centroceras gasparrinii
Cross section view through internode Figs 52-58. Centroceras gasparrinii
Creeping part of lower thallus having rhizoids (R). Figs 52-58. Centroceras gasparrinii
Cortical node with spermatangia (S) of male thallus Figs 52-58. Centroceras gasparrinii
Tetrasporangial thallus Figs 52-58. Centroceras gasparrinii
Tetrasporangia (T) with involucral branches (arrows) in abaxial side. Scale bars represent: Fig. 52 0.5 mm; Fig. 53 20 μm; Fig. 54 20 μm; Fig. 55 100 μm; Fig. 56 40 μm; Fig. 57 0.5 mm; Fig. 58 50 μm. Figs 52-58. Centroceras gasparrinii
Vegetative thallus Figs 59 & 60. Gayliella sp
Creeping and erect parts of thallus. Scale bars represent: Fig. 59 50 μm; Fig. 60 100 μm. Figs 59 & 60. Gayliella sp
Vegetative thallus Figs 61 & 62. Ceramium sp
Cortical nodes. Scale bars represent: Fig. 61 100 μm; Fig. 62 20 μm. Figs 61 & 62. Ceramium sp
Herposiphonia tenella Fig. 63. Male thallus. Scale bar represents: 100 μm.
Thallus. Figs 64-67. Polysiphonia flacidissima
Apex with prominent scar cells (arrow). Figs 64-67. Polysiphonia flacidissima
Cross section of thallus Figs 64-67. Polysiphonia flacidissima
Cystocarp. Scale bars represent: Fig. 64 0.5 mm; Fig. 65 40 μm; Fig. 66 20 μm; Fig. 67 100 μm. Figs 64-67. Polysiphonia flacidissima
Vegetative thallus. Figs 68-70. Spyridia filamentosa.
Surface of axis Figs 68-70. Spyridia filamentosa.
Tangled branches (arrow). Scale bars represent: Fig. 68 0.5 mm; Fig. 69 40 μm; Fig. 70 1 mm. Figs 68-70. Spyridia filamentosa.
Vegetative thallus Figs 71 & 72. Heterosiphonia crispella
Branchlet. Scale bars represent: Fig. 71 0.5 mm; Fig. 72 100 μm.
The thallus is tangled, prostrate, creeping and erect, and 0.5 cm high. Branching is irregularly alternate. Rhizoids arise from each node.
Polysiphonia flaccidissima
Hollenberg 1942 (
Figs 64
-
67
)
The thallus is filamentous, erect, and 0.3 cm high. Branching is irregularly alternate with four pericentral cells. Scar cells are common between segments and apical filaments are highly branched. Cystocarps are spherical and on short stalk.
Spyridia filamentosa
(Wulfen) Harvey in W. Hooker 1833 (
Fig. 68
-
70
) Basionym:
Fucus filamentousus
Wulfen 1803; 64.
The thallus is filamentous, erect and then coiled, and about 7 cm high. Branchlets are delicate and unbranched, with incomplete cortication.
Heterosiphonia crispella
(C. Agardh) M. J. Wynne 1985 (
Fig. 71
&
72
) Basionym:
Callithamnion crispellum
C. Agardh 1828; 183.
The thallus is delicate, erect, not corticated, and 0.4 cm high. Branchlets are deciduous, and dichotomously to alternately branched. Our material is at a young plant stage.
Chondria collinsiana
M. Howe 1920 (
Fig. 73
-
85
)
The thallus is solitary, erect, and 0.8-1.2 cm high. There are 5-6 pericentral cells. Apices are truncate to slightly rounded and tufted with dichotomously branched fila-
Vegetative thallus. Fig. 73-85. Chondria collinsiana
Surface view of thallus Fig. 73-85. Chondria collinsiana
Apex. Fig. 73-85. Chondria collinsiana
Cross section of thallus. Fig. 73-85. Chondria collinsiana
Apical cell (arrow) of branch Fig. 73-85. Chondria collinsiana
Male thallus Fig. 73-85. Chondria collinsiana
Male apex with flat disc like spermatangial sorus (arrows). Fig. 73-85. Chondria collinsiana
Spermatangial sorus with spermatangia (S). Fig. 73-85. Chondria collinsiana
Female thallus Fig. 73-85. Chondria collinsiana
Young cystocarp (C). Fig. 73-85. Chondria collinsiana
Tetrasporic thallus Fig. 73-85. Chondria collinsiana
Cross section of tetrasporic thallus with tetrasporangia (T). Fig. 73-85. Chondria collinsiana
Tetrasporangium developed from a pericentral cell (P). Scale bars represent: Fig. 73 0.25 mm; Fig. 74 40 μm; Fig. 75 100 μm; Fig. 76 50 μm; Fig. 77 20 μm; Fig. 78 0.5 mm; Fig. 79 100 μm; Fig. 80 100 μm; Fig. 81 40 μm; Fig. 82 100 μm; Fig. 83 0.5 mm; Fig. 84 100 μm; Fig. 85 50 μm. Fig. 73-85. Chondria collinsiana
ments. Tetrasporangia are spherical, tetrahedrally divided, and produced on branchlets. Spermatangial sori are disc-shaped, circular to oval, flat, and form at the base of apical filaments. Cystocarps are on the short stalk and spherical to oval.
Acknowledgements
This work was supported by a 2009 research grant awarded to Tae Oh Cho by Chosun University.
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