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Seasonal and spatial variation in the distribution of mangrove macroalgae in the Clyde River, Australia
Estuarine, Coastal and Shelf Science 71 (2007) 683e690 www.elsevier.com/locate/ecss
Seasonal and spatial variation in the distribution of mangrove macroalgae in the Clyde River, Australia Felicity Melville*, Alex Pulkownik Department of Environmental Sciences, University of Technology, PO Box 123, Broadway, Sydney, NSW 2007, Australia Received 9 June 2006; accepted 21 September 2006 Available online 14 November 2006
Abstract The objective of this study was to determine whether there was significant spatial and temporal variation in macroalgae epiphytic on pneumatophores of the Grey Mangrove, Avicennia marina (Forsk.) Vierh., in the Clyde River, located 280 km south of Sydney, Australia. Three estuarine sites in the Clyde River were surveyed seasonally on four occasions over a two-year period, and algal distribution and abundance assessed in respect to temporal, inter-site, intertidal (from front to back of mangrove stand) and vertical (from bottom to top of pneumatophores) variation. Sediment and water characteristics, including nutrient levels, were also assessed in order to examine all variables of potential influence on algal distribution and abundance. The results indicated that intertidal position within sites, and vertical height along the length of the pneumatophore, were the greatest influence on algal frequency and biomass. Individual species dominated in different intertidal and vertical zones. These observations, together with the identification of three species of macroalgae that fulfil the criteria for bioindicators/biomonitors of environmental impacts are discussed. Ó 2006 Published by Elsevier Ltd. Keywords: mangrove; macroalgae; intertidal; pneumatophores; Clyde River; Australia
1. Introduction Mangroves can host diverse macroalgal assemblages that grow epiphytically on pneumatophores, prop roots, stems and other hard substrates (Zuccarello et al., 2001). The algae are exposed to the steep environmental gradients associated with the estuarine environment, including emersion and submersion during tidal cycles, and fluctuating temperature, salinity, light and nutrient conditions (Pregnall and Rudy, 1985). Such circumstances are unfavourable for most marine and freshwater algae, but mangrove-associated algae have adapted to this environment and flourished (Phillips et al., 1994). Like mangroves, mangrove macroalgae have an important role as primary producers in the estuarine ecosystem, through the production of organic material and contribution to nutrient * Corresponding author. Present address: Centre for Environmental Management, Central Queensland University, PO Box 1319, Gladstone, Qld 4680, Australia. E-mail address: [email protected] (F. Melville). 0272-7714/$ - see front matter Ó 2006 Published by Elsevier Ltd. doi:10.1016/j.ecss.2006.09.023
cycling, (Davey and Woelkerling, 1985; McClusky and Elliot, 2004). Macroalgae also function as food sources for grazing marine animals, and as a habitat for small estuarine invertebrates (Melville, 2005). Distinct patterns of macroalgal biogeography, and distribution and abundance of mangrove macroalgae in the intertidal zone, have emerged from the extensive studies carried out both in Australia (Davey and Woelkerling, 1985; King and Wheeler, 1985; King, 1990; King and Puttock, 1994; King, 1995), and overseas in other temperate mangrove ecosystems (Mann and Steinke, 1988; Phillips et al., 1994; Phillips et al., 1996; Broderick and Dawes, 1998). Although a number of factors have been shown to affect growth patterns, emersion frequency of the algae and species desiccation tolerance appear to be the most significant parameters (Druehl and Green, 1982; Zuccarello et al., 2001). Studies have found algal biomass to decline landwards from the water body, coinciding with the pneumatophores being emergent for successively longer periods during the tidal cycle (Davey and Woelkerling, 1985; Phillips et al., 1994). It has been suggested that the
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desiccation tolerance of algal species is the major determinant for their intertidal limit (Brown, 1987). Previous studies have found distributional differences among estuaries with differing pollution loads, in addition to correlations between sediment and algal metal concentrations (Melville, 2005; Melville and Pulkownik, 2006). However, inter-site and intra-site differences in distribution and biomass within the estuaries has not been addressed; nor was has temporal variability. This study examined the spatial and temporal variation of macroalgae epiphytic on pneumatophores (aerial roots) of the Grey mangrove, Avicennia marina (Forsk.) Vierh., in the Clyde River, located approximately 280 km south of Sydney, Australia. This study was part of a large-scale project assessing the potential of mangrove macroalgae as indicators of metal contamination in temperate estuaries (Melville, 2005; Melville and Pulkownik, 2006). The examination of the temporal and spatial variation exhibited by the macroalgae was an important component of the overall study. An understanding of the natural variation in species abundance and distribution (autoecology) is essential knowledge for any indicator species (Rainbow, 1995). The aim of this study was, therefore, to determine the extent of seasonal variation, and inter-site, intertidal and vertical zonation of mangrove macroalgae on pneumatophores of Avicennia marina (Forsk) Vierh. in the Clyde River estuary. A simultaneous study carried out in the Parramatta River in Sydney, Australia, indicated clear intertidal differences in algal distribution and abundance, but no spatial or temporal variation (Melville et al., 2005). The Clyde River estuary is a relatively pristine estuary located about 200 km from any major metropolitan area (Kirby
et al., 2001; Melville et al., 2004), whereas the Parramatta River estuary is located in the centre of Sydney, and has been shown to contain significantly higher pollutant concentrations (Melville et al., 2004; Melville, 2005; Melville and Pulkownik, 2006). Therefore, it is possible that the macroalgal zonation exhibited in the Parramatta River, may differ from those in the Clyde River. 2. Materials and methods 2.1. Site selection and study design Three study sites in the Clyde River (Fig. 1) were selected to give a range of estuarine water salinities. Mean salinities at Sites 1, 2 and 3 were approximately 20, 15 and 10 psu at low tide, respectively. However, these sites can experience wide fluctuations in salinity during king tides and rain events. At each site, three transects, 10 m apart, were set up along the tidal gradient, with three stations, each of approximately 4 m2, in different intertidal zones (front, mid and back) marked in each transect (Fig. 2). The stations at the front of the mangrove stand were situated approximately 1e2 m from the margin of the mangrove canopy at the waterline; stations in the back intertidal zone at 1e2 m from the stand transition into the terrestrial ecosystem; and in the mid-zone, halfway between the front and back zones (between 15 and 24 m in each site). 2.2. Site characteristics Vegetative characteristics of each site and zone were evaluated by estimating the average mangrove tree height and
N
Site 3
Site 2 Site 1
Fig. 1. Study sites in the Clyde River estuary, Australia.
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Transect B
Transect A
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2.5. Statistical analyses
Transect C
2m
Back zone (3)
Station A3
Mid zone (2)
Station A2
Front zone (1)
Station A1
Station B3 10m
Station B2 Station B1
Station C3 10m
Station C2
Edge of tree canopy
Station C1
2m
WATER Fig. 2. Experimental design for sampling in the Clyde River.
projective foliage cover (% PFC) at each station, as a measure of light availability to the pneumatophores, and, therefore, to the algae growing upon them. At each station, pneumatophore characteristics were also examined using 0.125 m2 quadrats. The number of pneumatophores in each quadrat, and their heights, were recorded, and pneumatophore density calculated as the number of pneumatophores per m2. The apex and basal width of pneumatophores were also measured, and used to calculate total pneumatophore surface area per m2. 2.3. Sample collection Summer and winter sampling was conducted over an 18 month period, during February and August 2002, and February and August 2003. Sediment samples were collected from each station within each intertidal zone; with 108 samples collected over the whole study. At each station, three pneumatophores were collected; with 324 collected over the whole study. Pneumatophores were cut at the mudline with clippers, sealed in plastic bags, and transported back to the laboratory on ice, for measurement and algal analyses. 2.4. Laboratory analyses Sediment samples were air-dried and sieved through a 2 mm mesh sieve (Allen, 1989). The <2 mm sediment fraction was then used to determine pH and salinity (as electrical conductivity in mS/cm) in 1:5 aqueous extracts, organic matter content (as % LOI, loss on ignition at 550 C), and total nitrogen and total phosphorus levels (mg kg1) (Allen, 1989; Rayment and Higginson, 1992). Pneumatophore height, and width at apex and base were recorded with callipers and pneumatophores cut into 5 cm vertical segments. Algae were scraped from each segment, taking care not to remove pneumatophore tissue, and stored separately in 4% formalin solution. The algal species were identified in each sample under a magnifying lamp using taxonomic literature (King and Wheeler, 1985; King and Puttock, 1994), separated and dried overnight at 45 C to determine biomass. Algal biomass was expressed on the basis of the surface area of each pneumatophore segment (g/m2), using previously determined dimensions of the pneumatophore. Frequencies for each algal species were calculated as the percentage of pneumatophores examined on which that species was detected.
To determine whether there were any significant spatial differences in site characteristics, pneumatophore heights or densities, Analyses of Variance were undertaken using General Linear Models (GLM, Minitab, Version 13.1, 2000). In all analyses, a ¼ 0.05. In order to examine the macroalgal community dynamics, non-metric Multidimensional Scaling, (MDS, Primer, Version 5.2.7, 2001) was used to provide a graphical depiction the influence of seasonal, site, intertidal and vertical segment variation on the algal community frequency and biomass. The raw algal data sets were square root transformed to achieve more equal weighting of the common and less common species, and using a Bray-Curtis distance measure, compiled into a similarity matrix, which was then used to calculate the MDS plot, using a variety of fixed factors. In these analyses, the MDS model offers a value, ‘stress’, to describe how well the ranked distance metrics between the samples are preserved, with low values indicating good preservation. In order to examine species-specific responses, GLM were then used to determine whether there were any significant differences, or interactions, among individual algal frequencies or biomass in regard to the factors examined in the MDS above (seasons, sites, intertidal zones and pneumatophore segments). 3. Results 3.1. Site characteristics Both water and sediment salinity were highest at Site 1 (Table 1), the most downstream site, and lowest at Site 3 (P < 0.001, F ¼ 5.26 and P ¼ 0.03, F ¼ 7.23 respectively, df ¼ 8, 25 for water and 35, 106 for sediment). Water salinities did not vary significantly over the four sampling periods (P ¼ 0.67, F ¼ 0.09). No significant differences in sediment pH, nitrogen and phosphorus levels, or sediment organic content were found among or within the study sites (Table 1). All sites consisted of trees of up to 10 m in height. Projective foliage cover was similar across all sites and intertidal zones (mean value 79 11%). Pneumatophore heights ranged from 6 to 13 cm, with a mean height of 9 cm (Table 2). Thus, two vertical pneumatophore segments were used to record Table 1 Water and sediment characteristics at study sites in the Clyde River estuary. Values are means SE, taken over four sampling surveys (n ¼ 27 and 108 for water and sediment, respectively) Characteristics
Site 1
Site 2
Site 3
Estuarine mean
Water salinity (psu) 20.4 0.5 15.7 0.5 10.5 0.3 15.5 3.5 Sediment salinity (mS/cm) 7.0 1.3 6.8 1.2 5.5 1.4 6.4 0.6 pH 6.3 0.1 6.3 0.1 6.5 0.1 6.4 0.1 Organic content (% LOI) 71 71 51 61 Nitrogen (mg/kg) 1.8 0.4 1.4 0.2 1.2 0.3 1.4 0.2 Phosphorus (mg/kg) 0.3 0.1 0.2 0.1 0.1 0.1 0.2 0.1
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Table 2 Pneumatophore characteristics at study sites in the Clyde River. Values are means SE (n ¼ 36). Density refers to the number of pneumatophores per m2. Surface area refers to the total surface area of pneumatophores (m2) per stand area (m2) Site
Intertidal zone
Mean Height (cm)
Density (no/m)
Surface area (m2/m2)
1
Front Mid Back
82 12 1 12 2
544 71 779 137 517 141
1.9 0.6 2.1 0.7 1.2 0.5
2
Front Mid Back
62 93 13 3
699 164 512 227 389 69
1.7 0.7 1.3 0.5 1.3 0.5
3
Front Mid Back Mean
61 72 91 91
1040 115 731 227 576 52 643 50
1.6 0.3 1.8 0.8 2.1 0.7 1.4 0.6
algal distribution: basal (0 to 5 cm from the mudline) and apex (>5 cm). Although pneumatophore heights, densities and total surface area did not vary significantly among the sites (P ¼ 0.24, F ¼ 0.27, df ¼ 107, 322), within each site pneumatophores were taller in the mid and back intertidal zones (P ¼ 0.04, F ¼ 3.45, df ¼ 35, 106). This did not translate into significantly higher total pneumatophore surface area (P ¼ 0.65, F ¼ 0.43), as pneumatophores tended to become narrower as they grew taller (Table 2). 3.2. Macroalgal presence/absence Six species of macroalgae were found on mangrove pneumatophores in the study sites. Five species of algae belonging to the Division Rhodophyta were identified: Caloglossa leprieurii (Montagne) J. Agardh, Catenella nipae Zanardini, Bostrychia moritziana (Sonder) J. Agardh, Bostrychia tenella (Lamouroux) J. Agardh, and Bostrychia tenuissima R.J. King et Puttock, and only one species from the Division Chlorophyta was present; Ulva australis Linnaeus.
Table 3 Frequency of occurrence (%) of macroalgal species in intertidal zones and along the length of pneumatophores during each survey in the Clyde River. Ulva australis is not included in the table as it was found only in trace amounts. Length along pneumatophores is described in 2 segments, basal (0e5 cm from mudline) and basal (>5 cm). Values are means across sites SE (n ¼ 36) Intertidal zone
Vertical segment
Feb 02
Aug 02
Feb 03
Aug 03
Caloglossa leprieurii Front Basal Apex Centre Basal Apex Back Basal Apex
0 0 0 0 0 0
0 44 0 44 44 0
0 0 0 0 44 0
0 0 77 0 30 24 77
Catenella nipae Front Basal Apex Centre Basal Apex Back Basal Apex
52 18 27 21 82 12 42 20 100 0 50 14
52 12 12 16 96 4 80 12 85 18 45 12
56 34 13 16 85 12 32 15 89 8 45 12
45 16 6 10 89 8 70 24 96 4 35 14
18 12 22 4 11 0 15 4
33 21 27 12 15 4 82 0 0
22 16 58 36 19 16 44 44 0
44 36 54 30 43 20 16 8 0 0
39 7 0 72 17 22 38 18 32
33 33 37 33 18 13 29 9 23 15
55 14 0 67 21 0 37 16 44
0 0 15 12 22 44 9 75
0 0 0 53 11 8 0
0 0 44 53 18 16 44
Bostrychia moritziana Front Basal Apex Centre Basal Apex Back Basal Apex Bostrychia tenella Front Basal Apex Centre Basal Apex Back Basal Apex Bostrychia tenuissima Front Basal Apex Centre Basal Apex Back Basal Apex
0 0 0 33 11 8 18 13 18 12 23 15 0 0 0 22 26 12 0
3.3. Macroalgal frequency and biomass Frequency and biomass of individual species in each intertidal zone and vertical pneumatophore segment are presented in Tables 3 and 4, respectively. Catenella nipae exhibited the highest frequency and abundance of all the species, whereas Caloglossa leprieurii was the least frequent and abundant. Bostrychia moritziana and Bostrychia tenella were found at similar frequencies and abundance, whereas Bostrychia tenuissima was less commonly found. Frequency of each species was significantly correlated with biomass, as expected (Table 5), indicating that the more frequently a species occurred within each zone or site the higher the species’ biomass in that same area. Ordination plots (MDS) of macroalgal frequency and biomass did not exhibit any distinct patterns of community structure in regard to season/sampling period or site (Figs. 3a,b and
4a,b). When individual species were analysed similar results were obtained, with no species exhibiting significantly different frequencies or abundances among the seasons or sites (P > 0.05 for all species, F ¼ 2.34 to 21.5, df ¼ 80, 322 for seasons and 107, 322 for sites). However, patterns were evident in regard to both intertidal zone (Figs. 3c and 4c) and vertical pneumatophore segment (Figs. 3d and 4d). The scatter of data points in the intertidal MDS plot indicated possible tidal gradient effects on the community structure, from the front to the back of the stand, with a separation of the front and back intertidal zones by the mid intertidal zone data points. The analysis of individual species indicated that four species exhibited significant differences in frequency and biomass among the intertidal zones. Both Caloglossa leprieurii and Bostrychia tenuissima were most frequently found in the back intertidal zone (P ¼ 0.001,
F. Melville, A. Pulkownik / Estuarine, Coastal and Shelf Science 71 (2007) 683e690 Table 4 Biomass of macroalgal species (g/m2 of pneumatophore surface area) in intertidal zones and along the length of pneumatophores during each survey in the Clyde River. Ulva australis is not included in the table as it was found only in trace amounts. Length along pneumatophores is described in 2 segments, basal (0e5 cm from mudline) and apex (>5 cm). Values are means across sites SE (n ¼ 108) Intertidal zone
Vertical segment
Feb 02
Aug 02
Feb 03
Aug 03
Caloglossa leprieurii Front Basal Apex Centre Basal Apex Back Basal Apex
0 0 0 0 0 0
0 Trace 0 Trace Trace 0
0 0 0 0 Trace 0
0 0 Trace 0 Trace Trace
Catenella nipae Front Basal Apex Centre Basal Apex Back Basal Apex
19 10 84 24 7 17 5 35 11 19 9
63 22 25 14 27 19 15 2 92
54 22 17 7 11 7 30 3 16 10
11 4 Trace 45 23 31 15 29 2 93
Bostrychia moritziana Front Basal Apex Centre Basal Apex Back Basal Apex
11 3 72 73 32 0 0
11 3 13 4 93 42 0 0
10 10 10 21 Trace 0
74 74 53 31 0 0
Bostrychia tenella Front Basal Apex Centre Basal Apex Back Basal Apex
0 Trace 11 31 21 31
21 0 21 Trace 10 Trace
Trace Trace 32 11 21 10
30 0 40 0 31 Trace
Bostrychia tenuissima Front Basal Apex Centre Basal Apex Back Basal Apex
0 0 0 Trace 20 0
0 0 10 Trace 41 11
0 0 0 Trace Trace 0
0 0 Trace 10 11 11
F ¼ 7.6 and P ¼ 0.001, F ¼ 3.45, respectively, df ¼ 35, 322), with Catenella nipae more abundant in the mid and back zones (P < 0.001, F ¼ 14.5), while Bostrychia moritziana was restricted to the front and mid zones (P < 0.001, F ¼ 12.3). In the ordination plots of algal frequency and biomass on vertical pneumatophore segments (Figs. 3d and 4d), the apex
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Feb-02 Aug-02 Feb-03 Aug-03
a
Stress: 0.12
b
Stress: 0.12
Site1 Site 2 Site 3
c
Stress: 0.12
back mid front
d
Stress: 0.12
basal apex
Table 5 Correlation between frequency and biomass of macroalgal species. All correlation values were significant (n ¼ 108) Species
Correlation value
C. leprieurii C. nipae B. moritziana B. tenella B. tenuissima
0.892 0.658 0.287 0.835 0.847
Fig. 3. Multidimensional scaling of macroalgal frequencies with respect to: (a) sample period; (b) sample sites; (c) intertidal zone; and (d) pneumatophore vertical segment (n ¼ 108). Stress refers to fitness to MDS model (Primer, 2001).
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a
Stress: 0.12
Feb-02 Aug-02 Feb-03 Aug-03
datapoints were slightly separated from the basal datapoints. The GLM of individual species indicated that overall there was higher biomass and frequency of algae on the basal segment in comparison with the apex segments. Biomass of Catenella nipae, Bostrychia tenella and Bostrychia tenuissima were significantly higher on the basal segments (P ¼ 0.03, F ¼ 4.3, P ¼ 0.04, F ¼ 2.1 and P ¼ 0.04, F ¼ 1.9, respectively, df ¼ 22, 322). 4. Discussion
b
Stress: 0.12
Site 1 Site 2 Site 3
c
Stress: 0.12
back mid front
d
Stress: 0.12
basal apex
Fig. 4. Multidimensional scaling of macroalgal biomass with respect to: (a) sample period; (b) sample sites; (c) intertidal zone; and (d) pneumatophore vertical segment (n ¼ 324). Stress refers to fitness to MDS model (Primer, 2001).
The understanding of how seasonal and spatial variability might affect the distribution and abundance of a species is important, both in evaluating its responses to metal contamination, and for the effective experimental design of a monitoring program. Furthermore, such information is of utmost importance in the selection, and potential utilisation of species as bioindicators or biomonitors of estuarine contamination. Only one other study (Melville et al., 2005), which was undertaken concurrently with this study, has simultaneously examined spatial variation in three dimensions and temporal variation of mangrove macroalgae. Only six species of mangrove macroalgae were identified in the Clyde River estuary. This low species richness can be considered typical of the temperate Australian mangrove areas (King, 1990; King and Puttock, 1994), with a similar number of species identified in other mangrove ecosystems in the Sydney region (Laursen and King, 2000; Melville et al., 2005). The species identified in this study have been reported to be present in many other temperate estuaries of the southern hemisphere, both in Australia and overseas in Africa and South America (King, 1990; Phillips et al., 1994; Pena et al., 1999; Melville et al., 2005; Melville and Pulkownik, 2006). No seasonal variation in macroalgal diversity and abundance was detected over the two annual cycles of monitoring, which has also been observed in other mangrove macroalgal communities in the Sydney region (Laursen and King, 2000; Melville et al., 2005). However, other studies have reported distinct peaks of macroalgal biomass in South African mangroves over the different seasons (Steinke and Naidoo, 1990). Such changes can be influenced by nutrient availability, which can increase during summer, stimulating algal growth, along with increased light and temperatures (Valiela et al., 1997). In this study, nutrient concentrations did not vary significantly over the different seasons, and this may have contributed to stable presence of macroalgae. No variation in algal distribution and abundance was found amongst the three study sites, indicating that the change in water and sediment salinity along the length of the estuary examined did not appear to have an impact on the algae. Estuarine organisms would be expected to be tolerant to salinity changes and this has been demonstrated for several Bostrychia species, and Caloglossa leprieurii, all of which displayed broad salinity tolerances (Yarish and Edwards, 1982; Karsten et al., 1994). Macroalgal frequency and biomass varied among intertidal zones, with each species exhibiting a preference for a particular
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intertidal zone, similar to the pattern found in the Parramatta River macroalgae (Melville et al., 2005). Most previous studies have suggested that the distribution of algae within intertidal zones is related to their tolerance to desiccation (Phillips et al., 1994; Zuccarello et al., 2001). Algae in the back intertidal zones will be emersed, as opposed to submersed, for longer periods than those at the stand front, and thus must be able to tolerate desiccation. Therefore, it appears that Bostrychia moritziana, found only in the front intertidal zone, was the least tolerant of desiccation, with Caloglossa leprieurii and Bostrychia tenuissima, which were found primarily in the back intertidal stand, the most tolerant of desiccation. However, competition for available pneumatophore attachment points, in addition to desiccation tolerance, may also influence macroalgal distribution. In some mangrove areas, macroalgal competition for pneumatophore attachment points is considered to be more important than competition for nutrients (Nedwell et al., 2002). It can be postulated that most algae would preferentially inhabit the front intertidal zone in order to avoid longer periods of desiccation. However, it is the ability to compete successfully that will determine the actual distribution of these macroalgal species. Bostrychia moritizana dominated the front intertidal zone and was rarely found in the back intertidal zones. This suggests a low desiccation tolerance and perhaps a superior competitive ability. The other macroalgal species found predominantly in the mid and back intertidal areas may prefer to inhabit the front zone but are unable to compete successfully with B. moritziana. On the other hand, longer periods of emersion, and therefore the higher light levels that accompany the mid and back intertidal zones, may be preferential to certain macroalgal species. Overall, it is possible that intertidal zonation of the macroalgal species in these estuaries is due to a combination of both competition and desiccation tolerance/intolerance. It is unlikely that the variation in pneumatophore heights amongst the intertidal zones was responsible for the intertidal algal variation, as total surface area did not vary significantly among the zones. The estimates of macroalgal abundance were obtained by expressing it in terms of biomass per unit of pneumatophore surface area and thus, were independent of the total number, or total surface area, of pneumatophores present at any site. It should also be noted that this study only examined macroalgae epiphytic on pneumatophores of Avicennia marina. It is well documented that these algae used a wide range of substrates for attachment, including tree trunks, fallen branches, rocks and mud surfaces (Beanland and Woelkerling, 1982; King and Puttock, 1994). Macroalgal frequency and biomass varied among vertical pneumatophore segments, as it did in the Parramatta River (Melville et al., 2005). Vertical zonation of macroalgae along the length of the pneumatophores is considered to be related to the light requirements of particular species, with higher pneumatophore segments receiving higher light levels (Phillips et al., 1996). Light levels as a function of canopy cover, did not vary significantly between seasons, sites or intertidal
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zones, with canopy cover over 75% in each site, although higher pneumatophore segments generally receive higher light levels than basal segments (Phillips et al., 1996). As Catenella nipae was always found on the basal pneumatophore segment, both in this study and others (Davey and Woelkerling, 1985; Phillips et al., 1996; Melville et al., 2005), it seems probable that this species requires lower light levels than other macroalgal species. In many field studies, Bostrychia species have been found towards the apex on pneumatophores, with laboratory studies indicating they require higher light levels than most other algal species (Mann and Steinke, 1988). In this study, however, both Bostrychia tenella and Bostrychia tenuissima were found in higher abundances in the basal pneumatophore segment, suggesting that light levels may vary among the mangrove stands examined, and perhaps these species have adapted to lower or higher light levels as necessary.
5. Conclusion In conclusion, the examination of the frequency and abundance of mangrove macroalgae in the Clyde estuary has exhibited significant intertidal and vertical zonation of several algal species. The spatial variation demonstrated by the algal community as a whole, and individual algal species, was similar to that exhibited in the Parramatta River (Melville et al., 2005), suggesting that the intertidal and vertical patterns may be common across many estuaries. This study has also elucidated environmental factors which may influence these macroalgal species, which may potentially be used as bioindicators and biomonitors of metal contamination. Criteria have been established by several studies (Rainbow, 1995; Conti and Cecchetti, 2003) that are considered essential for any indicator species. These include: no seasonal variation, to allow monitoring over the whole annual cycle; a widespread distribution, ensuring wide geographic relevance; knowledge of the ecology of the organism; and sufficient tissue for analysis, if required. Although none of the species examined exhibited seasonal variation, and all have been found in other temperate mangrove ecosystems throughout the world, only Catenella nipae, Bostrychia moritziana and Bostrychia tenella consistently provided sufficient tissue for laboratory analysis, and as such, could potentially become suitable indicator species, dependent on their sensitivity to contaminants.
Acknowledgements This project was supported by funding from the Sydney Olympic Park Authority. The authors thank Ralph Alquezar for his assistance with the field sampling, Narelle Richardson and Gemma Armstrong for their advice on laboratory methodology, and Professor Margaret Burchett, Associate Professor Richard Lim, Edwina Laginestra and Dr Jenny Stauber for guidance on the experimental design of this study.
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References Allen, S., 1989. Chemical Analysis of Ecological Materials. Blackwell Scientific Publications, Melbourne. Beanland, W.R., Woelkerling, W.J., 1982. Studies on Australian mangrove algae II: Composition and geographic distribution of communities in Spencer Gulf, South Australia. Proceedings of the Royal Society of Victoria 94, 309e313. Broderick, M.E., Dawes, C.J., 1998. Seasonal photosynthetic and respiratory responses of the red alga Bostrychia tenella (Ceramiales, Rhodophyta) from a salt marsh and mangal. Phycologia 37, 92e99. Brown, M.T., 1987. Effects of desiccation on photosynthesis of intertidal algae from a southern New Zealand shore. Botanica Marina 30, 121e127. Conti, M.E., Cecchetti, G., 2003. A biomonitoring study: trace metals in algae and molluscs from Tyrrhenian coastal areas. Environmental Research 93, 99e112. Davey, A., Woelkerling, W.J., 1985. Studies on Australian mangrove algae: I. Victorian communities: composition and geographic distribution. Proceedings of the Royal Society of Victoria 91, 53e66. Druehl, L.D., Green, J.M., 1982. Vertical distribution of intertidal seaweeds as related to patterns of submersion and emersion. Marine Ecology Progress Series 9, 163e170. Karsten, U., West, J.A., Zuccarello, G.C., Kirst, G.O., 1994. Physiological ecotypes in the marine alga Bostrychia radicans (Ceramiales, Rhodophyta) from the east coast of the USA. Journal of Phycology 30, 174e182. King, R.J., 1990. Macroalgae associated with the mangrove vegetation of Papua New Guinea. Botanica Marina 33, 55e62. King, R.J., 1995. Mangrove macroalgae: a review of Australian studies. Proceedings of the Linnean Society of New South Wales 115, 151e161. King, R.J., Puttock, C.F., 1994. Macroalgae associated with mangroves in Australia: Rhodophyta. Botanica Marina 37, 181e191. King, R.J., Wheeler, M.D., 1985. Composition and geographic distribution of mangrove macroalgal communities in New South Wales. Proceedings of the Linnean Society of New South Wales 108, 97e117. Kirby, J., Maher, W., Krikowa, F., 2001. Selenium, cadmium, copper and zinc concentrations in sediments and mullet (Mugil cephalus) from the southern basin of Lake Macquarie, NSW, Australia. Archives of Environmental Contamination and Toxicology 40, 246e256. Laursen, W.J., King, R.J., 2000. The distribution and abundance of mangrove macroalgae in Wooloware Bay, New South Wales, Australia. Botanica Marina 43, 377e384. Mann, F.D., Steinke, T.D., 1988. Photosynthetic and respiratory responses of the mangrove associated red algae Bostrychia radicans and Caloglossa leprieurii. South African Journal of Botany 54, 203e207. McClusky, D.S., Elliot, M., 2004. The Estuarine Ecosystem: Ecology, Threats and Management. Oxford University Press Inc., New York.
Melville F., 2005. Mangrove Algae in the Assessment of Estuarine Pollution [Ph.D.]. Sydney: University of Technology, Sydney, 289 p. Melville, F., Pulkownik, A., 2006. Investigation of mangrove macroalgae as bioindicators of estuarine contamination. Marine Pollution Bulletin 52, 1260e1269. Melville, F., Burchett, M., Pulkownik, A., 2004. Genetic variation among ageclasses of the mangrove Avicennia marina in clean and contaminated sediments. Marine Pollution Bulletin 49, 695e703. Melville, F., Pulkownik, A., Burchett, M., 2005. Zonal and seasonal variation in the distribution and abundance of mangrove macroalgae in the Parramatta River, Australia. Estuarine, Coastal and Shelf Science 64, 267e276. Nedwell, D.B., Sage, A.S., Underwood, G.J.C., 2002. Rapid assessment of macroalgal cover on intertidal sediments in a nutrient-enriched estuary. The Science of the Total Environment 285, 97e105. Pena, E.J., Zingmark, R., Nietch, C., 1999. Comparative photosynthesis of two species of intertidal epiphytic macroalgae on mangrove roots during submersion and emersion. Journal of Phycology 35, 1206e1214. Phillips, A., Lambert, G., Granger, J.E., Steinke, T.D., 1994. Horizontal zonation of epiphytic algae associated with Avicennia marina (Forsk.) Vierh. pneumatophores at Beachwoods Mangroves Nature Reserve, Durban, South Africa. Botanica Marina 39, 167e175. Phillips, A., Lambert, G., Granger, J.E., Steinke, T.D., 1996. Vertical zonation of epiphytic algae associated with Avicennia marina (Forsk.) Vierh. pneumatophores at Beachwood Mangroves Nature Reserve, Durban, South Africa. Botanica Marina 39, 167e175. Pregnall, A.M., Rudy, P.P., 1985. Contribution of green algal mats (Enteromorpha sp.) to seasonal production in an estuary. Marine Ecology Progress Series 24, 167e176. Rainbow, P.S., 1995. Biomonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin 31, 183e192. Rayment, G., Higginson, F., 1992. Australian Laboratory Handbook of Soil and Water Chemical Methods. Inkata Press, Melbourne. Steinke, T.D., Naidoo, Y., 1990. Biomass of algae epiphytic on pneumatophores of the mangrove Avicennia marina, in the St Lucia estuary. South African Journal of Botany 56, 226e232. Valiela, I., McClelland, J., Hauxwell, J., Behr, P.J., Hersh, D., Foreman, K., 1997. Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnology and Oceanography 42, 1105e1118. Yarish, C., Edwards, P., 1982. A field and cultural investigation of the horizontal and seasonal distribution of estuarine red algae of New Jersey. Phycologia 21, 112e124. Zuccarello, G.C., Yeates, P.H., Wright, J.T., Bartlett, J., 2001. Population structure and physiological differentiation of haplotypes of Caloglossa leprieurii (Rhodophyta) in a mangrove intertidal zone. Journal of Phycology 37, 235e244.
Seasonal and spatial variation in the distribution of mangrove macroalgae in the Clyde River, Australia Felicity Melville*, Alex Pulkownik Department of Environmental Sciences, University of Technology, PO Box 123, Broadway, Sydney, NSW 2007, Australia Received 9 June 2006; accepted 21 September 2006 Available online 14 November 2006
Abstract The objective of this study was to determine whether there was significant spatial and temporal variation in macroalgae epiphytic on pneumatophores of the Grey Mangrove, Avicennia marina (Forsk.) Vierh., in the Clyde River, located 280 km south of Sydney, Australia. Three estuarine sites in the Clyde River were surveyed seasonally on four occasions over a two-year period, and algal distribution and abundance assessed in respect to temporal, inter-site, intertidal (from front to back of mangrove stand) and vertical (from bottom to top of pneumatophores) variation. Sediment and water characteristics, including nutrient levels, were also assessed in order to examine all variables of potential influence on algal distribution and abundance. The results indicated that intertidal position within sites, and vertical height along the length of the pneumatophore, were the greatest influence on algal frequency and biomass. Individual species dominated in different intertidal and vertical zones. These observations, together with the identification of three species of macroalgae that fulfil the criteria for bioindicators/biomonitors of environmental impacts are discussed. Ó 2006 Published by Elsevier Ltd. Keywords: mangrove; macroalgae; intertidal; pneumatophores; Clyde River; Australia
1. Introduction Mangroves can host diverse macroalgal assemblages that grow epiphytically on pneumatophores, prop roots, stems and other hard substrates (Zuccarello et al., 2001). The algae are exposed to the steep environmental gradients associated with the estuarine environment, including emersion and submersion during tidal cycles, and fluctuating temperature, salinity, light and nutrient conditions (Pregnall and Rudy, 1985). Such circumstances are unfavourable for most marine and freshwater algae, but mangrove-associated algae have adapted to this environment and flourished (Phillips et al., 1994). Like mangroves, mangrove macroalgae have an important role as primary producers in the estuarine ecosystem, through the production of organic material and contribution to nutrient * Corresponding author. Present address: Centre for Environmental Management, Central Queensland University, PO Box 1319, Gladstone, Qld 4680, Australia. E-mail address: [email protected] (F. Melville). 0272-7714/$ - see front matter Ó 2006 Published by Elsevier Ltd. doi:10.1016/j.ecss.2006.09.023
cycling, (Davey and Woelkerling, 1985; McClusky and Elliot, 2004). Macroalgae also function as food sources for grazing marine animals, and as a habitat for small estuarine invertebrates (Melville, 2005). Distinct patterns of macroalgal biogeography, and distribution and abundance of mangrove macroalgae in the intertidal zone, have emerged from the extensive studies carried out both in Australia (Davey and Woelkerling, 1985; King and Wheeler, 1985; King, 1990; King and Puttock, 1994; King, 1995), and overseas in other temperate mangrove ecosystems (Mann and Steinke, 1988; Phillips et al., 1994; Phillips et al., 1996; Broderick and Dawes, 1998). Although a number of factors have been shown to affect growth patterns, emersion frequency of the algae and species desiccation tolerance appear to be the most significant parameters (Druehl and Green, 1982; Zuccarello et al., 2001). Studies have found algal biomass to decline landwards from the water body, coinciding with the pneumatophores being emergent for successively longer periods during the tidal cycle (Davey and Woelkerling, 1985; Phillips et al., 1994). It has been suggested that the
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desiccation tolerance of algal species is the major determinant for their intertidal limit (Brown, 1987). Previous studies have found distributional differences among estuaries with differing pollution loads, in addition to correlations between sediment and algal metal concentrations (Melville, 2005; Melville and Pulkownik, 2006). However, inter-site and intra-site differences in distribution and biomass within the estuaries has not been addressed; nor was has temporal variability. This study examined the spatial and temporal variation of macroalgae epiphytic on pneumatophores (aerial roots) of the Grey mangrove, Avicennia marina (Forsk.) Vierh., in the Clyde River, located approximately 280 km south of Sydney, Australia. This study was part of a large-scale project assessing the potential of mangrove macroalgae as indicators of metal contamination in temperate estuaries (Melville, 2005; Melville and Pulkownik, 2006). The examination of the temporal and spatial variation exhibited by the macroalgae was an important component of the overall study. An understanding of the natural variation in species abundance and distribution (autoecology) is essential knowledge for any indicator species (Rainbow, 1995). The aim of this study was, therefore, to determine the extent of seasonal variation, and inter-site, intertidal and vertical zonation of mangrove macroalgae on pneumatophores of Avicennia marina (Forsk) Vierh. in the Clyde River estuary. A simultaneous study carried out in the Parramatta River in Sydney, Australia, indicated clear intertidal differences in algal distribution and abundance, but no spatial or temporal variation (Melville et al., 2005). The Clyde River estuary is a relatively pristine estuary located about 200 km from any major metropolitan area (Kirby
et al., 2001; Melville et al., 2004), whereas the Parramatta River estuary is located in the centre of Sydney, and has been shown to contain significantly higher pollutant concentrations (Melville et al., 2004; Melville, 2005; Melville and Pulkownik, 2006). Therefore, it is possible that the macroalgal zonation exhibited in the Parramatta River, may differ from those in the Clyde River. 2. Materials and methods 2.1. Site selection and study design Three study sites in the Clyde River (Fig. 1) were selected to give a range of estuarine water salinities. Mean salinities at Sites 1, 2 and 3 were approximately 20, 15 and 10 psu at low tide, respectively. However, these sites can experience wide fluctuations in salinity during king tides and rain events. At each site, three transects, 10 m apart, were set up along the tidal gradient, with three stations, each of approximately 4 m2, in different intertidal zones (front, mid and back) marked in each transect (Fig. 2). The stations at the front of the mangrove stand were situated approximately 1e2 m from the margin of the mangrove canopy at the waterline; stations in the back intertidal zone at 1e2 m from the stand transition into the terrestrial ecosystem; and in the mid-zone, halfway between the front and back zones (between 15 and 24 m in each site). 2.2. Site characteristics Vegetative characteristics of each site and zone were evaluated by estimating the average mangrove tree height and
N
Site 3
Site 2 Site 1
Fig. 1. Study sites in the Clyde River estuary, Australia.
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Transect B
Transect A
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2.5. Statistical analyses
Transect C
2m
Back zone (3)
Station A3
Mid zone (2)
Station A2
Front zone (1)
Station A1
Station B3 10m
Station B2 Station B1
Station C3 10m
Station C2
Edge of tree canopy
Station C1
2m
WATER Fig. 2. Experimental design for sampling in the Clyde River.
projective foliage cover (% PFC) at each station, as a measure of light availability to the pneumatophores, and, therefore, to the algae growing upon them. At each station, pneumatophore characteristics were also examined using 0.125 m2 quadrats. The number of pneumatophores in each quadrat, and their heights, were recorded, and pneumatophore density calculated as the number of pneumatophores per m2. The apex and basal width of pneumatophores were also measured, and used to calculate total pneumatophore surface area per m2. 2.3. Sample collection Summer and winter sampling was conducted over an 18 month period, during February and August 2002, and February and August 2003. Sediment samples were collected from each station within each intertidal zone; with 108 samples collected over the whole study. At each station, three pneumatophores were collected; with 324 collected over the whole study. Pneumatophores were cut at the mudline with clippers, sealed in plastic bags, and transported back to the laboratory on ice, for measurement and algal analyses. 2.4. Laboratory analyses Sediment samples were air-dried and sieved through a 2 mm mesh sieve (Allen, 1989). The <2 mm sediment fraction was then used to determine pH and salinity (as electrical conductivity in mS/cm) in 1:5 aqueous extracts, organic matter content (as % LOI, loss on ignition at 550 C), and total nitrogen and total phosphorus levels (mg kg1) (Allen, 1989; Rayment and Higginson, 1992). Pneumatophore height, and width at apex and base were recorded with callipers and pneumatophores cut into 5 cm vertical segments. Algae were scraped from each segment, taking care not to remove pneumatophore tissue, and stored separately in 4% formalin solution. The algal species were identified in each sample under a magnifying lamp using taxonomic literature (King and Wheeler, 1985; King and Puttock, 1994), separated and dried overnight at 45 C to determine biomass. Algal biomass was expressed on the basis of the surface area of each pneumatophore segment (g/m2), using previously determined dimensions of the pneumatophore. Frequencies for each algal species were calculated as the percentage of pneumatophores examined on which that species was detected.
To determine whether there were any significant spatial differences in site characteristics, pneumatophore heights or densities, Analyses of Variance were undertaken using General Linear Models (GLM, Minitab, Version 13.1, 2000). In all analyses, a ¼ 0.05. In order to examine the macroalgal community dynamics, non-metric Multidimensional Scaling, (MDS, Primer, Version 5.2.7, 2001) was used to provide a graphical depiction the influence of seasonal, site, intertidal and vertical segment variation on the algal community frequency and biomass. The raw algal data sets were square root transformed to achieve more equal weighting of the common and less common species, and using a Bray-Curtis distance measure, compiled into a similarity matrix, which was then used to calculate the MDS plot, using a variety of fixed factors. In these analyses, the MDS model offers a value, ‘stress’, to describe how well the ranked distance metrics between the samples are preserved, with low values indicating good preservation. In order to examine species-specific responses, GLM were then used to determine whether there were any significant differences, or interactions, among individual algal frequencies or biomass in regard to the factors examined in the MDS above (seasons, sites, intertidal zones and pneumatophore segments). 3. Results 3.1. Site characteristics Both water and sediment salinity were highest at Site 1 (Table 1), the most downstream site, and lowest at Site 3 (P < 0.001, F ¼ 5.26 and P ¼ 0.03, F ¼ 7.23 respectively, df ¼ 8, 25 for water and 35, 106 for sediment). Water salinities did not vary significantly over the four sampling periods (P ¼ 0.67, F ¼ 0.09). No significant differences in sediment pH, nitrogen and phosphorus levels, or sediment organic content were found among or within the study sites (Table 1). All sites consisted of trees of up to 10 m in height. Projective foliage cover was similar across all sites and intertidal zones (mean value 79 11%). Pneumatophore heights ranged from 6 to 13 cm, with a mean height of 9 cm (Table 2). Thus, two vertical pneumatophore segments were used to record Table 1 Water and sediment characteristics at study sites in the Clyde River estuary. Values are means SE, taken over four sampling surveys (n ¼ 27 and 108 for water and sediment, respectively) Characteristics
Site 1
Site 2
Site 3
Estuarine mean
Water salinity (psu) 20.4 0.5 15.7 0.5 10.5 0.3 15.5 3.5 Sediment salinity (mS/cm) 7.0 1.3 6.8 1.2 5.5 1.4 6.4 0.6 pH 6.3 0.1 6.3 0.1 6.5 0.1 6.4 0.1 Organic content (% LOI) 71 71 51 61 Nitrogen (mg/kg) 1.8 0.4 1.4 0.2 1.2 0.3 1.4 0.2 Phosphorus (mg/kg) 0.3 0.1 0.2 0.1 0.1 0.1 0.2 0.1
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Table 2 Pneumatophore characteristics at study sites in the Clyde River. Values are means SE (n ¼ 36). Density refers to the number of pneumatophores per m2. Surface area refers to the total surface area of pneumatophores (m2) per stand area (m2) Site
Intertidal zone
Mean Height (cm)
Density (no/m)
Surface area (m2/m2)
1
Front Mid Back
82 12 1 12 2
544 71 779 137 517 141
1.9 0.6 2.1 0.7 1.2 0.5
2
Front Mid Back
62 93 13 3
699 164 512 227 389 69
1.7 0.7 1.3 0.5 1.3 0.5
3
Front Mid Back Mean
61 72 91 91
1040 115 731 227 576 52 643 50
1.6 0.3 1.8 0.8 2.1 0.7 1.4 0.6
algal distribution: basal (0 to 5 cm from the mudline) and apex (>5 cm). Although pneumatophore heights, densities and total surface area did not vary significantly among the sites (P ¼ 0.24, F ¼ 0.27, df ¼ 107, 322), within each site pneumatophores were taller in the mid and back intertidal zones (P ¼ 0.04, F ¼ 3.45, df ¼ 35, 106). This did not translate into significantly higher total pneumatophore surface area (P ¼ 0.65, F ¼ 0.43), as pneumatophores tended to become narrower as they grew taller (Table 2). 3.2. Macroalgal presence/absence Six species of macroalgae were found on mangrove pneumatophores in the study sites. Five species of algae belonging to the Division Rhodophyta were identified: Caloglossa leprieurii (Montagne) J. Agardh, Catenella nipae Zanardini, Bostrychia moritziana (Sonder) J. Agardh, Bostrychia tenella (Lamouroux) J. Agardh, and Bostrychia tenuissima R.J. King et Puttock, and only one species from the Division Chlorophyta was present; Ulva australis Linnaeus.
Table 3 Frequency of occurrence (%) of macroalgal species in intertidal zones and along the length of pneumatophores during each survey in the Clyde River. Ulva australis is not included in the table as it was found only in trace amounts. Length along pneumatophores is described in 2 segments, basal (0e5 cm from mudline) and basal (>5 cm). Values are means across sites SE (n ¼ 36) Intertidal zone
Vertical segment
Feb 02
Aug 02
Feb 03
Aug 03
Caloglossa leprieurii Front Basal Apex Centre Basal Apex Back Basal Apex
0 0 0 0 0 0
0 44 0 44 44 0
0 0 0 0 44 0
0 0 77 0 30 24 77
Catenella nipae Front Basal Apex Centre Basal Apex Back Basal Apex
52 18 27 21 82 12 42 20 100 0 50 14
52 12 12 16 96 4 80 12 85 18 45 12
56 34 13 16 85 12 32 15 89 8 45 12
45 16 6 10 89 8 70 24 96 4 35 14
18 12 22 4 11 0 15 4
33 21 27 12 15 4 82 0 0
22 16 58 36 19 16 44 44 0
44 36 54 30 43 20 16 8 0 0
39 7 0 72 17 22 38 18 32
33 33 37 33 18 13 29 9 23 15
55 14 0 67 21 0 37 16 44
0 0 15 12 22 44 9 75
0 0 0 53 11 8 0
0 0 44 53 18 16 44
Bostrychia moritziana Front Basal Apex Centre Basal Apex Back Basal Apex Bostrychia tenella Front Basal Apex Centre Basal Apex Back Basal Apex Bostrychia tenuissima Front Basal Apex Centre Basal Apex Back Basal Apex
0 0 0 33 11 8 18 13 18 12 23 15 0 0 0 22 26 12 0
3.3. Macroalgal frequency and biomass Frequency and biomass of individual species in each intertidal zone and vertical pneumatophore segment are presented in Tables 3 and 4, respectively. Catenella nipae exhibited the highest frequency and abundance of all the species, whereas Caloglossa leprieurii was the least frequent and abundant. Bostrychia moritziana and Bostrychia tenella were found at similar frequencies and abundance, whereas Bostrychia tenuissima was less commonly found. Frequency of each species was significantly correlated with biomass, as expected (Table 5), indicating that the more frequently a species occurred within each zone or site the higher the species’ biomass in that same area. Ordination plots (MDS) of macroalgal frequency and biomass did not exhibit any distinct patterns of community structure in regard to season/sampling period or site (Figs. 3a,b and
4a,b). When individual species were analysed similar results were obtained, with no species exhibiting significantly different frequencies or abundances among the seasons or sites (P > 0.05 for all species, F ¼ 2.34 to 21.5, df ¼ 80, 322 for seasons and 107, 322 for sites). However, patterns were evident in regard to both intertidal zone (Figs. 3c and 4c) and vertical pneumatophore segment (Figs. 3d and 4d). The scatter of data points in the intertidal MDS plot indicated possible tidal gradient effects on the community structure, from the front to the back of the stand, with a separation of the front and back intertidal zones by the mid intertidal zone data points. The analysis of individual species indicated that four species exhibited significant differences in frequency and biomass among the intertidal zones. Both Caloglossa leprieurii and Bostrychia tenuissima were most frequently found in the back intertidal zone (P ¼ 0.001,
F. Melville, A. Pulkownik / Estuarine, Coastal and Shelf Science 71 (2007) 683e690 Table 4 Biomass of macroalgal species (g/m2 of pneumatophore surface area) in intertidal zones and along the length of pneumatophores during each survey in the Clyde River. Ulva australis is not included in the table as it was found only in trace amounts. Length along pneumatophores is described in 2 segments, basal (0e5 cm from mudline) and apex (>5 cm). Values are means across sites SE (n ¼ 108) Intertidal zone
Vertical segment
Feb 02
Aug 02
Feb 03
Aug 03
Caloglossa leprieurii Front Basal Apex Centre Basal Apex Back Basal Apex
0 0 0 0 0 0
0 Trace 0 Trace Trace 0
0 0 0 0 Trace 0
0 0 Trace 0 Trace Trace
Catenella nipae Front Basal Apex Centre Basal Apex Back Basal Apex
19 10 84 24 7 17 5 35 11 19 9
63 22 25 14 27 19 15 2 92
54 22 17 7 11 7 30 3 16 10
11 4 Trace 45 23 31 15 29 2 93
Bostrychia moritziana Front Basal Apex Centre Basal Apex Back Basal Apex
11 3 72 73 32 0 0
11 3 13 4 93 42 0 0
10 10 10 21 Trace 0
74 74 53 31 0 0
Bostrychia tenella Front Basal Apex Centre Basal Apex Back Basal Apex
0 Trace 11 31 21 31
21 0 21 Trace 10 Trace
Trace Trace 32 11 21 10
30 0 40 0 31 Trace
Bostrychia tenuissima Front Basal Apex Centre Basal Apex Back Basal Apex
0 0 0 Trace 20 0
0 0 10 Trace 41 11
0 0 0 Trace Trace 0
0 0 Trace 10 11 11
F ¼ 7.6 and P ¼ 0.001, F ¼ 3.45, respectively, df ¼ 35, 322), with Catenella nipae more abundant in the mid and back zones (P < 0.001, F ¼ 14.5), while Bostrychia moritziana was restricted to the front and mid zones (P < 0.001, F ¼ 12.3). In the ordination plots of algal frequency and biomass on vertical pneumatophore segments (Figs. 3d and 4d), the apex
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Feb-02 Aug-02 Feb-03 Aug-03
a
Stress: 0.12
b
Stress: 0.12
Site1 Site 2 Site 3
c
Stress: 0.12
back mid front
d
Stress: 0.12
basal apex
Table 5 Correlation between frequency and biomass of macroalgal species. All correlation values were significant (n ¼ 108) Species
Correlation value
C. leprieurii C. nipae B. moritziana B. tenella B. tenuissima
0.892 0.658 0.287 0.835 0.847
Fig. 3. Multidimensional scaling of macroalgal frequencies with respect to: (a) sample period; (b) sample sites; (c) intertidal zone; and (d) pneumatophore vertical segment (n ¼ 108). Stress refers to fitness to MDS model (Primer, 2001).
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a
Stress: 0.12
Feb-02 Aug-02 Feb-03 Aug-03
datapoints were slightly separated from the basal datapoints. The GLM of individual species indicated that overall there was higher biomass and frequency of algae on the basal segment in comparison with the apex segments. Biomass of Catenella nipae, Bostrychia tenella and Bostrychia tenuissima were significantly higher on the basal segments (P ¼ 0.03, F ¼ 4.3, P ¼ 0.04, F ¼ 2.1 and P ¼ 0.04, F ¼ 1.9, respectively, df ¼ 22, 322). 4. Discussion
b
Stress: 0.12
Site 1 Site 2 Site 3
c
Stress: 0.12
back mid front
d
Stress: 0.12
basal apex
Fig. 4. Multidimensional scaling of macroalgal biomass with respect to: (a) sample period; (b) sample sites; (c) intertidal zone; and (d) pneumatophore vertical segment (n ¼ 324). Stress refers to fitness to MDS model (Primer, 2001).
The understanding of how seasonal and spatial variability might affect the distribution and abundance of a species is important, both in evaluating its responses to metal contamination, and for the effective experimental design of a monitoring program. Furthermore, such information is of utmost importance in the selection, and potential utilisation of species as bioindicators or biomonitors of estuarine contamination. Only one other study (Melville et al., 2005), which was undertaken concurrently with this study, has simultaneously examined spatial variation in three dimensions and temporal variation of mangrove macroalgae. Only six species of mangrove macroalgae were identified in the Clyde River estuary. This low species richness can be considered typical of the temperate Australian mangrove areas (King, 1990; King and Puttock, 1994), with a similar number of species identified in other mangrove ecosystems in the Sydney region (Laursen and King, 2000; Melville et al., 2005). The species identified in this study have been reported to be present in many other temperate estuaries of the southern hemisphere, both in Australia and overseas in Africa and South America (King, 1990; Phillips et al., 1994; Pena et al., 1999; Melville et al., 2005; Melville and Pulkownik, 2006). No seasonal variation in macroalgal diversity and abundance was detected over the two annual cycles of monitoring, which has also been observed in other mangrove macroalgal communities in the Sydney region (Laursen and King, 2000; Melville et al., 2005). However, other studies have reported distinct peaks of macroalgal biomass in South African mangroves over the different seasons (Steinke and Naidoo, 1990). Such changes can be influenced by nutrient availability, which can increase during summer, stimulating algal growth, along with increased light and temperatures (Valiela et al., 1997). In this study, nutrient concentrations did not vary significantly over the different seasons, and this may have contributed to stable presence of macroalgae. No variation in algal distribution and abundance was found amongst the three study sites, indicating that the change in water and sediment salinity along the length of the estuary examined did not appear to have an impact on the algae. Estuarine organisms would be expected to be tolerant to salinity changes and this has been demonstrated for several Bostrychia species, and Caloglossa leprieurii, all of which displayed broad salinity tolerances (Yarish and Edwards, 1982; Karsten et al., 1994). Macroalgal frequency and biomass varied among intertidal zones, with each species exhibiting a preference for a particular
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intertidal zone, similar to the pattern found in the Parramatta River macroalgae (Melville et al., 2005). Most previous studies have suggested that the distribution of algae within intertidal zones is related to their tolerance to desiccation (Phillips et al., 1994; Zuccarello et al., 2001). Algae in the back intertidal zones will be emersed, as opposed to submersed, for longer periods than those at the stand front, and thus must be able to tolerate desiccation. Therefore, it appears that Bostrychia moritziana, found only in the front intertidal zone, was the least tolerant of desiccation, with Caloglossa leprieurii and Bostrychia tenuissima, which were found primarily in the back intertidal stand, the most tolerant of desiccation. However, competition for available pneumatophore attachment points, in addition to desiccation tolerance, may also influence macroalgal distribution. In some mangrove areas, macroalgal competition for pneumatophore attachment points is considered to be more important than competition for nutrients (Nedwell et al., 2002). It can be postulated that most algae would preferentially inhabit the front intertidal zone in order to avoid longer periods of desiccation. However, it is the ability to compete successfully that will determine the actual distribution of these macroalgal species. Bostrychia moritizana dominated the front intertidal zone and was rarely found in the back intertidal zones. This suggests a low desiccation tolerance and perhaps a superior competitive ability. The other macroalgal species found predominantly in the mid and back intertidal areas may prefer to inhabit the front zone but are unable to compete successfully with B. moritziana. On the other hand, longer periods of emersion, and therefore the higher light levels that accompany the mid and back intertidal zones, may be preferential to certain macroalgal species. Overall, it is possible that intertidal zonation of the macroalgal species in these estuaries is due to a combination of both competition and desiccation tolerance/intolerance. It is unlikely that the variation in pneumatophore heights amongst the intertidal zones was responsible for the intertidal algal variation, as total surface area did not vary significantly among the zones. The estimates of macroalgal abundance were obtained by expressing it in terms of biomass per unit of pneumatophore surface area and thus, were independent of the total number, or total surface area, of pneumatophores present at any site. It should also be noted that this study only examined macroalgae epiphytic on pneumatophores of Avicennia marina. It is well documented that these algae used a wide range of substrates for attachment, including tree trunks, fallen branches, rocks and mud surfaces (Beanland and Woelkerling, 1982; King and Puttock, 1994). Macroalgal frequency and biomass varied among vertical pneumatophore segments, as it did in the Parramatta River (Melville et al., 2005). Vertical zonation of macroalgae along the length of the pneumatophores is considered to be related to the light requirements of particular species, with higher pneumatophore segments receiving higher light levels (Phillips et al., 1996). Light levels as a function of canopy cover, did not vary significantly between seasons, sites or intertidal
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zones, with canopy cover over 75% in each site, although higher pneumatophore segments generally receive higher light levels than basal segments (Phillips et al., 1996). As Catenella nipae was always found on the basal pneumatophore segment, both in this study and others (Davey and Woelkerling, 1985; Phillips et al., 1996; Melville et al., 2005), it seems probable that this species requires lower light levels than other macroalgal species. In many field studies, Bostrychia species have been found towards the apex on pneumatophores, with laboratory studies indicating they require higher light levels than most other algal species (Mann and Steinke, 1988). In this study, however, both Bostrychia tenella and Bostrychia tenuissima were found in higher abundances in the basal pneumatophore segment, suggesting that light levels may vary among the mangrove stands examined, and perhaps these species have adapted to lower or higher light levels as necessary.
5. Conclusion In conclusion, the examination of the frequency and abundance of mangrove macroalgae in the Clyde estuary has exhibited significant intertidal and vertical zonation of several algal species. The spatial variation demonstrated by the algal community as a whole, and individual algal species, was similar to that exhibited in the Parramatta River (Melville et al., 2005), suggesting that the intertidal and vertical patterns may be common across many estuaries. This study has also elucidated environmental factors which may influence these macroalgal species, which may potentially be used as bioindicators and biomonitors of metal contamination. Criteria have been established by several studies (Rainbow, 1995; Conti and Cecchetti, 2003) that are considered essential for any indicator species. These include: no seasonal variation, to allow monitoring over the whole annual cycle; a widespread distribution, ensuring wide geographic relevance; knowledge of the ecology of the organism; and sufficient tissue for analysis, if required. Although none of the species examined exhibited seasonal variation, and all have been found in other temperate mangrove ecosystems throughout the world, only Catenella nipae, Bostrychia moritziana and Bostrychia tenella consistently provided sufficient tissue for laboratory analysis, and as such, could potentially become suitable indicator species, dependent on their sensitivity to contaminants.
Acknowledgements This project was supported by funding from the Sydney Olympic Park Authority. The authors thank Ralph Alquezar for his assistance with the field sampling, Narelle Richardson and Gemma Armstrong for their advice on laboratory methodology, and Professor Margaret Burchett, Associate Professor Richard Lim, Edwina Laginestra and Dr Jenny Stauber for guidance on the experimental design of this study.
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