Qualitative Changes in Macroalgal Assemblages

Botanica Marina Vol. 45, 2002, pp. 130±138 # 2002 by Walter de Gruyter ´ Berlin ´ New York

Qualitative Changes in Macroalgal Assemblages under Two Contrasting Climatic Conditions in a Subtropical Estuary M. J. Ochoa-Izaguirrea, b, J. L. Carballob, c and F. Pez-Osunab, c* Facultad de Ciencias del Mar, Universidad AutÕnoma de Sinaloa, Paseo Claussen s/n, Mazatln, Sinaloa, Mexico Posgrado en Ciencias del Mar y LimnologÌa, c Instituto de Ciencias del Mar y LimnologÌa, Unidad Acadmica Mazatln, Universidad Nacional AutÕnoma de Mexico, Apartado Postal 811, Mazatln 82000, Mexico a

b

* Corresponding author: [email protected]

In this study, we examined the qualitative changes in macroalgal assemblages during the climatic phenomena of drought and rainy season in 45 sampling stations along Estero de UrÌas in the Gulf of California. The lagoon has a mouth that connects it to the ocean, but there is no continuous supply of fresh water, and physico-chemical characteristics are highly influenced by the contrasting weather in this region. The ratio of green algae versus total species per sampling station was used as an indicator of change in organic enrichment. The ratio was high during both seasons, and the nutrient concentration averaged 14.8 mg at N/L and 1.0 mM dissolved-P during the drought and 12.4 mg at N/L and 1.7 mM dissolved-P during the rainy season, showing that the estuary has constant high levels of nutrients in both seasons. However, the average number of species per sampling station, and the number of stations with macroalgae were both larger during the drought season, mainly with Ulva lactuca, U. lobata and Enteromorpha clathrata. In contrast, during the rainy season the assemblages in some parts of the estuary are dominated by red seaweeds such as Gracilariopsis sjoestedtii and Caloglossa leprieurii. Moreover, in spite of the drought season (when it is not possible to observe clear assemblages), during the rainy season four main groups of stations were established by means of a classification analysis based upon the number of species that occur in the different stations. It seems that during the drought the system is environmentally more homogeneous than during the rains, when there is a slight improvement of water conditions, and different environmental zones are established.

Introduction Estuaries are highly productive ecosystems that support numerous organisms adapted to this environment, such as macroalgae, which are considered the most important primary producers in shallow coastal waters (Neushul and Coon 1971). The macroalgae participate in carbon and nitrogen cycles (Darley 1982), recycle dissolved organic matter, help form and pack the substratum, and deter erosion (Scagel 1959). In estuaries, environmental factors like salinity, water temperature, and nutrients vary greatly throughout the year (Sfriso et al. 1988). These changes can be induced by anthropogenic activities or are related to natural processes (Valiela et al. 1992, Pedersen and Borum 1996). Environmental factors such as light, temperature and nutrients, among others, can limit macroalgal development, whether by excess or default, resulting in seasonal cycles of growth and reproduction related mainly to seasonal changes in such factors (Darley 1982). Thus, benthic vegetation has been used as an ecological quality indicator in different marine environments (Edwards 1972, Panayotidis et al. 1999, Hardy et al. 1993), relating aspects like community dynamics and struc-

ture (Josselyn and West 1985) to the effects of contamination or other environmental stress (Cox and Norton 1996). The UrÌas estuary is an internal coastal lagoon that is permanently connected to the ocean via a wide mouth. This valuable ecosystem is exposed to intensive human activity which causes an overenrichment by anthropogenic nutrients, altering its functions and properties. There is no continuous supply of fresh water, and the physico-chemical characteristics of the estuary are highly influenced by the contrasting weather in this region where there is a rainy and a drought season. Due to the complexity of the system, we intend to show only the most important qualitative changes in macroalgal assemblages during these two contrasting periods.

Material and Methods Study area and sampling The study area is located along the southeast coast of the Gulf of California, and includes the lagoon system known as Estero de UrÌas between 238 10' 36º and 238 13' 00º N and 1068 20' 00º and 1068 25' 35º W (Fig. 1).

Qualitative changes in macroalgal assemblages in a subtropical estuary

131

Fig. 1. Location of the study area showing the sampling stations.

Mazatln Harbor is situated in the lower and intermediate part of the coastal lagoon system. It has a surface area of 18 km2 and a length of 17 km. The port and fishing fleet are located along the first 3 km (from the mouth); urban waste and runoff from a thermoelectrical power plant, along with other fishing industries producing great quantities of organic waste, flow into the estuary from km 3 to 7 (from the mouth). The remaining length of the estuary's margins are dense with mangroves, and the upper part where a large shrimp farm is located receives shrimp pond effluents. The climate is tropical/subtropical, with two contrasting seasons of the year (GarcÌa 1973). The average annual temperature is 25 8C, average annual rainfall is 800 mm (occurring mainly during the rainy season), and salinity is 34.0 % (lvarez-LeÕn 1977). According to Pritchard (1967) this water body can be considered as an estuarine system during the rainy season (July± October) and an anti-estuarine system in the drought season (November±June). We selected 45 sampling stations along the estuary to include the greatest environmental and spatial diversity possible (Fig. 1). All the macroalgae present at each station were collected in April (drought season) and in October (rainy season), along two replicated 50-meter-long transects. Each transect was 4 m wide, and all species present within those perimeters were registered. Species were determined according to Abbott and Hollenberg (1976) and Wynne (1998), and

values for number of species were obtained. The authors for each species are indicated in Table I. Biotic and environmental heterogeneity The similarities among the sampling stations were established by means of a classification analysis, using the species present as variables in the established zones. The similarity matrix for the classification was calculated by means of the Sorensen qualitative index (Krebs 1989). This index was chosen as it does not consider the double absences, frequently found in our data base, in its calculations. The results were then graphically described using dendrograms with the unweighted pair-group method using arithmetic averages (UPGMA) aggregation algorithm (Sneath and Sokal 1973). An ordination analysis by means of a nonmetric multidimensional scaling program (MDS) was carried out based on the similarity matrix between stations (Kruskal and Wish 1978). The Kruskal stress coefficient was used in order to test the ordination obtained by the MDS (Clarke 1993). The Cox and Norton (1996) method (ratio of green algae versus total species found in one station) was used in order to determine those areas affected by environmental stress. In order to examine environmental heterogeneity three sampling stations were established along the

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Table I. Presence/absence of macroalgae at each sampling station. n

Chlorophyta Ulva dactylifera Setchell et Gardner U. lactuca Linnaeus d d U. lobata (Kçtzing) Setchell et Gardner Enteromorpha clathrata d r r (Roth) Greville E. flexuosa (Wulfen ex Roth) J. Agardh E. intestinalis (Linnaeus) Link r E. linza (Linnaeus) J. Agardh Chaetomorpha anteninna (Bory) Kçtzing Cladophora sp. C. microcladiodes Collins d r r Cladophoropsis sp. Rhizoclonium sp. r r Codium isabelae Taylor Bryopsis hypnoides Lamouroux Caulerpa sertularioides (S. G. Gmelin) Howe Ulothrix aequalis Kçtzing r

d d

d d

d d

d d d

d

d d

d d

d d d d

d

d

d d d

d d

d d d d d

d

d

d d

1

d dr r

dr dr d

r d d d

d d

d

16 d

d

2

d

d

8 3 1

d d

d

d

d

r

d

d

d r r

r

25 2

d d

dr

3 3 2 4 1 1 4 2

Phaeophyta Dictyota johnstoni Setchell et Gardner Dictyota sp. Padina durvillaei Bory Ectocarpus sp.

d

d

d

d d

d

d

d d r r d dr

9 1 3 1

d

Rhodophyta Stylonema alsidii (Zanardini) K. M. Drew Gelidium sclerophyllum Taylor Hypnea pannosa J. Agardh

r

d

r r r dr r

d

4

r

3 2

M. J. Ochoa-Izaguirre et al.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45

Table I. Continued 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 d

d d

d

d

d

d r r r

dr d dr r

r

r r r

r r

2

d

dr dr

d d

1

r

1 dr dr

2 6

r

1

d r

3

d

2

r r

d

r r d d

r d d

dr dr dr d dr dr dr r r dr dr r d dr r r dr dr dr r d

d

d

d d d

d

d

2 1 4 1 9 11

r

8

d

3 5 1

d d

The last column (n) shows the number of stations where each species appears. d: present in the dry season; r: present in the rainy season; dr: present in both.

15

d

r d

7 1

d


H. valentiae (Turner) Montagne Gelidiopsis tenuis Setchell et Gardner Gracilaria crispata Setchell et Gardner Gracilariopsis sjoestedtii d d (Kylin) Dawson Gymnogongrus leptophyllus J. Agardh Ahnfeltia plicata (Hudson) Fries Grateloupia abbreviata Kylin Antithamnion graffei (Grunow) DeToni Callithamnion paschale Bærgesen Centroceras clavulatum (C. Agardh) Montagne Ceramium caudatum Setchell et dr Gardner C. mazatlanense Dawson C. taylorii Dawson Ceramium sp. r Griffithsia pacifica Kylin Bostrychia sp. Caloglossa leprieurii (Montagne) J. Agardh Polysiphonia johnstonii Setchell et Gardner P. mollis Hooker et Harvey d P. pacifica Hollenberg r r dr Tayloriella dictyurus (J. Agardh) Kylin

n

133

134


estuary: E1, an area surrounded by mangroves next to a shrimp farm in the inner part of the estuary (average depth 0.5 m); E2, located in the middle of the estuary, is a mangrove area about 2 km from a thermoelectrical plant (average depth 1.2 m); E3 was next to the mouth of the estuary, located in front of a tuna fishing fleet, and close to seafood packing industries (average depth 0.8 m). Temperature and salinity were measured at each station every two weeks, and nitrites, nitrates, dissolved phosphorus (Strickland and Parsons 1972) and ammonium (Pez-Osuna et al. 1997) were measured 15 days before each sampling. Data on rainfall was provided by the ComisiÕn Nacional del Agua, CNA (1998) (National Water Commission).

at the mouth of the estuary had the greatest number of species in both seasons. The average number of species per station was greater during the drought (3 species) than during the rains (1 species), and the greatest number of stations without macroalgae were found during the rainy season (13). Layers of the bluegreen microalgae Microcoleus lyngbyaceus (Kçtzing) Crouan were found at stations 5 and 8 (drought season), and at stations 7 to 14 (rainy season), where little or no other macroalgae were found. On the other hand, during the drought season, there was the greatest number of stations with predominantly green algae (average close to 100 %, especially at the stations in

Results Environmental heterogeneity The rainy season lasted from June to October (Fig. 2), with a maximum rainfall of 395.8 mm in September (CNA 1998). The average temperature was 26.3 8C during the drought season and 31.5 8C during the rainy season (Fig. 3). Average salinity during the drought season was 39.4 % (maximum 45.5 %), and 31.7 % during the rains (minimum 9.0 %) (Fig. 4). The nutrient concentration was typical of eutrophicated systems (Ignatiades et al. 1992), averaging 14.8 mg at N/ L during the drought and 12.4 mg at N/L during the rainy season. The average value for the N:P ratio was greater during the drought season, and the average value for phosphates was greater during the rainy season (Table II). Species composition There were 44 species of macroalgae, 35 in the drought season (13 appeared exclusively in this season), 31 in the rainy season (9 exclusively), and 22 found present in both seasons (Table I, Fig. 5). Generally the stations

Fig. 2. Monthly precipitation during the sampling period.

Fig. 3. Water temperature (8C) at the three sampling stations.

Fig. 4. Salinity (%) at the three sampling stations.


the middle of the estuary) (Fig. 6). During the rainy season, red algae were prominent, although in some places in the middle estuary the percentage of green algae was maintained at levels similar to the ones found during the drought season. Those places are very close to the main urban sewage that flows into the estuary through the Infiernillo estuary (sampling stations 33±37), and have a very high content of a filamentous marine cyanobacteria of the genus Lyngbya, which can form mats covering the seabottom completely. The analysis for similarity found no clear assemblages during the drought season (Fig. 7a), contrary to the rainy season when 4 main groups were observed (Fig. 7b): Group A (19 % similarity) formed by the stations located in the external part of the estuary (stations 36±40 and 42); group B (28.59 % similarity) corresponds to stations located in the middle part of the estuary (stations 1±4, 34 and 35); group C (100 % similarity) formed by stations found mostly in the middle part of the estuary close to a thermoelectrical plant (stations 11, 13, 14, 26, 28±30, 32, 33, 43 and 44); and group D (84.30 % similarity) corresponds to the stations located in the inner part of the estuary (stations 15±17 and 19±25). The MDS ordination analysis (Fig. 7c) was carried out jointly on the total species in both seasons (stress = 0.12), and seems to indicate an environmental gradient from the mouth of the estuary towards the inner areas. A first group can be observed on the left, corresponding to the stations located at the estuary's entrance with mostly marine species. There is a second group formed by the stations in the middle area of the estuary where green algae are dominant and where there is a strong industrial activity; a third group of stations corresponds to the stations most inland with a wellestablished mangrove ecosystem nearby. At most stations the species found were different in each season, and only Ulva lobata, Padina durvillaei, Gelidium sclerophyllum, Grateloupia abbreviata, Gracilariopsis sjoestedtii and Antithamniom graffei appeared in both seasons. During the drought season the species that were most widely distributed were

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Fig. 5. Number of species at each station during the drought and rainy seasons.

Fig. 6. Green algae as a percentage of the total species found at each station.

Ulva lactuca (25 stations), Enteromorpha clathrata (14), Dictyota johnstonii (9) and Gracilariopsis sjoestedtii (8). During the rainy season Ulva lactuca was found at only one station, and the species Gracilariopsis sjoestedtii (11 stations) and Caloglossa leprieurii (10) were most widely distributed.

Table II. Nutrients. Variable

E1

E2

E3

Dissolved phosphorus (mM) Nitrites (mM) Nitrates (mM) Ammonium (mM) Total inorganic nitrogen (mg at N/L) N:P ratio

1.13±2.77

0.72±1.24

1.13±0.97

0.26±0.64 1.74±1.23 12.25±8.77 14.25±10.64

0.36±0.23 3.92±0.49 14.95±6.38 19.23±7.10

0.55±0.38 1.75±1.39 8.57±17.81 10.87±19.58

12.61±3.84

26.71±5.73

9.62±20.19

The first value corresponds to the dry season and the second value corresponds to the rainy season.

Discussion The changes in salinity are clearly related to the rainy season. The nutrient values, especially at the entrance and middle part of the estuary, were typical of eutrophicated systems (Ignatiades et al. 1992), possibly due to the nearby presence of anthropogenic effluents, as is also indicated by the percentage of green algae found in the middle part of the estuary in both seasons. Pez-Osuna et al. (1997) found that in the inner part of the estuary the average values for inorganic nitrogen were slightly higher during the drought (18.3 mM) than during the rains (16.8 mM), and that it was conversely

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Fig. 7. a±b: Dendrograms of stations based upon group average clustering using Sorensen similarity on the matrix of presence/ absence of species in the drought (no clear assemblages observed) and rainy season (four clear assemblages). c: Two dimensional nonmetric multidimensional scaling (MDS) plot of stations in both seasons based on a similarity matrix species established by Sorensen index (stress = 0.12). d: The four main assemblages of macroalgae are indicated on the map.

so for phosphates (1.4 mM during drought and 2.5 mM during rains). The N:P ratios are comparable to those found in other Mexican lagoons (De la Lanza 1994), and suggest that the nutrients were not limiting factors for the development of macroalgae. Generally, most species found in the estuary system are ephimerous algae (genera Ulva, Chaetomorpha, Cladophora and Ceramium) adapted to nutrient-rich environments (Pedersen and Borum 1996). The greatest number of species in both seasons was always found at the mouth of the estuary indicating that transition zones between different environments (estuarine vs. marine) are where the most diverse communities develop (Krebs 1985). Towards the middle and inner part of the estuary there is a change toward predominant green algae due to their tolerance of high levels of nutrients (Edwards 1972, Hardy et al. 1993). There were 35 species during the drought season and 31 species during the rains, the number of exclusive species was also greater during the drought season (13) than during the rains (9), with mostly green algae present. This is evidence that the macroalgal commu-

nity of the UrÌas estuary system is generally better adapted to the environmental conditions present during drought. The most representative species during the drought was Ulva lactuca, which practically disappeared during the rains (it was found only at station 42), and was substituted by Gracilariopsis sjoestedtii. This coincides with the observations of Alvarez-LeÕn (1977) for Ulva lactuca; in our case, however, the presence of Gracilariopsis sjoestedtii was prolonged until the drought season, and it was more consistent throughout time and space than Ulva lactuca. The results of the classification analysis during the rainy season indicate that the environmental factors that control the distribution of macroalgae in the UrÌas estuary define areas with a certain environmental homogeneity, which can be translated into a certain similarity in the specific composition of each zone. According to the results, the grouping of stations divides the estuary system into four biotic homogeneous areas (Fig. 7d), which seem to separate the system into four categories of ecological quality: Zone A), an area of transition between the marine and estuarine envir-


onments; zone B), located next to the El Infiernillo estuary where the influence of urban waste waters is greatest; zone C), located in the inner part of the system where the influence of a thermoelectric plant is greater, causing a notable increase in temperature in nearby areas; zone D), located in the most inland area of the estuary which is covered by mangroves and close to shrimp farms which also release waste waters. These results generally coincide with those found by AlvarezLeÕn (1977), who characterized this area as three zones according to morphology, sediments, coastal vegetation and fauna, as well as type of effluents dumped into the estuary. During the drought season, however, these results do not define such clear environmental areas, and when we analyze both periods together by means of an MDS analysis, we can only observe a slight gradient in the distribution of species from the entrance to the inner part of the estuary (Fig. 7c). The species responsible for the separation into groups as pointed out above could be considered

137

bioindicators for each environmental zone (Fig. 7d): Caloglossa leprieurii and Bostrychia sp., for zone A, Enteromorpha clathrata for zone B, Gelidium sclerophyllum and Antithamnion graffei for zone C, and Gracilariopsis sjoestedtii for zone D. There was also another environmental zone in the middle part of the estuary characterized by the presence of the greenblue microalgae Microcoleus lyngbyaceus.

Acknowledgements This work was carried out with funding from Unidad Acadmica Mazatln del Instituto de Ciencias del Mar y LimnologÌa, UNAM and was part of the Master Thesis of M. J. O. I. We thank H. BojÕrquez Leyva, G. RamÌrez Resndiz, M. C. RamÌrez Juregui and J. R. Ruelas Inzunza for their assistance in the laboratory and help in the preparation of the manuscript. Accepted 10 November 2001.

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